Clinical Anatomy and Physiology of the Visual System [4 ed.] 0323711685, 9780323711685, 2021936357, 9780323711692, 0323711693

Table of contents :
Contents
1 Introduction to the Visual System
2 Ocular Adnexa and Lacrimal System
3 Cornea
4 Sclera, Conjunctiva, and Limbus
5 Uvea
6 Aqueous and Vitreous Humors
7 Crystalline Lens
8 Retina
9 Ocular Embryology
10 Bones of the Skull and Orbit
11 Extraocular Muscles
12 Orbital Blood Supply
13 Cranial Nerve Innervation of Ocular Structures
14 Autonomic Innervation of Ocular Structures
15 Visual Pathway
Index

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2015v1.0

CLINICAL

ANA TOMY

and

PHYSIOLOGYof

VISUAL

the

SYSTEM

FOURTH

EDITION

Fourth

CLINICAL

and

ANN

Professor

Pacic

Forest

REMINGTON,

OD,

MS,

Emerita

University

ANA TOMY

PHYSIOLOGYof

VISUAL

LEE

Edition

FAAO

SYSTEM

DENISE

Professor

College

Grove, Oregon

of

Optometr y

the

Pacic

Forest

GOODWIN,

of

OD,

FAAO

Optometr y

University

College

Grove, Oregon

of

Optometr y

3251

St.

Riverport

Louis,

Lane

Missouri

CLINICAL

63043

ANATOMY

FOURTH

EDITION

Copyright

©

2022

by

AND

PHYSIOLO GY

OF

THE

VISUAL

SYSTEM,

ISBN:

Elsevier,

Inc.

All

rights

978-0-323-71168-5

reser ved.

No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical,

including

from

cies

the

photocopying,

publisher.

recording,

Details

and

our

arrangements

Agency,

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be

is

book

than

as

found

and

may

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be

on

on

with

our

or

to

any

seek

information

permission,

organizations

website:

individual

noted

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(other

herein).

Notices

Practitioners

and

researchers

must

always

rely

on

their

own

experience

and

knowledge

in

evaluating

and

using

any information, methods, compounds or experiments described herein. Because of rapid advances in the medi-

cal sciences, in particular, independent verication of diagnoses and drug dosages should be made. To the fullest

extent

or

of

the

damage

operation

Previous

Librar y

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digit

property

2012,

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Brian

assumed

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matter

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2005,

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products

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authors,

liability,

Kayla

1998

Wolfe

Kristen

Shereen

Helm

Jameel

Venkatachalam

Salisbur y

Canada

is

the

print

number :

9

8

7

6

5

4

3

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editors

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or

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2021936357

Specialist:

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P R E F A C E

Clinical

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images

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ture

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disease

clinical

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or

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“Clinical

emphasize

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common

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diseases,

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clinical

a

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anatomy

physiolog y.

clini-

on

the

Lee

Ann

Denise

Remington,

Goodwin,

OD,

OD,

MS

FAAO

vii

A C K N O W L E D G M E N T S

We

have

engaging

of

had

the

students

Optometr y.

enthusiasm

pleasure

while

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motivate

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kindness;

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also

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of

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with

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for

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warm

Kristen

Elsevier,

ness

extraordinar y

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Coyle

and

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Fraser

Horn

for

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constant

level of support they have provided and to the optometr y faculty

and

grateful.

tently

encouragement

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our

championed

tact

Wolfe,

combined

appreciate

the

throughout

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her

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whole.

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suggestions.

ix

C O N T E N T S

Preface,

vii

Acknowledgments,

1

Introduction

2

Ocular

3

Cornea,

4

Sclera,

5

Uvea,

6

Aqueous

7

Crystalline

to

Adnexa

the

Visual

and

System, 1

Lacrimal

System, 10

30

Conjunctiva,

and

Limbus, 53

62

and

8

Retina,

9

Ocular

111

ix

Vitreous

Lens,

Humors, 82

Embryology,

10

Bones

of

the

11

Extraocular

12

Orbital

13

Cranial

14

Autonomic

15

Visual

Skull

140

and

Muscles,

Blood

Supply,

Nerve

Orbit, 159

175

193

Innervation

Innervation

Pathway,

of

of

Ocular

Ocular

Structures, 208

Structures, 222

239

97 Index,

257

xi

CLINICAL

ANA TOMY

and

PHYSIOLOGYof

VISUAL

the

SYSTEM

FOURTH

EDITION

1

Introduction

from

the

anterior

portion

of

amount

of

entering

cess

of

of

light

sight

structures,

and

each

organization

of

and

analyzes

visual

of

perception

which

each

and

is

interprets

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involves

complex

designed

structure

for

enables

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system

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of

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light

bone

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a

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tissue

system

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carries

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to

view

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book

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well

nervous

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the

of

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macroscopic

components

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in

and

through

the

central

surrounding

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microscopic

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contains

terior

of

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uvea,

cell

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pupil.

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diaphragm

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posteriorly

posterior

posterior

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ciliar y

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body.

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behind

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e

is

and

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and posterior chambers are continuous with one another through

the

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duced

THE

the

exits the eye through the optic ner ve, and is transmitted to vari-

lens.

FEATURES

muscle

of

cesses, changes light energ y into a signal that can be transmitted

ment

ANATOMIC

the

part

rounds the retina and supplies nutrients to the outer retinal layers.

structures.

within

by

bin-

nutrients,

visual perception, inuences a myriad of decisions and activities.

omy

light

the

System

shape and diameter of the pupil and are supplied by the autonomic

the

motor,

surrounding

pathway

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and

that

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accurate

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Muscles

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blood

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produce

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embryonic

Visual

body, which produces the components of the aqueous humor and

e eye houses the elements that take in light rays and change

the

same

the

e visual system takes in information from the environment in

form

the

to

by

for

and

the

the

e

both

ciliar y

contain

body.

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particularly

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which

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the

is

pro-

nourish-

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space,

lies

and

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EYE cent to the inner retinal layer and is bounded in front by the lens.

e

of

eye,

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also

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layer

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up

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chamber

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view

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retina.

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exacting

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at

the

the vitreous

area

of

the

humor.

posterior

to

e

the

eye

lens

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through

change

the

shape

to

mechanism

of

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is

function.

throughout

all

a

vascular

Some

three

of

layer

the

of

the

eye,

histological

structures

and

are

AND

PLANES

science,

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specic

terminolog y

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basic to its discussion. e following anatomic directions should

Superior,

the

bring

rays

at

Anatomy

•

is

helps

allows

cornea,

a

•

region

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transparent

e

by

and

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light

uids

and

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conjunctiva

is

DIRECTIONS

•

retina.

in

globe,

the

refraction,

substance,

located

protec-

the

Anterior,

by

e

globe,

of

familiar

of

conjunctiva.

shape

•

and,

the

maintains

be

anterior

is

retina.

connective

opaque

gel-like

accommodation.

layer

structures

onto

that

ANATOMIC tion

a

lens

chamber and provides additional refractive power for accurately

focusing

middle

body,

3.

called

(Fig.

or

or

or

or

1.2):

ventral:

dorsal:

cranial:

caudal:

from

near

away

the

the

from

toward

toward

toward

away

the

the

the

from

front

back

head

the

head

midline

the

midline

point

the

of

point

origin

of

origin

1

CHAPTER

2

1

Introduction

to

the Visual

System

Iris

Cor nea

Anterior Exter nal

scleral

chamber

sulcus

Cor neoscleral

Bulbar

border

conjunctiva

Ciliar y

muscle

Ora

serrata

Pars

Ciliar y

plicata

body

Pars

plana

Medial

rectus

Lateral

rectus

Retina

Choroid

Fovea

Sclera

Lamina

cribrosa

Dural

sheath Long

posterior

ciliar y

ar ter y

Optic

ner ve

Shor t

Fig. 1.1

e

tures

•

following

(Fig.

•

Sagittal:

used

in

describing

anatomic

struc-

plane

dividing

the

sagittal

structure

into

C orona l

or

right

structure

plane

and

f ront a l:

dividing

running

t he

from

into

through

le

anterior

right

the

and

to

le

midline,

posterior

the

plane

st r uc ture

into

Axial

into

the

r unning

anter ior

f rom

and

side

to

p oster ior

entire

is

the

For

or

transverse:

superior

and

horizontal

inferior

plane,

parts.

ar teries

dividing

the

structure

are

is

locations

to

the

is

center

of

the

vitread

is

of

the

the

the

spherical

the

used

globe,

body

as

inner

globe,

the

mean

is

anterior

For

1.1).

outer,

other wise.

inner

sclerad

to

or

would

to

used

toward

references

references

point.

which

is

In

(see Fig.

specied

retina

term

structure,

confusing.

reference

to

unless

example,

a

be

ciliar y

referred

globe

addition,

and

globe

sometimes

cornea)

anterior

tures

halves.

ver t ica l

the

can

posterior

of

sides.

dividing

p ar ts.

•

B ecause

tions

vertical

Midsagittal:

side,

are

ciliar y

Horizontal section of the globe showing major components.

1.3):

locations,

•

planes

posterior

the

to

example,

the

e

lie

(i.e.,

the

layers

reference

point

within

sclera

(see

of

the

loca-

and

center

pupil

or

is

is

struc-

to

the

reference

vitreous.

Fig.

toward

vitreous.

to

anterior

pole

When

mean

the

to

1.1).

the

In

sclera,

CHAPTER

1

Introduction

to

the Visual

3

System

Sagittal

(median)

plane

Coronal

(frontal)

plane

Posterior

Superior

Inferior

Anterior

Axial

(horizontal)

plane

Lateral

Medial

Proximal

Distal

Fig. 1.3

R.

Anatomic

Anatomy

and

Heinemann;

lens

Fig.

1.2

ames

Anatomic

R.

Anatomy

directions.

and

worth-Heinemann;

(From

Human

Palastanga

Movement.

N,

Oxford,

Field

UK:

D,

So-

Butter-

1989.)

and

long,

(Fig.

in

cornea

1.4C).

of

are

CONDITIONS

If

power

Various

the

refractive

primarily

between

light

seen.

the

the

rays

come

is

rection,

into

condition

such

distance

cornea

cornea,

as

vision.

the

and

lens,

lens,

on

called

or

optical

and

focus

is

glasses

In

of

components

correlates

retina

the

so

retina,

a

emmetropia

contact

hyperopia

with

that

lenses,

the

the

clear

parallel

image

1.4A).

necessar y

(farsightedness),

the

eye,

distances

incoming

(Fig.

is

of

will

No

for

be

cor-

clear

distance

Myopia

the

eye,

is

section

structures

e

mine

the

retina

convex

the

(Fig.

lens

in

incoming

1.4B).

front

light

thereby

causing

Hyperopia

of

rays.

the

eye

can

to

images

be

to

focus

corrected

increase

the

by

behind

placing

convergence

In myopia (nearsightedness),

either

a

of

the

D,

Soames

Butter worth-

can

or,

rays

be

more

to

corrected

the

likely,

focus

by

in

the

placing

incoming

eyeball

front

light

of

a

the

is

concave

rays

to

too

retina

lens

diverge.

INSTRUMENTATION

briey

cur vature

the

corneal

are

used

to

assess

the

health

and

function

describes

some

of

these

instruments

and

the

of

the

cornea

refractive

is

one

power.

A

of

the

factors

keratometer

that

deter-

measures

the

cur vature of the central 3 to 4 mm of the anterior corneal surface

and

provides

automated

lens,

Field

UK:

examined.

of

and

strong

light

causing

instruments

cur vature

cornea

N,

Oxford,

of elements of the visual pathway and the supporting structures.

from the cornea to the retina is too short for the refractive power

the

too

parallel

OPHTHALMIC

REFRACTIVE

Palastanga

Movement.

1989.)

causing

front

planes. (From

Human

gives

is

an

information

between

corneal

indication

instrument

lenses

in

is

dicult

the

about

principle

topographer

of

an

the

power

and

meridians

maps

corneal

important

cases.

the

the

at

corneal

cur vature

adjunct

in

the

that

at

the

dierence

location.

surface

selected

tting

of

in

An

and

points.

contact

CHAPTER

4

1

Introduction

to

the Visual

System

retinal

uses

layers.

this

to

choroidal

OCT

angiography

produce

high

vasculature.

detects

resolution

is

does

not

motion

images

require

of

the

of

the

use

blood

and

retinal

and

of

injectable

dyes, and the images can be obtained within seconds. Additional

instrumentation

and

ner ves

parasitic,

A

e

and

and

visual

can

can

allow

aid

visualization

in

the

fungal

infection

eld

the

is

area

of

corneal

dierentiation

in

corneal

that

a

of

layers,

cells,

bacterial,

viral,

tissue.

person

sees,

including

those

areas seen in the peripher y. A perimeter is used to test the extent,

sensitivity,

and

perimeters

as

well

the

as

completeness

provide

statistical

probabilities

of

Neuroimaging

imaging

and

imaging

of

any

visual

on

eld.

maps

the

of

Computerized

the

reliability

visual

of

the

eld,

test

and

defects.

techniques,

globe,

this

detailed

information

computed

the

of

extremely

such

tomography,

orbit,

and

as

magnetic

allow

visual

resonance

increasingly

pathway

detailed

anatomy.

ese

B

images

provide

physiological

and

pathological

information

never before available. Having a basic understanding of the nor-

mal

anatomical

BASIC

Because

book

C

1.4

light

comes

parallel

A

Refractive

light

convex

light

rays

lens

comes

lens

is

focus

is

a

to

the

to

a

used

focus

to

used

on

a

comes

into

light

focus

to

conditions.

retina.

the

retina.

front

the

Emmetropia,

behind

correct

the

in

correct

retina.

the

focus

to

on

focus

on

A,

of

C,

Karl

which

Hyperopia,

retina

condition

Myopia,

retina

condition

(Courtesy

B,

the

in

(dotted

in

which

(dotted

lines).

and

in

paral-

bring

which

lines).

and

bring

the

Citek,

O.D.,

Pacic

A

light

the

parallel

many

All

of

Optometr y,

Forest

Grove,

body

is

inside

called

portion

the

of

the

fundus.

eye

is

level,

structures

this

details

section

of

are

discussed

briey

tissues

are

in

reviews

addressed

this

basic

in

the

structures

are

epithelial,

made

up

connective,

of

one

or

muscle,

more

and

of

the

ner vous

four

tissue.

ized

to

perform

a

common

function.

rays

into

Epithelial

Tissue

Universit y

tissue

oen

takes

the

form

of

sheets

of

epithelial

cells

Ore.)

surrounding

is

patholog y.

concave

either

cavity.

e

detecting

FEATURES

anatomical

Other

in

A tissue is dened as a collection of similar cells that are special-

that

ber

the

aid

chapters.

tissues:

Epithelial College

of

histological

histolog y.

pertinent

basic

will

HISTOLOGICAL

the

human

Fig.

lel

at

appearance

examined

the

vitreous

using

an

cham-

ophthalmo-

cover

the

Epithelial

external

cells

lie

on

a

surface

of

a

basement

structure

or

membrane

that

that

line

a

attaches

them to underlying connective tissue. e basement membrane

can

be

divided

the

optic

nerve

about

head,

and

ocular

and

blood

vessels

systemic

can

health

be

assessed

obtained.

is

is the only place in the body in which blood vessels can be viewed

is

directly and noninvasively. V arious systemic diseases, such as dia-

betes,

T o

hypertension,

obtain

drugs

are

a

more

and

arteriosclerosis,

complete

administered

to

view

of

inuence

the

the

can

alter

inside

iris

of

ocular

the

muscles,

vessels.

eye,

topical

causing

the

the

tissue

apical

or

surface,

rests

Epithelial

Squamous

height

on

cells

cells

and

Epithelium

thalmoscope

Endothelium

a

allows

of

biomicroscope.

stereoscopic

the

globe

is

and

viewing

the

of

eyelids

combination

of

an

the

fundus.

can

be

assessed

illumination

with

system

layer

layers

and a binocular microscope allows stereoscopic views of various

the

parts

cells

of

parent

of

the

eye.

ocular

auxiliar y

measure

the

obtain

provides

optic

ner ve

benecial

such

can

as

be

pressure

coherence

noninvasively

It

structures,

instruments

intraocular

Optical

tures.

Particularly

the

and

to

a

with

view

cross-sectional

and

can

view

and

the

the

(OCT)

three-dimensional

head

the

cornea

used

tomography

is

interior

image

the

lens.

the

A

trans-

number

biomicroscope

uses

mapping

measure

of

of

of

of

light

the

the

lamina,

secreted

thickness

of

cells

is

usually

in

the

and

and

the

to

a

consists

of

simple

name

stratied

surface

contact

platelike,

cavities.

with

layer.

the

is

cells

given

to

by

the

Only

higher

is

surface.

(Fig.

are

of

than

1.5).

equal

wide.

referred

to

as

simple

columnar.

the

simple

squamous

consisting

described

the

underlying

basal

cells

under-

or

Epithelium

is

the

shape

cells

cuboidal,

and

to

are

of

of

faces

the

cuboidal

layer

basement

columnar

that

according

single

special

as

surface

columnar

of

certain

referred

in

at

product

membrane

classied

squamous,

is

lines

the

a

basal

or

by

of

the

deepest

membrane,

and

several

shape

layer

this

of

of

layer

cells.

Keratinized, stratied squamous epithelium has a surface layer

eye.

of squamous cells with cytoplasm that has been transformed into

to

struc-

retina

is

are

lamina,

to

waves

optical

simple

that

are

width,

simple:

outside

whereas

basement

consisting

pupil to become enlarged, or mydriatic. A binocular indirect oph-

e

the

reticular

basal

lying connective tissue layer. e free surface of the epithelial cell

retina,

the

parts:

e

information

and

two

epithelial

and

cell,

into

scope, which illuminates the interior of the eye with a bright light.

and

specic

a

substance

resistant

ese

to

called

keratin,

mechanical

keratinized

a

tough

injur y,

surface

protective

bacterial

cells

material

invasion,

constantly

are

and

relatively

water

sloughed

o

loss.

and

are replaced from the layers below where cell division takes place.

CHAPTER

1

Introduction

to

the Visual

5

System

Simple

Squamous

Cuboidal

Columnar

Stratified

Squamous

nonkeratinized

Cuboidal

Columnar

Keratinized

Fig.

1.5

Types

delphia:

Many

epithelial

gathered

into

cells

groups,

of

epithelia.

Saunders;

are

are

20 07 ,

adapted

referred

to

for

as

p

(From

Gartner

LP ,

Hiatt

JL.

Color T extbook

of

Histology.

3rd

ed.

Phila-

87 .)

secretion

glands.

and,

Glands

when

can

be

(Fig.

tion

1.6).

of

Glands

their

can

also

secretion:

be

named

mucous,

according

serous,

or

to

the

composi-

sebaceous.

classied according to the manner of secretion—exocrine glands

secrete

through

endocrine

can

also

a

glands

be

duct

classied

duction—holocrine

secretor y

material;

plasm

the

is

a

in

product

the

the

directly

according

glands

cell

and

epithelial

into

to

secrete

apocrine

secretion;

of

onto

secrete

the

without

process

secrete

secretion

loss

of

surface,

any

whereas

bloodstream.

complete

glands

the

the

of

cells

part

of

Glands

secretion

laden

of

the

with

cell

merocrine

cellular

pro-

the

cyto-

glands

components

A

Connective

Connective

space

not

include

tissue.

Tissue

tissue

provides

occupied

bone,

ground

A

is

B

tissue.

tendons,

tissue

consists

combination

substance

structure

other

muscle,

Connective

substance.

by

called

of

and

blood,

of

of

bers,

protein

extracellular

C

Secretion

and

its

contents Intact

cell

(secretion)

New

cell

Pinched

portion

off

of

cell

(secretion)

Fig.

LP ,

1.6

Hiatt

Modes

JL.

of

glandular

Color T extbook

of

secretion.

Histology.

A,

3rd

Holocrine.

ed.

B,

Merocrine.

Philadelphia:

C,

Saunders;

Apocrine.

2007 ,

p

(From

105.)

and

and

bers

matrix.

Disintegrating

cell

and

Gartner

lls

connective

lymph,

cells,

insoluble

the

support

Types

the

tissue

adipose

ground

within

the

Connective

CHAPTER

6

tissue

sue

can

has

be

classied

relatively

nective

tissue,

as

fewer

in

1

Introduction

loose

cells

which

or

and

the

dense.

bers

cells

and

to

the Visual

Loose

per

area

bers

connective

than

are

System

dense

tightly

tis-

con-

packed.

myelinated

including

Dense connective tissue can be characterized as regular or irreg-

ing

ular

brain

on

the

basis

Among

the

broblasts

of

ber

cells

arrangement.

that

(attened

may

cells

be

that

found

in

produce

connective

and

tissue

maintain

the

are

bers

or

conduction

the

unmyelinated.

speed.

providing

extracellular

barrier.

central

and

physical

Microglial

in

cells

system.

number

in

have

and

homeostasis,

ner vous

increase

Myelinization

Astroc ytes

a

metabolic

and

ey

the

possess

of

of

maintain-

in

immune

the

or

blood

response

phagocytic

damage

impulse

functions,

support,

participating

mediate

areas

improves

number

in

properties

disease.

and ground substance), macrophages (phagocytic cells), mast cells

(which

tissue

contain

heparin

composed

and

primarily

histamine),

of

fat

cells

is

and

fat

called

cells.

Connective

adipose

BRIEF

REVIEW

OF

HUMAN

CELLULAR

tissue.

PHYSIOLOGY e bers found in connective tissue include exible collagen

bers

with

high

elastic

bers,

bers

are

tissue.

of

a

tensile

which

major

ese

e

amino

acid

because

various

are

e

bers

that

of

the

types

amorphous

glycans,

and

much

of

coiled

the

of

proteoglycans,

of

ocular

and

of

the

helix

of

chains

such

substance,

three

connective

can

polypeptide

dier

has

a

tissue

to

their

is

pat-

separated

and

several

structures.

which

bound

in

banded

Collagen

in

water

and

macromolecules

dierences,

connective

of

bers,

eye’s

protein

dierences.

consists

reticular

stretching. Collagen

tropocollagen

basis

ground

embedded,

of

polypeptide

the

components

are

a

sequence

on

delicate

extensive

composed

have

sequences,

into

types

are

individual

tern

strength,

undergo

component

bers

tropocollagen

chains.

can

the

cells

A

cell

glycosamino-

glycoproteins.

layer

layers

lular

face

area)

phobic

projects

Muscle

or

tissue

smooth

Striated

and

is

brane’s

and

may

muscle

is

a

of

its

muscle

located

control

of

and

control,

e

the

ber

be

is

of

and

tissue

control.

dark

cardiac

skeletal

elongated,

ner vous

striated

muscle.

discussed

is

autonomic

light

of

as

involuntar y

whereas

are

an

nucleus.

or

classied

cardiac

structure

contraction

smooth

can

pattern

skeletal

voluntar y

It

voluntar y

regular

into

centrally

untar y

tissue.

under

involuntarily.

mechanism

e

be

has

under

controlled

single

contractile

in

muscle

muscle

Chapter

slender

is

bands

Skeletal

cell

under

11.

with

the

is

and

brane.

a

system.

the

Nerve

are

tissue

both

tein

cells

that

to

two

react

the

several

that

axon,

gering

tic

impulse,

potential

a

to

types

a

of

cells:

stimulus

neurons.

e

cytoplasmic

at

in

a

the

reaches

excitator y

membrane

of

or

the

form

specialized

the

neurotransmitter

an

neurons,

and

conduct

which

a

nerve

neuron

cell

projections.

body,

e

called

projections

an

is

of

an

junction,

presynaptic

released

inhibitor y

second

action

into

potential,

a

synapse.

membrane

the

of

synaptic

response

in

the

passes

As

the

gap,

the

rst

trig-

postsynap-

neuron.

astrocytes,

neuroglial

extensions

encircle

cell

of

ner ve

rial

and

in

microglial

the

bers

cells.

peripheral

Schwann

and

the

area)

of

each

a

of

a

hydrophobic

phospholipid

inside

the

(intracel-

cell.

A

hydro-

phospholipid

membrane.

Other

on

layer

Cholesterol

be

molecules.

the

mol-

outside

embedded

the

bers

the

largest

and

of

be

in

both

cell

mem-

surfaces

proteins

have

of

por-

cell.

(cytosol)

may

Carbohydrates

extracellular

membrane-spanning

are

the

cell

contains

and

are

tissue

actin

various

composed

specic:

and

myosin

neurolaments

structure

cellular

its

e

and

in

e

genes

of

keratin

bers

protein

the

pro-

bers

in

neurons.

acid

of

and

control

most

the

e

the

of

the

for

in

sar-

c yto-

genetic

which

proteins

acid

as

intra-

the

is

cell,

mate-

organized

chromosomes

ribonucleic

manufacture

provides

center

(DNA),

within

granules

cytoplasm,

support

the

contains

deoxyribonucleic

Ribosomes,

the

and

nucleus,

function

chromosomes.

provides

and

are

the

proteins

directed

by

the

to

cells

form

in

a

Schwann

ner vous

the

system.

peripheral

myelin

cells

sheath,

are

the

only

Cytoplasmic

ner vous

system

and oligodendro-

steroid

optic

ner ve).

Ner ve

bers

thus

are

either

protein

and

lipid

ribosomes

powerhouse

the

the

form

where

of

of

and

lipid

synthesis.

and

is

of

synthesis.

Rough

involved

in

Smooth

endoplas-

endoplasmic

producing

them

enzymes,

down

into

Fluid

into

the

and

passively

up

cytoplasm

by

is

occur

intracellular

take

the

transport

diusion

that

reticulum

proteins.

result

or

old

across

a

a

cell

of

inner

cisternae.

in

e

energy

wall

of

is

is

the

production

systems

containing

organelles

that

transported

down

supply

e

into

digestive

molecules

and

cell’ s

(ATP).

folded

bacteria

component

solute

either

produce

triphosphate

processes

Lysosomes,

powerful

cell,

mitochondria

biochemical

ATP .

the

adenosine

double-walled

are

out

and

reused

of

the

reab-

cell.

membrane

concentration

break

or

can

occur

gradient

or

by

facilitated diusion using membrane transport proteins (Fig. 1.8).

Molecules

with

the

tion

the

for

Golgi apparatus modies and packages proteins. Mitochondria,

occurs

for

sites

mic reticulum does not have embedded ribosomes. It is involved

ing

myelin

both

from

soluble

may

c ytoplasm

transport.

within

into

c ytes do the same in the central ner vous system (including form-

the

of

gives

sorbed

Neuroglia in the central ner vous system include oligodendro-

cytes,

and

inside

cellular

cellular

in

action

molecules

muscles,

the

ner ves

composed

skeleton is a three-dimensional scaolding within the cytoplasm

jection that conducts impulses away from the cell body is an axon

between

is

hydrophilic

on

the

coating

coplasm

that conduct impulses to the cell body are dendrites, and the pro-

ner ve

of

water

microlaments

houses

A

to

glycocalyx

epithelium,

in

support

has

a

tubulin.

metabolic

soma,

two

extending

center

Microtubules

impulse, and neuroglia, which are cells that provide structure and

the

the

e

solutions

and

cellular DNA. e endoplasmic reticulum within the cytoplasm

encompasses

specialized

1.7).

cell

surrounding

(extracellular

chain

bilayer,

genome.

Tissue

acid

permeability

lipid

within

Nerve

outside

Protein

directs

invol-

and

toward

form

bers.

subdivided

muscle

the

is

(Fig.

aqueous

each

lipids

ecules found in the central fatty acid portion decrease the mem-

tions

Tissue

surrounds

hydrophilic

area

the

fatty

e

Muscle

of

intermediate

may

and

membrane

double

can

use

of

when

and

no

be

transported

active

molecules

energy

against

transport,

is

pass

the

which

from

expended.

a

concentration

requires

higher

to

Facilitated

a

energy.

lower

diusion

gradient

Diusion

concentra-

may

occur

CHAPTER

Extracellular

1

Introduction

to

the Visual

7

System

space

Glycoprotein Glycolipid

Outer

leaflet

Inner

Cholesterol

leaflet

Fatty

acid Integral

tails Peripheral

protein

Channel protein

Polar

head

Cytoplasm

Fig.

3rd

through

within

channel

the

cell

intracellular

ion

Model

proteins

or

the

carrier

create

extracellular

across

of

Philadelphia:

membrane

and

movement

1.7

ed.

the

lipid

cell

membrane.

Saunders;

proteins.

water-lled

spaces.

bilayer

p

Channel

passages

ese

and

20 07 ,

proteins

linking

channels

move

ions

(From

Gartner

LP ,

the

facilitate

without

the

cellular

inside

matrix

then

using

cesses

gates.

V oltage-gated

a

channels

neurotransmitter

or

channels

open

a

when

a

nucleotide

open

with

signaling

like

depolarization.

molecule,

cyclic

such

guanosine

as

mono-

that

into

is

aerobic

ecient,

molecule.

cilia

deformation.

Some

of

Histology.

channels

are

of

by

36

to

glucose.

regulated

Integrins

activate

ATP

the

of

for

f rom

either

either

that

produced

yields

is

more

per

two

pro-

through

metabolism

ATP

glycolysis

extracellular

enzymes

metabolic

produced

Aerobic

molecules

Anaerobic

f rom

Energ y

molecules,

metabolism.

signals

membrane-spanning

intracellular

processes.

38

by

are

information

and

cellular

anaerobic

with

are

cell.

carr y

cell

supplied

or

with

like

T extbook

and

the

can

the

inuence

ecule

contact

Color

outside

phosphate, binds to the channel. Mechanical-gated channels open

physical

JL.

metabolism

or

proteins

expenditure of energy. e channels control entrance into the cell

Ligand-gated

Hiatt

16.)

mol-

ATP

per

+

not gated, such as potassium (K

) channels or aquaporins, and are

always open. Transport across a cell membrane using carrier pro-

INTERCELLULAR teins

requires

transferred.

between

method

e

the

is

internal

carrier

such

and

as

sites

proteins

intracellular

slower

Molecules,

binding

and

the

never

ion

form

but

and

can

amino

or

a

extracellular

selective

glucose

for

molecule

direct

connection

environments.

carry

acids,

larger

are

is

molecules.

moved

in

this

Intercellular

and

to

tions.

Tight

or with the use of energy (active transport). e most well-known

mosomes),

+

porters

and

tration

are

diering

the

ATPase

substances

steady

supply

apical

oen

and

and

contain

pump.

against

of

ATP .

basal

ion

Here,

the

trans-

may

concen-

Transporting

membranes

channels;

have

however,

Gap

by

junctions

permitting

cells.

Physical

ATPase pumps are generally located in the basolateral

Aquaporins

intrinsic

not

allow

are

proteins

other

bidirectional

that

specically

materials

to

pass

channels

allow

composed

water

through

the

passage

channel.

junctional

allow

one

types

connections

zonula

macula

form

communication

of

changes,

factors,

proteins.

environment

intracellular

With

to

another

of

junc-

between

occludens

adherens

anchoring

and

(des-

junctions

ions

such

can

and

as

between

small

pressure

modulate

adjacent

molecules

and

cells

between

biochemical

junctions

and

alter

or

the

tight

Ridgelike

fuse

with

maintain

body

the

lipids

epithelia,

metabolic

viability

are

used

myriad

of

of

as

components

and

retina.

functions

or

the

cell.

building

are

biochemical

are

complex

Amino

blocks

broken

in

down

pathways

acids,

and

the

as

a

activities

that

carbohydrates,

construction

source

processes

of

of

energ y.

function

in

ing

cell.

branes

the

of

one

allows

cell

As

are

the

elevations

paired

fused.

that

to

changes

the

in

interior

junctions,

comes

on

complementar y

cytoskeleton

barrier

is

relayed

(occluding)

bor.

ciliary

C ellular

be

the

cell

extracellular

and

may

aect

processes.

lens,

A

include

adherens,

to

main

fused

hemidesmosomes

passage

pharmaceutical

membrane

cellular

form

cells,

Z onula

cells

three

between adjacent cells or between the cell and the basal lamina.

Aquaporins are numerous in ocular tissues, including the cornea,

and

are

+

/K

move

a

and

Both

Na

which

adjoining

occludens.

epithelial

ere

+

/K

major

but

the

need

polarized

membranes.

of

and

properties.

+

the Na

is

cotransporters

gradient

epithelia

pump

of

join

tissue.

junctions,

membranes

macula

transport

junctions

adjacent

way. Carrier proteins can function passively (facilitated diusion)

active

JUNCTIONS

being

e

the

bers

of

the

on

meet,

tight

cell.

passage

the

outer

direct

of

the

the

of

the

surface

with

cell

of

forms

unwanted

are

an

of

the

its

cell

neigh-

membrane

a

neighboring

junctions

is

leaet

contact

surface

ridges

strands

within

prevents

into

neighbor-

cell

mem-

connected

to

impermeable

material

between

CHAPTER

8

1

Introduction

Passive

to

the Visual

System

Transport

Extracellular

space

Plasma

Uniport

membrane

Simple

of

diffusion

Ion

lipids

channel-mediated

Carrier-mediated

diffusion

diffusion

Facilitated

diffusion

Cytoplasm

A

Active

Transport

Extracellular

space

Symport

Antiport

Coupled

Cytoplasm

transport

B

Fig.

adjacent

cells.

junctions

with

row

space.

of

Histology.

the

the

A

substance

cells

cells.

are

pass

substance

A,

energy

Passive

requiring

Philadelphia:

a

belt-like

portion

1.9).

of

In

these

occlude

through

a

must

pass

zone

2007 ,

tight

a l lows

t he

epithelium

between

the

cell.

In

c el l

e nt i re

e st

t he

its

origin

the

formed

in

in

surface,

by

a

of

Z onu l a

junc t ions

branes

t hat

are

be

nally,

proteins

in

is

in

and

function.

components

as

a

when

cell

the

complete.

the

zonula

A

tight

from

reaches

complex

occludens

diseases,

macula

the

cell

e

blood-aqueous

some

of

moves

barrier.

causing

occludens

aids

e

dys-

junction

shape.

bind

a

ence.

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cel ls

mac u l a

toget her.

le av i ng

g lycoprotei n

a

ad herens

T he

are

adj ac e nt

nar row

mater i a l.

anchor ing

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to

of

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Color T extbook

cel l

to

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sp ac e

tive

ar range me nt

e

cell

f rom

in

a

of

and

its

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1.9B).

t he

t he

t he

f rom

z onu l a

z onu l a

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at

t he

sp ace

t he

toget her

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t he

of

c y topl as m

lin kers ,

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a

ac i d - r ich

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Fig .

c ytopl as m

t he

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and

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and

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site

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t he

just

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d espite

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basement

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extend

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pl aque

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Fig .

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the

t he

pl as ma

intercel lu l ar

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f i l aments

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ap ex

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the

the

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LP ,

microf i l aments

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found

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1.9A).

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sloughed and replaced from below, zonula occludens, if present,

located

constantly

require

subst ances

rel at ively

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passing

not

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18.)

on

of

row

it

p

does

(From

is

be

is

that

intercellular

through

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zones,

the

by

Saunders;

cell,

sheet

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surface

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transport

mechanism.

s ome)

junction

the

an

forms

(Fig.

zonula

where

is

eectively

cannot

by

transport.

ed.

apical

cells

ridges

the

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3rd

occludens

joined

Instead

stratied

of

transport

entire

adjacent

intertwining

whose

the

of

Types

Active

Zonula

around

each

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1.8

B,

contain

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a

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membrane

similar

extends

connection

and

underlying

components

through

the

to

cell

between

connec-

desmosomes.

membrane

to

CHAPTER

1

Introduction

to

the Visual

9

System

ZO

ZA

ZO

ZA

DESM B

Connexin

MO

Connexon HEMI-DESM

Cell

Cell

1

BM

“Gap”

A

1.9

Zonula

fusing

Intercellular

occludens

the

into

the

its

cell

one

to

joins

the

the

join

tive

keratin

tissue

teins,

in

the

at

the

central

basement

intracellular

matrix,

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the

oen

Macula

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MO,

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no

of

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C,

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la-

in

called

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embedded

lateral

the

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that

by

span

a

group

the

cell

of

(usually

membrane

six)

and

pro-

unite

and

zonula

(~2nm)

strong,

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of

(see

from

the

generally

Six

zonula

a

proteins

nuclei.

a

with

bers

aspect

lie

of

adjacent

(connexins)

occludens.

1.9C).

cell

cells.

without

HEMI-DESM,

neighboring

Fig.

like

cells

basal

desmosome;

one

act

adjacent

joins

junctions

join

communication,

connections

tiple

cells.

ZO,

connexins

cell-to-cell

that

DESM,

connexon

ions

spot-like

adherens

two

of

adherens

junctions

adherens;

with

membranes

Zonula

membrane;

and

are

cell

present.

form

Basal

tissue.

junctions

space

occludens

Gap

occludens;

underlying

The

(desmosome)

(connexon). BM,

macula

the

A,

intercellular

adherens

membrane.

channel

to

complexes.

Hemidesmosomes

membrane.

plaque

attaching

with

cytoplasm.

hemidesmosomes;

to

cells

basement

another

surround

junctional

membranes.

extending

to

ments

between

C

Fig.

attach

2

to

cell

ese

that

is,

another.

syncytium,

forming

narrow

passage

A

that

of

group

is,

a

a

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channels

small

of

cells

single

called

allow

cell

rapid

molecules

with

such

with

mul-

2

Ocular

e

to

of

ocular

the

and

adnexa

globe.

the

tem,

is

eyelids,

which

an

Adnexa

includes

chapter

the

of

a

system

structures

discusses

palpebral

consists

excretor y

the

and

the

for

situated

eyebrows,

conjunctiva,

secretor y

tear

Lacrimal

and

system

in

proximity

nasal

bone

the

structures

pulls

the

the

for

System

lacrimal

tear

sys-

production

drainage.

duces

and

inserts

medial

horizontal

cularis

brow.

oculi

e

into

portion

furrows

(described

bers

of

the

of

over

in

medial

the

the

more

these

side

eyebrow

bridge

detail

muscles

of

the

frontalis.

inferiorly

of

the

later)

blend

and

nose.

lowers

with

e

the

one

It

pro-

orbi-

entire

another

1

and

are

dicult

ner ve—cranial

EYEBROW

e

consist

of

thick

skin

covered

by

usually

horizontally.

ner ve

All

are

inner vated

by

the

facial

VII.

characteristic

EXTERNAL prominent

margin,

separate.

FEATURES

eyebrows

short,

to

In

hairs

extending

arching

general,

across

slightly

but

in

the

men

the

superior

sometimes

brows

run

merely

along

FEATURES

OF

THE

EYELIDS

orbital

running

the

orbital

e

eyelids,

closed,

or

cover

palpebrae,

the

globe.

are

e

folds

of

eyelids

skin

have

and

tissue

four

that,

major

when

functions:

1

margin,

e

whereas

rst

in

body

hairs

those

of

women

the

produced

brows

during

run

above

the

embr yological

margin.

(1)

develop-

tures

they

cover

that

the

globe

produce

the

for

tear

protection,

lm,

(3)

on

(2)

they

opening,

contain

they

struc-

spread

the

1

ment

are

e

muscles

cerus,

eyebrow

expression

scalp

orbital

brow,

(Fig.

and

rim.

a

on

in

tear

the

movements,

2.1).

e

into

bers

look

the

forehead—the

superciliaris,

inserts

e

causing

originates

eyebrow.

located

corrugator

produce

the

the

are

of

an

and

impor tant

frontalis

muscle

connective

oriented

surprise

inferomedial

tissue

element

near

and

attention.

frontal

in

bone

the

and

facial

high

on

over

the

anterior

surface

of

the

eye,

and

(4)

superior

muscle

of

to

the

trouble

obliquely.

It

medial

or

moves

eyebrow.

concentration,

the

brow

It

is

and

the

eye-

corr ugator

inserts

down

and

characterized

its

bers

are

medially,

closure,

they move the tears toward drainage areas at the medial canthus.

On

closure,

whereas

closed

the

the

upper

lower

gently,

the

eyelid

eyelid

eyelids

moves

rises

only

should

down

to

slightly.

cover

the

cover

When

entire

the

the

cornea,

eyes

are

globe.

into

Palpebral

e

e

Fissure

palp ebral

average

ssure

vertical

is

the

area

palpebral

between

ssure

the

height

is

open

as

the

oriented

toward

the

11

mm

in

numerous

eyelid

Caucasians

variations

margins

to

and

exist

the

8.5

in

the

limbus

mm

in

(the

4

Asians.

positional

eyelids.

approximately

3

skin

on

superior

raise

e

pro-

oculi—

originates

ver tically

or

f rontalis,

orbicularis

lm

Although

relationship

junction

of

the

of

cornea

the

and

2

nose,

creating

cer us,

the

vertical

muscle

of

furrows

menace

between

or

the

aggression,

brows.

e

originates

pro-

on

the

sclera),

by

1.5

generally

to

2

mm

the

upper

when

the

eyelid

eyes

covers

are

open

the

superior

and

looking

limbus

straight

5

ahead.

eyelid

as

e

distance

margin

the

between

while

margin

to

the

reex

the

corneal

patient

is

distance,

in

is

reex

and

primar y

the

gaze,

approximately

upper

known

5

mm

in

Frontalis

Caucasians,

4.5

mm

in

African

Americans

and

L atinos,

and

6

Orbital

of

4

portion

mm

usually

Procerus

e

within

1

lower

mm

of

eyelid

the

position

inferior

is

more

variable,

limbus.

ssure

in

the

lateral

and

medial

canthi.

e lateral

canthus

portion Corrugator

of

Asians.

lying

e upper and lower eyelids meet at the corners of the palpe-

bral

Palpebral

in

7–9

orbicularis

is

located

approximately

5

to

7

mm

medial

to

the

bony

orbital

orbicularis 9

margin

and

is

in

contact

with

the

globe.

e

medial

canthus

is

at the medial orbital margin but is separated from the globe by a

reser voir

of

the

row,

for

the

lacrimal

pooling

lake

is

crescent-shaped

canthus

allows

for

of

tears,

the plica

fold

lateral

of

the lacrimal

semilunaris

conjunctiva,

movement

of

lake.

(Fig.

located

the

eye

At

2.2).

in

the

oor

is

the

without

nar-

medial

stretch-

ing the bulbar conjunctiva. e caruncle is a small, pink mass of

modied

Fig.

are

10

2.1

Forehead

called

the

muscles

muscles

of

that

control

expression.

the

eyebrows. These

skin

located

just

medial

to

the

plica

semilunaris.

It

is

covered with epithelium that contains goblet cells, as well as ne

hairs

and

their

associated

sweat

and

sebaceous

glands.

CHAPTER

2

Ocular

Adnexa

and

Plica

Lacrimal

11

System

semilunaris

Caruncle

Lacrimal

punctum

Papilla

Cilia

Fig.

2.2

Structures

located

in

left

medial

canthus.

the orbital septum and orbicularis muscle descends lower into the CLINICAL

COMMENT: Lagophthalmos 10

1

eyelid

eliminating

the

superior

palpebral

11–15

sulcus.

Lagophthalmos refers to an incomplete closure of the eyelids (Fig. 2.3). Its cause

In may

be

physiological,

mechanical

(e.g.,

scarring),

or

paralytic.

the

lower

most

evident

during

sleep,

when

drying

of

the

inferior

cornea

may

occur.

irritated

Clinical

epithelial

eyes

are

assessment

disruption,

evident

of

the

on

awakening,

inferior

manifesting

as

cornea

staining

and

will

with

punctate

show

keratitis

varying

uorescein

the

lower

distinct.

palpebral

sulcus,

lid

into

tarsal

and

orbital

parts,

is

which

oen

e

tarsal

portion

rests

against

the

globe,

and

not

the

can

degrees

of

orbital

the

dye.

portion

cheek,

nasojugal

the

Eyelid

inferior

result.

ver y Scratchy,

the

Lagophthalmos

separates is

eyelid,

extends

extending

and

just

malar

attachment

of

from

past

sulci

the

the

the

(see

skin

lower

to

border

inferior

Fig.

the

2.4).

of

the

orbital

ese

underlying

tarsus

margin

furrows

onto

to

the

occur

connective

at

tissue

Topography and

become

more

prominent

with

age.

e upper eyelid extends to the eyebrow and is divided into tarsal

and orbital or preseptal parts. e tarsal portion lies closest to the

Eyelid lid

margin,

rests

on

and

the

the

globe,

and

contains

the

tarsal

plate.

e skin

is

thin,

underlying

loose

connective

tissue

is

eyelid

adipose

tissue.

e

orbital

portion

extends

from

the

tarsus

and

eyebrow,

and

a

furrow—the

superior

palpebral

the

rests

pores

against

of

the

the

globe

meibomian

and

contains

glands.

e

the

cilia

eye-

(eye-

to lashes)

the

margin

devoid lashes

of

Margin

e

are

arranged

at

the

lid

margin

in

a

double

or

triple

row,

sulcus— with

approximately

150

in

the

upper

eyelid

and

75

in

the

lower

separates the tarsal portion from the orbital portion (Fig. 2.4). is 16

eyelid.

e

lashes

curl

upward

on

the

upper

and

downward

on

sulcus separates the pretarsal skin, which is tightly adherent to the the underlying

tissue,

from

the

preseptal

skin,

which

is

only

lower

to

its

underlying

tissue

and

may

contain

a

Replacement

lashes

grow

to

full

size

in

approxi-

loosely mately

adherent

lid.

cushion

10

weeks,

and

each

lash

is

replaced

approximately

ever y

of 9

5 fat.

In

eyelids

of

those

of

Eastern

Asian

descent,

the

fat

months.

e

eyelashes

are

richly

supplied

with

ner ves,

caus-

between ing

them

which

to

will

asis

sensitive

elicit

CLINICAL

Various

be

than

even

protective

the

away

diseases

growth

from

can

of

the

slightest

response—a

COMMENT: Conditions

epithelial

(misdirected

rather

a

to

cause

eyelashes,

palpebral

in

which

ssure).

touch,

blink.

Affecting

madarosis

unexpected

the

(loss

the

Contact

Cilia

of

eyelashes)

eyelashes

between

or

grow

the

trichi-

toward

eyelashes

and cornea can cause irritation and painful abrasions and can lead to corneal

ulceration.

Receptors

The

for

problem

lashes

prostaglandin

can

be

analogs

removed

have

by

been

epilation.

found

in

the

bulb

and

stem

17

of

eyelash

follicles.

When

these

receptors

are

inuenced

by

prostaglandin

analogs, increased growth and pigmentation of eyelashes occur. Prostaglandin

analogs

e

Fig.

2.3

close.

Lagophthalmos

of

the

left

eye. The

eyelids

do

not

fully

the

are

type

pores

cilia

tiva,

a

the

(Fig.

of

of

medication

the

commonly

meibomian

2.5A),

and

mucocutaneous

the

used

glands

to

are

transition

junction

treat

(line

located

from

of

glaucoma.

skin

Marx),

posterior

to

to

conjunc-

occurs

just

CHAPTER

12

2

Ocular

Adnexa

and

Lacrimal

System

Orbital

portion

Superior

Malar

of

eyelid

palpebral

sulcus

sulcus

Tarsal

Nasojugal

Fig.

portion

of

eyelid

sulcus

2.4

Surface

anatomy

A

of

the

eyelids.

B

Fig.

2.5

samine

posterior

to

these

Eyelid

green.

openings

margin.

A,

Meibomian

(Courtesy T racy

(Fig.

2.5B).

A

Doll,

groove

gland

O.D.,

called

orices;

Pacic

the

gray

B,

University

mucocutaneous

College

GROSS

of

junction

Optometr y,

ANATOMY

stained

Forest

OF

with

Grove,

THE

lis-

Ore.)

EYELID

line runs along the eyelid margin between the cilia insertions and

Orbicularis the

pores

of

the

meibomian

glands.

is

groove

is

the

location

a surgical plane that divides the eyelid into anterior and posterior

e

portions.

below

e

eyelid

one-sixth

the

a

ciliar y

small

ing

is

2.2).

to

the

can

lacrimal

portion.

carries

Fig.

medial

the

elevation

that

(see

margin

e

be

divided

portion,

division

containing

the

tears

Usually,

no

punctum,

the

cilia

along

and

two

the

occurs

the

into

into

at

lacrimal

parts:

lateral

the

or

lacrimal

meibomian

lacrimal

medial

ve-sixths

punctum,

nasolacrimal

the

the

pores

striated

the

encircles

bers

of

the

subcutaneous

the

palpebral

orbicularis

connective

ssure

and

oculi

tissue

muscle

layer.

extends

are

located

e

muscle

from

the

eyelid

is

open-

system

are

of

Muscle

papilla,

the

drainage

portion

Oculi

of

found

the

eyelid

margin.

CLINICAL

Epicanthus,

COMMENT: Epicanthus

or

an

epicanthal

fold,

is

a

vertical

fold

of

skin

at

the

nasal

canthus

arising in the medial area of the upper eyelid and terminating in the nasal can-

thal

area

(Fig.

2.6).

It

is

common

in

newborns

and

may

cause

the

appearance

of esotropia. A parent of an infant with an epicanthal fold might worry that the

child's

eyes

As

bridge

An

the

are

epicanthal

of

crossed;

the

fold

however,

nose

is

a

develops,

common

in

cover

the

those

test

will

epicanthal

of

Asian

identify

fold

a

true

gradually

descent

because

esotropia.

disappears.

there

is

no

Fig. connection

between

18

orbicularis

the

upper

and

lower

preseptal

portions

of

the

2.6

Epicanthal

fold

may

gi ve

rise

to

pseudoesotropia.

palpebral

(From

Kanski

JJ,

Nischal

KK.

Ophthalmology:

Clinical

muscle.

Differential

Diagnosis.

St

Louis:

Mosby;

1999.)

Signs

and

CHAPTER

Fig.

is

2.7

Medial

composed

dial

orbital

laterally

to

of

canthal

margin

the

Larrabee WF .

structures.

semicircles

and

lateral

of

medial

canthal

Anatomy

of

The

muscle

canthal

tendon.

the

eyelids

orbicularis

bers

oculi

originating

tendon.

(From

The

Most

[review].

Ocular

the

Fig.

me-

Mobley

overlap

onto

the

orbital

margin.

It

is

the

globe

xed

to

bones

by

the

orbicularis

retaining

ligament.

e

be

divided

Palpebral

into

Portion

two

of

regions:

the

palpebral

Orbicularis

and

and,

after

unless

trauma

if

are

more

tissue

Orbital

Muscle

Portion

superiorly

to

margin.

notch

Fig.

is

divided

the

further

structures

that

into

the

pretarsal

divisions

and

preseptal

overlie.

e

parts,

palpebral

portion is composed of semicircles of muscle bers originating at

the

medial

orbital

margin

and

medial

canthal

tendon

(Fig.

attaching

to

the

lateral

canthal

tendon

common

can

may

in

the

cause

also

a

corneal

cause

lower

abrasion.

entropion.

eyelid

and

can

Scarring

Both

be

of

ectropion

corrected

the

and

The

anatomic

relationship

of

the

muscular

and

surgi-

connec-

is

an

important

consideration

when

repair

is

done.

laterally.

e

orbital

area

(see

outer

orbital

of

the

portion

the

to

of

the

orbital

10.7).

the

margin,

Orbicularis

to

just

concentric

palpebral

medial

orbicularis

margin,

e

Muscle

portion

the

oculi

medial

muscle

to

circular

and

is

attached

supraorbital

bers

attach

infraorbital

the

encircle

inferiorly

at

the

the

foramen.

2.7)

19

and

disease

components

e

It

ectropion.

orbital.

area of the eyelid that rests on the globe and is closest to the eyelid

for

Involutional

relieved,

or

necessary.

e palpebral portion of the orbicularis oculi muscle occupies the

named

2.8

muscle tive

can

13

System

the cally,

orbital

Lacrimal

SR,

2005;13:488.)

entropion

to

and

attach

eyelid

margin

Adnexa

muscle

at

bers

SP ,

2

supe-

Orbicularis

Action

20–22

rior

and

inferior

Deep

muscle

palpebral

bers

fuse

orbicularis

with

bers

one

arise

another

from

laterally.

attachments

23

the

posterior

tion

of

the

lacrimal

palpebral

crest

and

part

of

medial

the

orbital

on

VII

orbicularis

(the

facial

oculi

muscle

ner ve).

is

inner vated

Contraction

of

the

by

cranial

palpebral

ner ve

portion

of

24

wall.

orbicularis,

e

is

Horner

sec-

muscle,

the

orbicularis

bral

orbicularis

and

a

closes

is

the

the

eyelid

muscle

of

gently.

action

In

in

addition,

an

the

palpe-

involuntar y

blink

25

encircles

the

lacrimal

canaliculi.

Contraction

of

this

portion

voluntar y

wink.

Relaxation

of

the

levator

muscle

occurs

28

of

the

orbicularis

assists

in

moving

tears

through

the

canaliculi

concurrently.

Spontaneous

involuntar y

blinking

renews

the

26

into

the

with

nasolacrimal

the

medial

drainage

rectus

muscle

system.

pulley

Horner

and

check

muscle,

along

ligament,

sup-

24

port

the

medial

aspect

of

the

tarsal

plate.

Another section of the palpebral orbicularis, Riolan muscle, lies

near the lid margin on both sides of the meibomian gland openings.

It

maintains

the

eyelid

margins

close

to

the

globe

and

may

aid

in

21 27

regulation of meibum expression from the meibomian glands.

CLINICAL

Abnormal

pion

(Fig.

normal

its

2.8).

the

cheek,

A

may

Inversion

against

tears

in

the

the

the

the

from

occur,

of

of

aging

of

this

process.

the

lacrimal

causing

margin

cause

globe,

the

eyelid

Ectropion

eyelid

common

occurrence

position

drain

COMMENT:

eversion

of

Entropion

away

from

is

loss

As

the

lacrimal

lake.

irritation

margin,

and

of

eyelid

punctum

Epiphora,

the

called

the

an

delicate

entropion,

globe

orbicularis

is

margin

no

may

in

of

this

result

called

falls

longer

overow

skin

is

muscle

in

ectro-

tone,

away

position

tears

a

from

onto

to

the

area.

from

spasm

of

Fig. 2.9 the

orbicularis

oculi

muscle

causing

the

lid

margin

to

turn

inward

(Fig.

mology: This

inward

turning

of

the

eyelid

margin

puts

the

eyelashes

in

contact

Involutional entropion. (From Kanski JJ. Clinical Ophthal-

2.9).

A

Systematic

with

Heinemann;

2003.)

Approach.

ed

5,

Oxford,

UK:

Butter worth-

CHAPTER

14

2

Ocular

Adnexa

and

Lacrimal

System

precorneal tear lm. A reex blink is protective and may be elic-

ese

ited by a number of stimuli—a loud noise; corneal, conjunctival,

rior

or

vide

cilial

touch;

When

the

or

the

orbital

sudden

portion

approach

of

the

of

an

object.

orbicularis

contracts,

the

eye

as

ligaments

orbit

from

support

acting

as

form

the

for

a

brous

trochlea

the

pulley

upper

for

bands

to

the

eyelid

the

that

span

lateral

and

levator.

the

orbital

orbital

ey

are

anterior

wall.

structures

located

supe-

ey

at

pro-

as

the

well

point

34

closes

tightly,

temple,

and

and

the

areas

cheek—are

surrounding

involved

in

the

the

lids—the

contraction.

forehead,

Such

closure is oen a protective mechanism against ocular pain or aer

injury

and

tightly

in

is

a

called

strong

reex

blepharospasm.

contraction,

forces

If

the

lids

compressing

are

the

where the levator muscle bers end and the aponeurosis begins.

eyelid

closed

orbital

Levator

As

it

Aponeurosis

enters

dinous

the

eyelid,

expansion,

the

the

levator

levator

becomes

a

aponeurosis.

fan-shaped

Unlike

a

ten-

typical

29

contents

e

of

signicantly

antagonist

muscle

tion

can

is

the

the

to

increase

the

levator

palpebral

muscle.

orbicularis

the

e

muscle

is

intraocular

portion

of

antagonist

the

frontalis

to

pressure.

the

the

tendon,

orbicularis

orbital

por-

muscle.

e

Palpebral

superior

upper

eyelid,

extends

into

Levator

upper

palpebral

is

the

located

upper

levator

within

eyelid.

It

Muscle

muscle,

the

orbit

lid,

originates

the

retractor

on

the

the

of

globe

lesser

the

and

wing

of

face

of

skin

of

tarsal

bundles

the

eyelid,

orbital

its

the

and

the

septum

entire

although

some

extensive

e

and

third

to

ese

of

insert

run

the

the

into

the

en,

anterior

the

sur-

between

primarily

into

sheet

of

tendinous

tissue.

the

bers

insert

bers

extend

width.

anterior

orbicularis

an

connective

lower

the

into

septum.

submuscular

into

plate,

of

out

orbital

across

the

insert

spreads

the

the

out

through

bers

the

muscle

to

penetrate

fanning

pass

posterior

above

aponeurosis

posterior

aponeurosis

bers

Superior

the

beginning

the

into

the

intermuscular

35

the

its

sphenoid

sheath

As

the

bone

blends

levator

above

with

and

the

approaches

in

front

sheath

the

of

of

the

eyelid

the

optic

superior

from

its

foramen,

rectus

posterior

and

muscle.

origin

at

septa of the orbicularis (see Fig. 2.10).

the

levator

aponeurosis,

skin,

and

e attachments between

orbicularis

anchor

the

skin

to the underlying tissue in the pretarsal area of the eyelid and cre-

35

the

orbital

ment

apex,

(Whitnall

two

ligaments,

ligament),

the

found

superior

above

transverse

the

levator,

liga-

and

the

ate

the

the

upper

eyelid

aponeurotic

crease.

bers

do

In

not

those

attach

of

as

Eastern

Asian

extensively

to

descent,

the

cutane-

1,11,35

intermuscular

form

a

sleeve

transverse

around

the

ligament,

levator

found

which

below

changes

the

the

levator,

anteroposte-

10

rior

direction

of

the

levator

to

superoinferior

(Fig.

ous

12

e

transverse

ligament

causing

two

side

an

absent

extensions

or

of

lowered

the

eyelid

crease.

aponeurosis

are

referred

to

as

30–33

2.10).

horns. e lateral horn helps to support the lacrimal gland by hold-

ing

Superior

tissue

it

against

the

orbital

roof,

dividing

the

gland

into

orbital

and

palpebral lobes (Fig. 2.11). e lateral horn then attaches to the lat-

Frontal

bone

eral

canthal

tendon

and

lateral

orbital

tubercle.

e

medial

horn

is

attached to the medial canthal tendon and posterior lacrimal crest.

Levator Adipose

tissue

muscle

Levator

Action

Contraction

e

Orbital

septum

of

the

globe

transverse

ner ve,

ligament

Orbicularis

the

superior

position

levator

Intermuscular

of

connection

is

rectus

so

that

inner vated

cranial

e

levator

between

ner ve

eyelids

are

muscle

the

muscle

as

by

the

the

causes

sheath

of

elevation

the

coordinates

eye

is

eyelid

elevated,

superior

of

levator

the

division

eyelid.

sheath

position

lid

of

the

and

is

the

with

raised.

e

oculomotor

III.

closed

by

relaxation

of

the

levator

and

con-

muscle

traction Tarsal

of

of

the

orbicularis

oculi

muscles.

e

tonic

activity

of

muscle

the

Müller

levator

open.

with

In

a

a

and

the

blink,

burst

of

relaxation

tonic

of

activity

activity,

the

the

of

orbicularis

the

levator

orbicularis

is

rapidly

hold

the

eyelid

suspended,

lowers

the

and

lid

fol-

Tarsal

plate

lowed

by

a

cessation

of

orbicularis

activity

and

resumption

of

36

levator

tonicity.

Retractor

of

the

Lower

Eyelid

Tendon

e of

retractor

of

the

lower

eyelid

is

the

capsulopalpebral

fascia

levator 37

muscle

(lower eyelid aponeurosis).

is is analogous to the levator apo-

neurosis in the upper eyelid. e capsulopalpebral fascia, an ante-

rior

extension

from

the

sheath

of

the

inferior

rectus

muscle

and

the suspensory ligament, inserts into the inferior edge of the tarsal

37

plate.

is

ment.

e

lower

eyelid

insertion

lower

coordinates

eyelid

elevates

is

lid

depressed

slightly

on

position

on

globe

upward

with

globe

depression,

movement

of

move-

and

the

the

globe.

e capsulopalpebral fascia also fuses with the orbital septum and

sends

some

bers

to

insert

into

the

inferior

fornix

(the

junction

37

Fig.

2.10

Sagittal

section

of

upper

eyelid.

between the palpebral and bulbar conjunctiva).

In contrast to the

CHAPTER

2

Ocular

Adnexa

and

Lacrimal

15

System

Levator

Orbital

portion

lacrimal

aponeurosis

of

Superior

gland Tarsal

muscle tarsal

Palpebral

portion

lacrimal

of

plate

Müller

of

gland

Medial

canthal

tendon

Lateral

canthal

tendon

Inferior

tarsal

plate

Fig.

2.11

Orbital area viewed from the front, with skin, subcutaneous tissue, and orbital septum

removed. The

tion

levator

aponeurosis,

of

Müller

there

are

levator

muscle

few

tendon

are

is

sectioned

before

its

insertion

on

the

tarsal

plate. The

origin

and

inser -

evident.

attachments

to

the

skin

of

the

lower lid. is results in a poorly formed lower lid crease.

lower

border

about

whether

of

the

the

tarsal

inferior

plate,

although

tarsal

muscle

investigators

actually

disagree

inserts

into

1

9

29

the

32

38

tarsal plate or inserts into the tissue below the tarsal plate.

Tarsal

e

Muscle

superior

of

tarsal

Müller

muscle

Both

(Müller

muscle)

is

composed

of

smooth muscle and originates on the posteroinferior aspect of the

the

superior

sympathetic

vated

(as

in

and

bers

inferior

that

situations

widen

tarsal

the

associated

muscles

palpebral

with

fear

or

are

inner vated

ssure

when

by

acti-

surprise).

levator muscle. ese smooth muscle bers begin to appear within

the striated muscle at the point at which the muscle becomes apo-

neurotic.

of

the

e

tarsal

superior

plate

tarsal

(see Figs.

muscle

2.10 and

inserts

2.11).

on

the

superior

Contraction

of

CLINICAL

can

provide

2

mm

of

additional

lid

Ptosis

Ptosis is a condition in which the upper eyelid droops or sags. It can be caused

Müller

by weakness or paralysis of either the levator or Müller muscle. If Müller mus-

10

muscle

COMMENT:

edge

cle

elevation.

alone

levator

is

is

affected,

involved

a

(Fig.

less

2.12).

noticeable

An

form

individual

of

with

ptosis

ptosis

occurs

might

than

when

attempt

to

the

raise

A similar smooth muscle, the inferior tarsal muscle, is found

the

lid

by

using

the

frontalis

muscle,

which

results

in

elevation

in the lower eyelid. It arises from the inferior rectus muscle sheath

and

wrinkling

of

the

forehead.

and inserts into the lower palpebral conjunctiva and possibly the

A

B

Fig.

the

2.12

right

both

A,

Mild

eyelid

cases,

ptosis

of

following

indicating

a

use

the

right

cranial

of

the

eyelid

ner ve

associated

III

front alis

palsy.

muscle

with

Note

to

Horner

the

aid

in

syndrome.

elevation

raising

of

the

the

B,

Severe

ipsilateral

eyelid.

ptosis

eyebrow

of

in

of

the

eyebrow

CHAPTER

16

Orbital

e

to

that

the

the

(see

Fig.

rim

is

to

the

no

thin

sheet

encircles

contents

from

aponeurosis

and

Lacrimal

System

the

brous

orbit.

from

the

3.7

of

the

4.4

acts

eyelid

superior

to

It

connective

a

barrier

structures.

orbital

mm

as

tis-

above

rim

the

to

e

and

e

insert

orbital

into

superior

the

septum

tarsal

tarsal

appreciable

plate

plate

dierence

extends

of

from

the

the

plate

inferior

height

is

in

insertion

the

inferior

shorter

in

eyelid.

Asians,

site

of

the

14

b orders

j oine d

lower

of

of

to

b ot h

t he

b ord ers

t he

me di a l

exp ansion

are

j oine d

of

to

and

t he

an

l atera l

c ant ha l

l e vator

tend on ,

ex p ans ion

of

t he

L o ckwo o d.

Glands

e

of

the

Eyelids

meibomian

embedded

resemble

such

in

a

that

glands

the

large

their

(tarsal

tarsal

plate.

bunch

of

openings

glands)

ese

grapes

are

and

located

are

long,

are

in

a

sebaceous

glands

multilobed

glands

arranged

row

vertically

along

the

eyelid

15

margin

posterior

meibomian

to

the

glands

cilia

are

(Fig.

found

2.13).

in

the

Approximately

upper

eyelid,

25

and

to

20

to

27

Plate

eyelid

t heir

ligament

40

Each

are

insert

tarsal

orbital septum in relation to the tarsal plate in dierent races.

Tarsal

upp er

tendons

19

2.10).

Although

there

a

extends

levator

14

orbital

is

orbital

septum

into

Adnexa

The

septum

concentrically

separate

orbital

Ocular

Septum

orbital

sue

2

30

contains

a

tarsal

plate

(tarsus)

that

gives

meibomian

the

eyelid

length

the

globe.

2

of

a

glands

gland

is

are

found

approximately

in

the

5.5

lower

mm

in

eyelid.

the

upper

e

lid

and

27

rigidity

In

and

those

of

structure

Asian

and

shapes

descent,

the

it

to

the

superior

cur vature

tarsal

plate

15

compared

sal

plate

with

is

15

the

mm

high

5

in

high

in

8

mm

high

the

in

the

lower

meibomian

lid.

On

glands

can

eyelid

eversion

sometimes

be

the

seen

vertical

as

rows

yellow

of

streaks

39

Caucasians.

mm

is

mm

e

both

inferior

Caucasians

tar-

through

and

outer

the

lipid

palpebral

layer

of

the

conjunctiva.

tear

ese

glands

secrete

the

lm.

39

Asians.

to

10

approximately

of

e

anterior

submuscular

surface

connective

of

the

tissue.

tarsal

e

plate

is

posterior

adjacent

surface

is CLINICAL

adherent

to

the

the

superior

the

marginal

palpebral

tarsus

is

border

conjunctiva.

attached

lies

at

the

to

the

eyelid

e

orbital

Müller

margin.

border

muscle,

e

of

Some

whereas

lateral

bomian

aspect

be

COMMENT: Contact

studies

have

glands

dependent

in

on

identied

contact

the

a

loss

lens

type

of

Lens

in

both

wearers

lens

but

Wear

the

(Fig.

number

2.14).

rather

on

and

Loss

the

the

length

does

duration

not

of

of

mei-

appear

wear

to

and

is

41

of

the

eral

tarsal

canthal

aspect

of

plate

is

tendon.

the

tarsal

attached

Recent

plate

is

to

the

studies

orbital

have

attached

to

margin

shown

the

by

that

orbital

the

the

speculated

lat-

by

rectus

capsulopalpebral

fascia

consists

of

caused

by

chronic

irritation.

the

23

medial

be

medial

margin

24

Horner muscle and the medial rectus capsulopalpebral fascia.

e

to

the

e

medial

sebaceous

Zeis

glands

secrete

sebum

into

the

hair

fol-

licle of the cilia, coating the eyelash sha to keep it from becom-

9

rectus

muscle

attaching

to

pulley,

the

the

lacrimal

medial

check

caruncle

and

ligament,

tarsal

and

plate.

bers

e

ing

dense

brittle.

e

Moll

glands

have

been

called

modied

sweat

glands

but

42

connective

orbital

rim

during

eye

tissue

hold

and

structures

the

lid

tarsal

connecting

plates

in

the

tarsal

position

plates

against

to

the

the

globe

movements.

are

more

ey

into

the

accurately

are

the

lid

located

hair

described

near

follicle,

margin.

the

eyelid

into

Similar

as

the

specialized

margin

Zeis

glands

and

gland

found

apocrine

their

duct,

in

the

glands.

ducts

or

empty

directly

axillae

are

onto

scent

9

organs,

CLINICAL

When

COMMENT: Eyelid

attempting

applicator

or

to

evert

ngertip

experiences

difculty

the

above

in

the

eyelid,

superior

everting

e

Eversion

upper

the

one

edge

eyelid

if

should

of

the

the

place

tarsal

a

cotton-tipped

plate.

applicator

is

The

in

glands

of

the

tarsal

is

of

of

the

likely

not

lacrimal

function

glands

conjunctival

W olfring are

the

fornix,

located

of

the

Krause

and

along

of

the

Moll

are

located

accessory

the

orbital

are

oval

16

gland.

border

in

the

lacrimal

of

the

tar-

the

sal

middle

that

accessory

stroma

novice

placed

but

plate

(see

Fig.

2.13).

ese

glands

and

display

numer-

plate.

ous acini. In the upper fornix, 20 to 40 glands of Krause are found,

1

although

e

Canthal

e

are

Tendons

canthal

the

tendons,

insertion

canthal

tendon

only

glands

accessory

previously

points

of

occupies

a

the

known

as

orbicularis

signicant

area

palpebral

muscle.

in

the

ligaments,

e

medial

six

of

to

eight

W olfring

lacrimal

such

are

glands

glands

less

appear

numerous.

appears

similar

to

in

the

lower

fornix.

e

secretion

that

of

the

of

main

the

lac-

rimal gland and contributes to the aqueous layer of the tear lm.

medial

canthal

HISTOLOGICAL

FEATURES

OF

THE

EYELID

region. It was thought to divide into two limbs, but recent studies

have

shown

only

one

limb

that

attaches

to

the

anterior

lacrimal

Skin

24

crest.

Because

greater

role

in

of

this,

Horner

stabilizing

the

muscle

tarsal

is

now

plate

thought

medially.

to

e

play

a

medial

e skin of the eyelid contains many ne hairs, sebaceous glands,

and

sweat

glands.

It

is

the

thinnest

skin

in

the

body,

easily

forms

1

canthal tendon lies anterior to the orbital septum (see Fig. 10.22).

e

lateral

septum

the

Fig.

and

lateral

orbital

10.22).

and

the

allow

slight

tendon is

the

margin

Fibrous

tendon

a

canthal

attaches

at

edges

the

connections

check

lateral

located

lateral

ligament

posterior

of

lateral

the

orbital

between

for

displacement

the

of

the

lateral

the

to

the

tarsal

orbital

plates

tubercle

lateral

rectus

lateral

to

(see

canthal

muscle

canthus

with

folds

e

a

and

wrinkles,

epidermal

granular

and

layer

layer,

of

and

is

almost

the

a

skin

transparent

consists

supercial

of

layer

a

in

basal

that

is

abduction.

very

young.

germinal

layer,

keratinized.

e

underlying dermis is abundant in elastic bers. A very sparse are-

olar

connective

tissue

layer,

the

subcutaneous

tissue,

lies

below

the dermis. is thin layer is devoid of adipose tissue in the tarsal

portion.

A

pad

of

fat

is

oen

located

in

this

region

40

extreme

the

in

9

portion

that

separates

the

orbicularis

from

the

skin.

the

orbital

CHAPTER

Accessor y

gland

(of

2

Ocular

Adnexa

and

Lacrimal

System

lacrimal

Krause) Orbicularis

oculi

Superior

muscle

(of

tarsal

Subcutaneous

Müller)

connective

Accessor y

gland

(of

muscle

tissue

lacrimal

Wolfring)

Epider mis

of

Palpebral

skin

Aponeurosis

of

conjunctiva

levator

muscle

T arsal

plate

Submuscular

areolar

layer

Meibomian

glands

Gland

Zeis

of

Moll

gland

Riolan

muscle

Hair

Pore

of

meibomian

Fig.

2.13

Sagittal

section

of

the

eyelid

Grade

the

Grade

2.14

upper

gland

Infrared

eyelid.

loss.

Grove,

digital

B,

Ore.)

and

glands.

meibomian

Patrick

C4

2

Grade

photography

Normal

(Courtesy

muscles

C3

1

Fig.

palpebral

B

C2

C1

gland

illustrating

A

follicle

Caroline,

of

meibomian

glands

of

C.O.T .,

the

glands.

lower

Pacic

3

A,

eyelid.

Universit y

Grade

Normal

C,

meibomian

Grading

College

scale

of

for

glands

of

meibomian

Optometr y,

Forest

4

17

CHAPTER

18

2

Ocular

Adnexa

and

Lacrimal

System

the CLINICAL

COMMENT: Fluid

Accumulation

in

the

skin

muscle The

loose

connective

tissue

layer

of

the

eyelid

can

be

separated

easily

in

underlying

injuries

or

tissue

the

and

is

the

accumulation

site

of

for

the

accumulation

exudates

in

of

blood

inammatory

or

superior

to

be

of

the

greatly

ecchymosis

skin

and

distensible,

(a

black

the

as

eye).

ne

underlying

evidenced

This

skin

in

adjacent

patients

recovers

tissue

with

rapidly

allow

periorbital

after

this

and

stretching

will

cause

exaggerated

skin

or

because

e

portion

tarsal

of

the

eyelid.

muscle

are

e

smooth

located

plate

and

insert

into

its

upper

above

edge.

brils

vertically

and

of

composed

this

tissue

horizontally

of

are

to

dense

of

connective

uniform

surround

the

size

tissue.

and

r un

meibomian

e

both

glands.

folds.

Muscles

tal

tarsal

superior

Plates

collagen

e

Conjunctiva

palpebral

conjunctiva

lines

the

inner

surface

of

the

eyelid

and at the fornix transitions into bulbar conjunctiva, which covers

orbicularis

striated

tarsal

tarsal plates are

Palpebral

e

the

The

of the elasticity of the dermis. With advancing age, however, the skin loses its

elasticity,

in

the

area

cellulitis

distention

of

edema

conditions.

Tarsal thinness

rmly

bers

from

the the

so

Eyelid

oculi lies

muscle

section

of

orbicularis

bundles

the

lid

bundles

the

lid

margin,

the

meibomian

deep

run

prepared

are

small

cut

for

in

muscle

glands

to

the

subcutaneous

throughout

the

microscopic

cross-section

bundles

represent

a

In

ese

a

sagit-

examination,

(Fig.

located

specic

layer.

eyelid.

on

part

2.15).

both

of

sclera.

epithelial

At

the

layer

mucocutaneous

of

the

conjunctiva

junction of

is

the

continuous

lid

margin,

with

the

the

epithe-

the

lium of the skin (see Fig. 2.15). As the conjunctiva lines the eyelid,

Along

squamous cells of the skin are replaced by cuboidal and columnar

sides

the

the

of

orbicu-

cells

of

the

conjunctiva,

forming

a

stratied

columnar

mucoepi-

thelial layer, and the granular and keratinized layers of the skin are

43

laris,

the

margin

ciliar y

against

Posterior

part

the

to

(Riolan

globe

the

muscle),

(see Fig.

orbicularis

which

holds

the

eyelid

discontinued.

2.15).

lies

e

another

layer

of

loose

con-

epithelial

layer

of

the

conjunctiva

thickens

at

the

muco-

cutaneous junction (see Fig. 2.15) and may be a location for stem

44

nective

the

sal

tissue,

muscle

plate

the

is

from

a

vessels

the

submuscular

the

tarsal

potential

of

the

areolar

plate.

space,

palpebral

layer,

B etween

the

this

pretarsal

arcades.

An

which

layer

space,

separates

and

that

analogous

the

tar-

contains

preseptal

space is located between the orbicularis and the orbital septum.

cells that repopulate the palpebral conjunctival epithelium.

mucocutaneous

junction

the

edge

conjunctival

ened

held

area

of

tightly

of

palpebral

against

the

transitions

the

upper

and

conjunctiva,

eye

by

the

to

the

lid

lower

0.3

to

Riolan

wiper

eyelids.

1.5

mm

muscle

is

in

and

e

region

height,

is

at

thick-

the

is

part

43

Tendinous bers of the levator aponeurosis run through the

submuscular

rior

tarsal

tissue

muscle

layer

to

between

insert

into

the

the

orbicularis

tarsal

plate

and

and

the

the

supe-

skin

of

of the eyelid that makes contact with the globe.

It is responsible

for spreading tears during the blink. In the lid wiper region there

are large stratied cuboidal and columnar cells interspersed with

45

the eyelid (see Fig. 2.13). It is this insertion of bers that anchors

Levator

goblet

cells

that

secrete

mucin

onto

the

Orbicularis

muscle

conjunctiva

Gland

Meibomian

of

Moll

glands

Hair

Riolan

surface.

Epidermis

aponeurosis

Palpebral

ocular

follicle

muscle

Zeiss

Mucocutaneou s

junction

Fig.

2.15

Light

micrograph

of

the

upper

eyelid.

gland

for

eyelash

CHAPTER

with

e

2

Ocular

advancing

goblet

ing

the

the

cell

cell

cell

Adnexa

age

and

swell

nally

mucin

and

and

in

inammator y

that

goblet

releasing

into

ner ves

conditions.

accumulate,

shaped.

mucus

sympathetic

19

System

droplets

become

ruptures,

Parasympathetic

Lacrimal

increases

produces

to

and

e

the

have

caus-

surface

tear

been

of

layers.

associ-

49

ated

with

goblet

cells

Invaginations

of

the

called

fornix,

mucus

are

into

the

and

may

play

conjunctival

cr ypts

cavity

a

role

in

epithelium,

of

Henle.

formed

by

their

oen

Goblet

these

secretion.

located

cells

near

release

invaginations,

their

and

the

mucus may become trapped if the opening to the cr ypt is narrow.

e

surface

microvilli

of

and

the

supercial

microplicae

and

conjunctival

is

covered

50

similar

icles,

to

found

junctival

As

Fig.

2.16

margin.

Lid

wiper

epitheliopathy

(Courtesy T racy

Optometr y,

Forest

Doll,

Grove,

O.D.,

along

Pacic

the

lower

Universit y

eyelid

College

of

that

extend

below

cell,

these

found

outward

secreted

by

the

may

vesicles

the

on

be

form

membrane

a

the

source

epithelial

chemical

cells.

of

ese

chains

contains

glycocalyx

Subsurface

the

of

cell

bond

a

51

surface.

additional

with

goblet

corneal

outer

an

fuse

to

the

cell

with

supercial

mucous

material.

membrane,

with

the

increase

chains

mucous

the

ves-

con-

layer

adherence

of the tear lm. ese vesicle membranes may also contribute to

Ore.)

52

the

CLINICAL

Lid

wiper

COMMENT: Lid

epitheliopathy

epithelium

along

the

occurs

eyelid

Wiper

when

margin

microvilli

present

on

the

surface

of

the

epithelial

cell.

Epitheliopathy

there

because

is

of

alteration

increased

of

the

friction

conjunctival

between

the

46

eyelid and the ocular surface or contact lens surface (Fig. 2.16).

Tear instabil-

CLINICAL

COMMENT: Vitamin

A

Deciency

Vitamin A deciency has been associated with a loss of goblet cells. In dry-eye

disorders

showing

a

decrease

in

the

number

of

goblet

cells,

treatment

53

ity

or

eyelid

anatomy

that

causes

greater

pressure

between

the

lid

and

cornea

47

can

contribute

to

this

vitamin

A

disease,

condition.

therapy

cellular

can

induce

proteins

may

the

be

reappearance

activated

of

goblet

causing

with

54

cells.

In

keratinization

of

acute

the

sur-

55

face

epithelia.

Goblet cells, which produce, store, and secrete the innermost

mucous layer of the tear lm, are scattered throughout the strati-

e

submucosa

(stroma,

substantia

propria)

of

the

palpe-

ed columnar conjunctival epithelium (Fig. 2.17). ese cells are

bral conjunctiva is ver y thin in the tarsal portion of the eyelid but

most

becomes increasingly thick in the orbital portion. It is composed

numerous

in

the

plica

semilunaris

followed

by

the

inferior

48

nasal

aspect

of

the

tarsal

conjunctiva.

eir

number

decreases

of

loose,

vascularized

connective

tissue

that

can

be

subdivided

into an outer lymphoid layer and a deep brous layer. In addition

to

the

normal

broblasts,

lymphoid

nuclear

connective

ground

layer

tissue

substance,

contains

leukocytes,

components

and

a

few

macrophages,

eosinophils,

ne

mast

(collagen

elastic

cells,

accumulations

brils,

bers),

the

polymorpho-

of

lymphocytes,

56

and

in

occasional

the

Langerhans

lymphoid

layer,

cells.

making

Immunoglobulin

the

conjunctiva

an

A

is

found

immunologi-

57,58

cally

active

tissue.

More

lymphoid

tissue

is

found

in

palpe-

59

bral

conjunctiva

e

lying

brils

deep

and

pale

with

conjunctiva

palp ebral

a

is

be

COMMENT: Conjunctival

pinhead

are

composed

of

most

ne

often

small,

located

granular

degeneration.

These

a

the

material

nodules

with

of

under-

collagen

ner ves,

merges

the

blo o d

clinical

to

of

tarsal

vess els

sign

of

and

and

is

plate.

that

anemia.

Concretions

tarsal

and

are

vess els,

layer

tissue

yellow-white

in

network

blo o d

supplied

may

conjunctiva

brous

connective

richly

are

the

random

broblasts,

dens e

so

concretions

cellular

connects

conjunctiva

Conjunctival

and

conjunctiva.

contains

glands.

the

is

bulbar

layer

numerous

CLINICAL

are

in

and

lacrimal

continuous

e

brous

str uctures

accessor y

than

nodules

about

conjunctiva

membranous

hardened

but

the

(Fig.

debris,

contain

size

2.18).

of

products

no

a

They

of

calcium

60

deposits.

Fig.

2.17

Light

micrograph

of

the

conjunctival

removed

bral

epithelium

showing

goblet

cells.

Concretions

are

found

more

often

in

palpeif

they

produce

foreign

body

irritation.

elderly

patients

and

can

be

a

CHAPTER

20

2

Ocular

Adnexa

and

Lacrimal

System

move

centrally

begin

to

in

the

acini,

become

large

and

polyhedral,

27

synthesize

meibocyte

and

the

degenerates,

cell

Cells

in

membrane

var ying

Decomposed

During

tarsal

the

a

lipids

the

lipid

begins

to

and

63

droplets.

decomposition

down

the

surrounding

(lipid

with

nucleus

of

move

releasing

secretion

the

ll

As

diminish

each

in

size,

disintegrates.

stages

cells

blink,

plate

and

meibum

droplets

duct

Riolan

into

and

the

cell

pack

each

toward

muscle

tear

saccule.

opening.

compresses

lm,

debris)

the

at

which

forms

the

the

point

outer-

most lipid layer of the tear lm. e predominant inner vation of

meibomian

glands

is

parasympathetic

and

27

lipid

production

e

oily

meibum

glands

cous

of

cause

secretion

to

of

distinguish

the

than

or

skin

and

sebum;

cell

the

it

meibomian

from

hair

sebum

64

sebum

follicles.

is

may

act

to

alter

the

65

rupture.

more

glands

secreted

Meibum

polar

and

has

by

is

if

been

the

called

sebaceous

much

more

mixed

vis-

with

the

66

Fig.

2.18

Concretions

on

the

inferior

palpebral

tear

conjuncti va.

lm

will

contaminate

Histologically,

meibomian

Glands

e

the

just

meibomian

length

of

the

glands

tarsal

are

large

plate.

sebaceous

Each

consists

glands

of

10

27

secretor y

arranged

acini

attached

vertically

to

such

a

large

that

the

central

to

61

is

lobes

Meibomian

is

by

surrounded

actively

glands

the

by

dividing

are

holocrine

decomposition

a

layer

cells.

of

of

(Fig.

2.20).

ey

release

myoepithelial

e

daughter

eir

entire

cells

cells,

In

is

from

becoming

acini

and

general,

sebum

Zeis

are

two

into

cell.

and

called

Zeis

glands,

glands

glands

follicle,

are

however,

associated

Zeis

the

it.

with

are

thereby

the

at

duct

the

edge

secretion

Each

is

is

acinus

lled

with

meibocytes,

Moll

the

glands,

eyelash

cavity,

large

the

neck

to

and

of

oen

ey

which

surround

the

of

becomes

appears

columnar

apocrine

consist

empty

secretor y

secretor y

glands,

a

spiral

narrow

and

cells

cells.

is

are

as

it

(Fig.

Because

the

Meibomian

gland

duct

Riolan

muscle

Light

micrograph

shown.

of

of

follicle

follicle.

the

the

meibomian

glands

embedded

gland

in

the

tar sal

plate. The

duct

located

forms

2.21).

junction

are

per

begins

surrounded

Mucocutaneous

Zeis

also

that

Riolan

2.19

the

cilia

brittle.

modied

follicle.

lumen

cuboidal

cells

dr y

muscle

pore

eyelash

preventing

gland

and

to

composed

present

Meibomian

Fig.

similar

are

61

e

located

glands.

the

two

or

of the tarsal plate corresponding to the eyelid margin (Fig. 2.19).

produced

or

disrupt

sebaceous

e

62

duct.

opening

occupying

15

one

the

glands.

and

a

by

as

a

near

large

duct.

a

e

layer

of

Myoepithelial

Moll

gland

is

an

CHAPTER

Zeis

gland

with

Fig.

The

apocrine

but

the

lid

of

gland,

parts

duct

of

margin

a

of

its

Zeis

Light

is

or

cilia.

peptides

micrograph

is

composed

cytoplasm.

gland,

it

e

might

open

proteins

in

not

duct

Histochemical

and

for

of

the

of

the

follicle

Adnexa

Lacrimal

21

System

gland

margin.

A

Zeis

gland

is

located

might

directly

studies

Moll

whole

empty

onto

have

gland

the

cell

into

that

eye-

identied

secretions

suggest

a

role

in

42

and

ocular

next

to

a

hair

follicle.

Accessor y

a

lacrimal

truncated-pyramid

central

immune

defense

protecting

the

lash

sha

67

surface.

lumen

(Fig.

glands

shape

2.22).

Accessor y Moll

and

Zeis

cilia

eyelid

Ocular

evident.

secretion

cellular

between

antimicrobial

2.20

duct

Hair

duct

2

are

groups

arranged

e

acini

in

are

of

an

secretor y

oval

cells

pattern

surrounded,

with

around

a

sometimes

lacrimal

gland

gland

Meibomian

Hair

follicle

Fig.

Fig.

2.21

glands

Light

are

micrograph

seen.

of

a

hair

gland

follicle

of

a

cilia. T wo

Moll

2.22

lacrimal

a

Light

gland

meibomian

is

micrograph

seen

gland.

near

of

the

a

lower

tarsal

eyelid.

plate,

within

An

accessor y

which

houses

CHAPTER

22

2

Ocular

Adnexa

and

Lacrimal

System

incompletely, by a row of myoepithelial cells. ese are merocrine

glands—that

and

these

is,

the

glands

cell

have

remains

the

same

intact

and

secretes

histological

a

makeup

product—

as

the

main

68

lacrimal

gland.

e

secretion

contains

antibacterial

agents,

69

lysozyme,

lacrimal

lactoferrin,

glands

are

and

immunoglubulins.

densely

inner vated,

as

is

e

the

accessor y

main

lacrimal

70

gland.

Animal

studies

suggest

that

the

ducts

of

W olfring

glands

68

have a tortuous course and open onto the palpebral conjunctiva.

CLINICAL

A

COMMENT: Common

hordeolum

is

an

acute

Eyelid

inammation

of

an

Conditions

eyelid

gland,

usually

caused

by

71

staphylococci.

lum,

or

(Fig.

An

common

2.23).

A

infected

stye,

and

localized

Zeis

or

usually

infection

of

Moll

gland

comes

a

to

a

is

called

head

meibomian

on

gland

an

the

external

skin

usually

of

hordeo-

the

drains

eyelid

from

the

inside surface of the eyelid and thus is called an internal hordeolum (Fig. 2.24).

Mild

cases

cases

A

a

usually

might

chalazion

is

meibomian

may

resolve

require

extrude

a

localized,

gland,

its

often

secretion

inammation.

Medical

Blepharitis

an

(anterior

caused

is

a

or

or

disruption

warm

noninfectious,

caused

into

by

the

an

treatment,

and

therapy

disease

tissue,

duct

but

more

of

either

on

is

the

(posterior

the

lid

painless

(Fig.

setting

sometimes

glands

microora

sometimes

obstructed

surrounding

surgical

meibomian

of

compress

severe

treatment.

inammatory

blepharitis)

by

with

antibiotic

up

swelling

2.25).

a

The

of

gland

Fig.

granulomatous

2.24

Internal

hordeolum.

necessary.

eyelid

skin

and

blepharitis).

margin

with

It

lashes

is

often

increased

pres-

infratrochlear

maticofacial

division

of

branch

and

the

of

the

ophthalmic

infraorbital

trigeminal

ner ves,

ner ve

ner ve

branches

(Fig.

2.27).

and

of

the

the

Motor

zygo-

maxillar y

control

of

72

ence of Staphylococcus aureus

In addition, Demodex parasites increase with

the

age

and

can

cause

blepharitis

involving

either

the

lashes

or

the

orbicularis

is

through

the

temporal

and

zygomatic

meibomian

branches 73

muscle

of

the

facial

ner ve,

and

that

of

the

levator

muscle

is

74

glands.

Clinical

presentation

includes

crusting

or

translucent

debris

sur-

through the superior division of the oculomotor ner ve. e tarsal rounding

the

lash

base,

erythema

of

the

lid

margin,

or

plugging

of

the

meibo-

smooth

muscles

are

inner vated

by

sympathetic

bers

from

the

mian glands (Fig. 2.26). Blepharitis is typically a chronic condition that requires

superior periodic

treatments

tiparasitic

can

lead

agents

to

loss

with

to

of

aid

warm

in

compresses,

restoring

eyelashes,

normal

lid

hygiene,

microora.

hyperkeratinization

and

and

antibiotic

Long-term

brosis

of

or

glands,

and

hyperemia,

telangiectasia,

and

scarring

of

the

the

lid

an-

meibo-

75

BLOOD

blood

each

e

ophthalmic

ner ve

lid

is

lear,

of

provide

supplied

and

the

OF

and

THE

by

lacrimal

trigeminal

the

supraorbital,

ner ve.

Fig.

divisions

inner vation

ner ves,

branches

Inner vation

2.23

OF

THE

EYELIDS

vessels

eyelid.

e

are

located

marginal

in

a

series

palpebral

of

arcades

arcade

lies

or

near

arches

the

in

eyelid

EYELIDS

maxillar y

sensor y

SUPPLY

margin.

e

INNERVATION

ganglion.

blepharitis

72

mian

cer vical

External

of

the

of

the

eyelids.

supratrochlear,

of

to

trigeminal

e

infratroch-

the

ophthalmic

the

lower

hordeolum.

lid

upper

is

division

from

the

margin,

and

the

edge

the

tarsal

of

arcades

are

peripheral

plate

anastomosing

palpebral

arteries.

either

ophthalmic

lateral

the

palpebral

e

2.28).

branches

medial

arter y

arteries

Fig.

palpebral

(Fig.

are

2.25

or

arcade

e

from

palpebral

from

the

branches

Painless

of

lies

near

vessels

the

medial

arteries

lacrimal

chalazion.

orbital

and

these

lateral

branch

dorsonasal

the

the

forming

from

arter y.

arter y.

e

CHAPTER

2

Ocular

blepharitis

showing

A

Adnexa

and

Lacrimal

23

System

B

Fig.

ing

Normal

common

lower

2.26

the

variations

variation

Inammation

base

occur

is

a

of

in

lack

the

the

of

of

Eyelids.

eyelash.

blood

the

B,

A,

Anterior

Plugged

supply,

peripheral

and

meibomian

the

arcade

most

in

the

debris

it

is

(4)

lid.

translucent

debris

surround-

gland.

and

the

it

mum

helps

remove

primar y

provides

optical

(lysozyme,

source

a

sloughed

of

smooth

function;

beta-lysin,

epithelial

atmospheric

refractive

(5)

it

surface

contains

lactoferrin,

cells

oxygen

and

for

necessar y

antibacterial

and

debris;

the

(3)

cornea;

for

opti-

substances

immunoglobulins)

to

76

help

LACRIMAL

protect

lacrimal

infection;

(6)

it

helps

to

maintain

corneal

SYSTEM hydration

e

against

system

consists

of

the

lacrimal

and

ancillary

glands,

through

changes

in

tonicity

that

occur

with

evapora-

tion; and (7) it contains various growth factors and peptides that

69

tear lm, puncta, canaliculi, and nasolacrimal duct. ese structures

work

together

to

balance

the

inow

and

outow

of

the

tears

can

while

providing appropriate moisture to the cornea and conjunctiva.

regulate

ocular

surface

wound

repair.

Traditionally, the tear lm is described as having three layers;

however,

there

is

no

clear

distinction

between

the

aqueous

and

77

mucin

Tear

e

Film

tear

several

ser ves

containing

lm,

which

functions:

as

a

layers

covers

(1)

lubricant

it

the

keeps

between

anterior

the

the

surface

surface

globe

of

and

of

the

the

eye

eyelids;

globe,

moist

(2)

Levator

Superior

Lateral

tarsus

it

has

and

traps

palpebrae

superioris

tendon

ily

(Fig.

waxy

produced

evaporation,

and

by

vein,

and

esters,

the

the

tear

ar ter y ,

ner ve

e

cholesterol,

by

free

glands.

lubrication

lm

and

for

layer

smooth

lowering

vein,

and

surface

ner ve

Lacrimal

vein,

Lateral

ner ve

ner ve

Superior

Lacrimal

and

palpebral

arcade

ar ter y Medial

palpebral

Medial

canthal

ar ter y

canthal

tendon

tendon

palpebral

ar ter y Inferior

palpebral

arcade

Angular

Orbital

ar ter y

and

vein

septum

Inferior

tarsus

Infraorbital

T ransverse

facial

ar ter y

and

ner ve

ar ter y

Fig.

2.27

Human

Palpebral

Anatomy.

innervation.

Elsevier

2019.)

(From

Klonisch T ,

Hombach-Klonisch

S.

Sobotta.

Clinical

Atlas

of

lipid

layer

primar-

layer

eyelid

Infratrochlear

ar ter y,

a

acids,

lipid

Supratrochlear

ar ter y,

is

fatty

e

palpebral

ar ter y

Lateral

outermost

meibomian

provides

stabilizes

Supraorbital

2.29).

retards

movement,

tension,

keeping

CHAPTER

24

2

Ocular

Adnexa

Peripheral

Marginal

Lateral

palpebral

palpebral

palpebral

and

Lacrimal

Lipid

Superficial

arcade

arcade

System

arteries Aqueous

artery

Supraorbital

layer

temporal

layer

artery

Mucin

layer

Epithelium

–

glycolcalyx

Supratrochlear

Fig.

2.29

Schematic

representation

of

the

tear

lm.

artery

Middle

palpebral

arteries

Lacrimal

e Angular

Secretory

lacrimal

accessor y

conjunctival

e

nasal

artery

ral

artery

of

larger

Facial

2.28

cial

Palpebral

MJ.

Anatomy

structures.

Ophthalmic

1998;

blood

In:

of

Nesi

Plastic

and

supply.

and

the

F A,

ocular

Lisman

adnexa,

RD,

Reconstructive

from:

orbit,

Levine

Lemke

and

MR,

eds:

Surger y. 2nd

BN,

related

ed.

fa-

Smith’ s

St

Louis:

is

the

edge

lies

one-third

vided

into

lacrimal

plate.

to

the

main

gland

Ducts

the

or

lacrimal

glands,

the

three

can

be

the

size

of

both

the

gland,

and

the

above

portions

of

the

edge

lid

gland

and

is

is

the

subdi-

upper

exit

is

the

lobe

everted,

the

the

against

and

palpebral

lobe

of

of

against

rests

to

into

portion

levator,

e

upper

the

lies

surface

orbital

the

tempo-

divided

orbital

surface

muscle.

the

is

the

posterior

aponeurosis

against

the

If

on

just

gland

inferior

lies

rectus

sections.

seen

by

fossa

superior

superior

edge

a

bone,

lacrimal

e

fossa,

lateral

in

frontal

orbital,

e

medial

the

from

meibomian

located

the

2.11).

lacrimal

one-half

two

the

e

and

Fig.

shaped.

on

is

of

margin.

(see

almond

of

gland

plate

palpebral

aponeurosis,

lateral

artery

(Adapted

orbital

muscle

periorbita

the

orbital

portions,

levator

Lucarelli

includes

glands,

cells.

lacrimal

the

superior

two

lacrimal

goblet

main

side

the

Infraorbital

Fig.

system

artery

the

Dorsal

secretor y

System

the

tarsal

through

the

Mosby.)

palpebral

e

lobe.

lacrimal

gland

consists

of

lobules

made

up

of

numer-

27

tears

ous

from

layer

overowing

contains

onto

the

inorganic

cheeks.

salts,

e

glucose,

middle

urea,

or

aque-

enzymes,

pro-

ous

acini.

cells

Each

around

acinus

a

is

central

an

irregular

lumen

arrangement

surrounded

by

of

an

secretor y

incomplete

1

teins,

by

glycoproteins,

the

mucin

main

and

layer

acts

and

antibacterial

accessor y

as

an

lacrimal

interface

that

substances.

glands.

e

facilitates

It

is

secreted

innermost

adhesion

of

or

the

layer

of

acini

and

are

myoepithelial

drains

into

approximately

12

cells.

one

of

A

of

network

the

these

main

ducts,

of

ducts

connects

excretor y

which

empty

ducts.

into

the

ere

the

con-

1

aqueous

layer

of

the

tears

to

the

ocular

surface

and

provides

a

junctival

sac

in

the

superior

fornix.

e

secretion

is

composed

78

coating

e

the

which

mucin

layer

surface

and

is

goblet

viruses

friction

composed

epithelia

conjunctival

teria

reduces

and

cells.

between

of

the

mucin

can

binding

eyelid

glycocalyx

produced

Mucins

blocking

the

also

sites

and

bind

on

and

cornea.

secretion

secreted

and

from

by

entrap

microbes

the

bac-

and

pre-

of

water,

zyme,

are

electrolytes,

lactoferrin,

located

area

and

glands

in

the

are

and

and

the

antibacterial

subconjunctival

tarsal

plate.

identical

agents,

immunoglobulins.

to

tissue

Histologically,

the

main

e

between

the

lacrimal

including

accessor y

the

accessor y

gland.

Basic

lyso-

glands

fornix

lacrimal

secretion

69

venting

them

from

According

to

penetrating

some

sources,

the

ocular

the

tear

surface.

lm

is

4

to

maintains

8

μm

thick,

9

tears,

the

and

normal

reex

volume

secretion

of

the

increases

aqueous

the

portion

volume

in

of

the

response

to

79–81

with the aqueous layer accounting for 90% of the thickness.

a

stimulus.

B oth

main

and

accessor y

glands

play

a

role

in

basic

82

e

lipid

layer

is

approximately

53

nm

thick.

and

reex

e

secretion.

lacrimal

gland

is

supplied

by

the

lacrimal

arter y,

a

branch of the ophthalmic arter y. Sensor y inner vation is through

the CLINICAL

COMMENT: Tear

Film

lacrimal

ner ve,

a

branch

of

the

ophthalmic

division

of

the

Assessment

trigeminal

ner ve.

Vasomotor

sympathetic

inner vation

causes

Various clinical procedures are used to assess the extent of tear abnormalities.

In

one

method,

uorescein

dye

is

instilled

into

the

lower

cul-de-sac,

and

it

decreased

spreads throughout the tear lm. After a blink, the thin lipid upper layer begins

thetic

to

ing

break

down,

and

dry

spots

appear.

The

time

between

the

completion

of

the

blink and the rst appearance of a dry spot is termed the tear lm breakup time

(TBUT)

and

gives

an

indirect

measure

of

the

evaporative

rate.

Normally

the

83

TBUT

is

greater

than

10

seconds

and

longer

than

the

time

between

occurs

cornea

short

TBUT

can

occur

if

irregularities

or

disturbances

in

the

or

stimuli,

when

secretion

results

branches

conjunctiva

such

as

in

are

intense

and

secretomotor

increased

of

the

ophthalmic

stimulated

light.

lacrimation.

e

or

in

parasympa-

Reex

ner ve

response

aerent

tear-

within

to

pathway

the

external

for

reex

84

blinks.

tearing

A

lacrimal

inner vation

corneal

is

through

the

trigeminal

ner ve,

and

the

eerent

path-

surface

way

is

through

the

parasympathetic

bers

of

the

facial

ner ve.

prevent complete tear lm adherence or if abnormalities exist in the lipid layer

Although causing

increased

it

was

thought

that

accessor y

glands

provided

evaporation.

the

water y

component

of

tear

secretion

and

the

main

lacrimal

CHAPTER

gland

was

primarily

active

during

reex

or

psychogenic

2

Ocular

Adnexa

and

Lacrimal

25

System

stimu-

85

lation,

to

it

is

produce

77

now

the

thought

aqueous

that

all

layer

lacrimal

and

that

glands

production

69

levels

under

conditions

CLINICAL

COMMENT: Dry

Alteration

any

in

eye

or

often

seen

and

a

in

of

may

resulting

and

of

the

the

also

be

in

in

the

lm

and

care

known

caused

as

by

or

a

can

diseases,

eyelid

dry

anatomy

eye,

one

keratoconjunctivitis

deciency

of

between

cause

such

in

cause

hyperosmolarity

aging

87

stimulation.

of

or

lid

the

closure

most

can

common

practice.

interaction

tear

normal

Autoimmune

lm

eye

of

Eye

tear

tear

clinical

change

common,

tion.

layer

syndrome,

etiology

lm

in

depletion

disorders

Dry

stimulus

e rate of production ranges from low levels in sleep

high

result

is

together

86

driven.

to

work

as

the

and

a

any

sicca,

the

layers.

ocular

of

has

layers

complex

the

tear

deciency,

inammation,

aqueous

syndrome,

a

of

Aqueous

surface

decrease

Sjögren

of

tear

rheumatoid

is

produc-

arthritis,

Fig. 2.30 and

systemic

lupus

erythematosus,

can

affect

the

lacrimal

gland

causing

a deciency

struction

in

of

the

the

aqueous

layer.

meibomian

Increased

glands

meibum

resulting

in

viscosity

meibomian

can

gland

cause

The tear lm is seen as a green uorescence through

a

cobalt

blue

lter.

ob-

dysfunction

27

and

evaporative

dry

eye.

Loss

of

lipid

secretion

can

lead

to

alterations

in

Puncta the

to

lipid

dry

layer,

eye

decient

cell

allowing

symptoms

secretion

populations,

ocular

and

and

of

the

such

pemphigoid.

foreign

body

increased

as

evaporation

corneal

mucin

epithelial

layer

chemical

Complaints

are

burns,

of

the

tear

lm

compromise.

associated

with

with

dry

eye

reduced

with

goblet

syndrome,

include

and

Canaliculi

leading

Conditions

Stevens-Johnson

associated

and

and

scratchiness

A

small

aperture,

tissue

elevation,

rimal

and

Both

ciliar y

upper

the

the

and

lacrimal

lacrimal

portions

lower

lids

punctum,

papilla,

of

the

have

a

at

is

the

eyelid

single

located

junction

margin

in

a

of

the

(see

punctum

slight

Fig.

which

lac-

2.2).

drains

sensation.

the

tears

into

the

upper

and

lower

canaliculi,

respectively.

e

88

The

tear

sisting

dry

of

eye

age.

lm

articial

Punctual

dry

be

problems

permanent

to

can

eye

tears

can

plugs

closure

may

augmented

be

are

of

during

be

a

the

by

the

treated

the

day

with

temporary

punctum.

successfully

application

and

of

ointments

procedures

solution,

Ocular

treated

and

at

that

lubricants,

night.

More

decrease

electrocautery

surface

with

ocular

inammation

topical

serious

tear

can

con-

drain-

produce

contributing

antiinammatory

width

e

of

puncta

seen

only

e

join

the

if

lower

are

the

turned

eyelid

canaliculi

the

punctum

puncta

are

to

toward

edge

is

tubes

the

varies

between

the

globe

everted

in

the

lacrimal

and

and

0.9

89

mm.

normally

can

be

slightly.

upper

sac.

0.1

e

and

lower

walls

of

eyelids

the

that

canaliculi

agents,

contain

elastic

tissue

and

are

surrounded

by

bers

from

the

lac-

78

such

as

cyclosporin

or

litegrast

eye

drops.

rimal

rst

portion

portion

mately

Tear

e

Film

the

gland

fornix

globe.

and

uid

and

is

secreted

descends

Contraction

pores

of

mm;

the

the

a

orbicularis

canaliculus

slight

muscle

is

dilation,

(Horner

vertical

the

and

muscle).

extends

ampulla,

is

at

e

approxi-

the

base

of

Distribution

lacrimal

upper

2

of

of

eyelid

the

across

into

the

orbicularis

motion

spreads

the

lateral

anterior

forces

the

thin

part

of

surface

meibum

lipid

the

of

the

out

layer

of

across Canaliculus

(8

mm)

the surface. Each blink reforms the tear lm, spreading it over the

ocular

surface.

At the posterior edge of both upper and lower eyelid margins,

there

is

a

meniscus

of

tear

uid

(Fig.

2.30).

e

meniscus

at

the Nasolacrimal

lower lid is more easily seen. e upper tear meniscus is continusac

(10

mm)

ous with the lower meniscus at the lateral canthus whereas at the

medial

drain

canthus

into

the

them.

the

medial

the

lake

tear

e

canthus.

menisci

lacrimal

e

plica

lead

lake,

a

directly

tear

to

the

reser voir,

semilunaris

makes

puncta

is

up

and

located

the

oor

Canaliculus

(2

mm)

Nasolacrimal

duct

in

(12

Common

canaliculus Valve

and

the

caruncle

Nasolacrimal

Some

tear

uid

is

located

Drainage

is

lost

by

at

its

medial

mm)

of of

Hasner

side.

System

evaporation

and

some

by

reabsorption

through conjunctival tissue, but approximately 75% passes through

76

the nasolacrimal drainage system.

tem

consists

of

the

puncta,

e nasolacrimal drainage sys-

canaliculi,

lacrimal

sac,

and

mal duct, which empties into the nasal cavity (Fig. 2.31).

nasolacri-

Fig.

2.31

Anatomy

of

the

lacrimal

drainage

system.

(From

Kanski JJ. Clinical Ophthalmology. Ed 3, Oxford, UK: Butter worth-

Heinemann;

1995.)

CHAPTER

26

2

Ocular

Adnexa

and

Lacrimal

System

90

the

vertical

portion

of

the

canaliculus.

e

canaliculus

then

t he

blin k.

O t her

stud i es

supp or t

t he

l ack

of

volume

change

94 , 95

turns

horizontally

mately

8

mm

common

lacrimal

at

(see

to

run

Fig.

2.31).

canaliculus

sac

which

and

the

along

that

enters

the

lateral

enters

lid

margin

canaliculi

pierces

the

canaliculus

e

the

to

sac

of

the

a

a

w it hin

single

covering

sac.

produces

approxi-

form

periorbita

aspect

the

join

for

e

the

angle

physiologic

t he

Most

the

l acr ima l

of

duct

the

tears

before

Absorption

s ac.

the

are

absorbed

remaining

through

mucous

by

tears

the

enter

membranes

mucosal

the

is

lining

inferior

ver y

of

meatus.

rapid

and

so

substances, such as drugs, that are present in tears may enter the

96

valve

that

prevents

Lacrimal

Sac

reux.

and

blood

Nasolacrimal

stream

lacrimal

sac

lies

within

the

lacrimal

fossa

in

the

frontal

e

of

e

medial

process

sac

which

the

is

of

orbital

the

surrounded

runs

from

lacrimal

the

sac

is

wall.

maxillar y

by

fascia,

anterior

is

bone

fossa

and

to

the

by

is

by

lacrimal

with

posterior

the

formed

the

continuous

surrounded

body.

CHANGES

the

THE

EYELIDS

AND

SYSTEM

the

bone.

periorbita,

lacrimal

medial

IN

anterior

LACRIMAL portion

the

Duct

AGING e

of

crests.

e

aging

the

skin

tance

canthal

tendon

orbital

septum

gin

is

also

in

process

loses

is

apparent

elasticity,

between

increases

the

and

center

caused

by

of

in

the

eyelids

wrinkles

the

pupil

sagging

of

as

appear.

and

the

the

tissue

With

lower

lower

atrophies,

age

lid;

the

eyelid

this

dis-

mar-

change

97

anteriorly

and

the

behind

is

Horner

check

the

e

it

and

ligament

lacrimal

lacrimal

enters

the

of

sac

sac

of

the

of

15

is

fold

mucosal

uid

up

Tear

Drainage

the

duct

the

and

muscle

lie

valve

of

duct

bone.

terminates

the

greater

eyelid

in

in

the

Hasner

retrograde

just

e

as

duct

inferior

is

changes

levator

movement

of

cavity.

in

the

because

persons.

secretion

tone,

septum

prolapse

by

position

Some

or

by

entropion

age-related

elongation

weakens

nd

age

of

the

stenosis

B oth

studies

aer

and

and

with

changes

of

the

with

age

anteriorly.

eversion

system.

diminishes

ectropion

incidence

orbital

caused

drainage

in

pronounced

muscle

e

to

be

eyelid

lacrimal

elderly

fat

may

More

including

increase

orbicularis

orbital

of

females.

position,

described),

Tearing

the

than

aponeurosis.

allowing

found.

males

margin

(previously

maxillar y

prevents

nasal

rectus

nasolacrimal

the

point,

tissue

from

the

in

long

this

e

10.22).

into

canal

mm

At

medial

Fig.

empties

nose.

posteriorly.

the

(see

nasolacrimal

approximately

meatus

muscle

40

occur

that

the

more

the

years,

lower

of

punctum

passages

in

frequently

basal

rate

of

contributing

in

tear

to

dr y

98,99

During

closure,

the

eyelids

meet

rst

at

the

temporal

canthus.

eye,

the

incidence

of

which

increases

with

age.

Others

have

100

Closure

pool

then

in

the

moves

toward

lacrimal

lake.

the

e

medial

tear

canthus

menisci

where

are

the

pushed

tears

toward

determined

cell

that

population

tear

may

reex

secretion

decrease

over

decreases.

age

80

years,

e

and

a

goblet

decrease

100

the

lacrimal

plays

a

role

puncta

in

into

moving

which

tears

they

into

the

drain.

Capillar y

puncta

and

attraction

down

into

the

in

lysozyme

glands

and

atrophy

lactoferrin

resulting

76

canaliculi

between

One

theor y

noted.

With

decreased

age,

overall

meibomian

gland

secretion

27,101,102

blinks.

and

e underlying mechanism of tear drainage is not completely

understood.

is

in

involves

compression

of

the

canaliculi

ocular

glandular

mian

dr yness.

tissue

secretion

Causative

and

a

change

forming

a

in

more

factors

include

composition

viscous

of

material

the

that

loss

of

meibo-

does

not

41,103

and

expansion

eyes

are

of

closed,

the

lacrimal

Horner

sac

muscle

with

eyelid

contracts

closure.

When

shortening

the

the

cana-

ow

lid

as

easily.

margin

91

en,

upon

canaliculi

tion,

because

muscle

lateral

eyelid

expand

Horner

contraction

opening

pulling

muscle

uid

of

the

in

shares

(occurring

displacement

Horner

from

fascia

when

lateral

the

wall

muscle

the

puncta.

with

eye

of

relaxes,

the

is

the

In

and

upper

vascular

meibomian

gland

engorgement

pores

also

at

the

increases

half

of

the

lacrimal

sac,

creating

sac,

age.

sac,

causes

REFERENCES

expanding

negative

Doxanas

25

pulling

muscle

tears

causes

resulting

in

into

the

lacrimal

contraction

tears

being

of

the

pushed

from

Clinical

Anderson

Orbital

RL.

Eyebrows

Anatomy.

eyelids

Baltimore:

and

Williams

anterior

&

orbit.

Wilkins;

91

sac.

Relaxation

upper

MT,

pressure, In:

and

plugged

of

addi-

lacrimal

closed)

with

1.

the

and

incidence

103

liculi.

the

e

half

the

of

the

lacrimal

of

Horner

lacrimal

sac

sac

the

into

1984:57–88.

2.

Hwang

J

K,

Lee

Craniofacial

JH ,

L im

Surg.

H J.

Anatomy

of

t he

c or r ugator

mus cle.

2017;28:524–527.

25

nasolacrimal

O t her

3.

duct.

t he or ies

p o stu l at i ng

on

t he

me chanism

of

4.

drainage

prop os e

an

i ncre as e

in

pressure

w it h i n

t he

dur ing

lid

BL,

Liu

D,

in

Wit h

e yelid

closure,

t he

S,

w hite

Hsu

surgical

closure.

L am

Walls

RC.

p ers ons.

WM.

Pre valence

Am

Oriental

J

of

palp ebral

O phthalmol.

eyelids,

ssure

asym-

1995;120:518–522.

anatomic

dierence

and

l ac r ima l

92

s ac

L am

metr y

te ar

punc t a

consideration.

Ophthalmic

Plast

Reconstruct

Surg.

r is e 1986;2:59–64.

f rom

t he

lid

marg in

and

b e come

app os e d

and

o c clud e d

ha lf5.

Shams

P ,

Ortiz-Pérez

S,

Joshi

N.

Clinical

anatomy

of

the

periocu-

93

way

into

a

blin k.

The

c ana lic u li

and

l acr i ma l

s ac

are

c omlar

press e d,

forcing

t he

f lui ds

into

t he

nas ol acr i ma l

du c t .

As

st ar t

to

op en ,

compre ssi on

of

t he

c ana li c u li

sure

t he

t he

in

punc t a

t he

remai n

c ana lic u li.

negat ive

pressu re

o cclud e d,

When

pu l ls

t he

t he

c re at i ng

punc t a

te ars

in

a

negat ive

f i na l ly

Plast

Surg.

2013;29:255–263.

Murchison

AP ,

Sires

BA,

Jian-Amadi

A.

Margin

reex

distance

d e cre as e s , in

but

Facial

t he 6.

e yelids

region.

are

pres-

op e ne d,

im me d i ately

af ter

dierent

ethnic

groups.

Arch

Facial

Plast

Surg.

2009;11:

303–305.

7.

Jelks

the

GW ,

Jelks

palpebral

EB.

e

aperture.

inuence

Clin

Plast

of

orbital

Surg.

and

eyelid

anatomy

1991;18(1):183.

on

CHAPTER

8.

Fox

9.

Warwick

the

10.

Eye

e

palpebral

R.

Ocular

and

Stewart

Int

11.

SA.

Orbit.

JM,

Dailey

RA,

7th

Carter

Ophthalmol

ssure.

ed.

SR.

Clin.

Wobig

Am

appendages.

J

Ophthalmol.

In:

Eugene

Philadelphia:

Anatomy

and

32.

1966;62:73.

Wol’s

Saunders;

Anatomy

of

the

33.

Eyelid

Goldberg

visited.

RA,

Whitnall’s

surface

13.

14.

Jeong

anatomy.

coil.

S,

Arch

Lemke

an

eyelid.

Arch

Kakizaki

Kim

cial

16.

YS,

J

Dermatol

Surg

34.

Oncol.

Selva

on

Jakobiec

and

FA,

R,

Fine

Harper

18.

19.

Park

JW ,

fold.

J

A,

K,

and

L,

H,

with

the

use

at

of

e

e

Row ;

etal.

ocular

M,

the

palpebral

Anatomy

S.

37.

Orbital

in

of

septum

Asians

tarsal

adnexa:

eds.

H,

and

38.

and

J

Craniofa-

39.

conjunctiva,

Histolog y.

2nd

40.

Characterization

eyelids.

Eur

J

Y ,

of

an

of

Clin

R,

lower

Esthét.

etal.

eyelid

Ophthalmol.

Ichinose

A,

etal.

of

43.

canthal

raphe

YS,

Kim

and

DJ,

lateral

Kakizaki

the

medial

mol.

24.

Poh

E,

in

sac

or

Y ,

Anatomic

palpebral

Zako

study

ligament.

of

Ann

the

lateral

Plast

44.

by

drainage

H,

lacrimal

Horner’s

Clin

the

of

etal.

e

does

it

Anatomy

posterior

exist.

etal.

e

muscle

Am

R,

Y asutaka

S,

orbicularis

Okajimas

Folia

medial

J

limb

Ophthal-

45.

Knop

E,

meibomian

anatomy,

gland.

28.

anatomy

and

the

Eye.

Wobig

mol.

31.

WM

JL.

of

Jr.

T,

and

the

46.

MJ,

physiolog y.

the

Eye.

9th

ed.

St

e

etal.

oculi

Anat

functional

e

anatomy

muscle

Jpn.

47.

Louis:

Sci.

tarsi

48.

St

of

JP ,

the

PL,

the

on

Alm

Jr,

ed.

and

R,

RL,

B e ard

t heir

1977;95:1437.

MM,

KA,

Shin

JL,

Wirtschaer

American

JD,

Academy

of

anatomical

ligament.

Kor

study

J

of

the

Ophthalmol.

etal.

Levator

palpebrae

superioris:

2013;32:76–84.

Sib ony

d at a.

SY .

Anat.

PA.

Inv

Eyeli d

movement s :

O phthalmol

Vi sual

S c i.

RJ,

Detailed

anatomy

of

the

capsulopal-

2012;25:709–713.

RK.

retractors.

Linberg

Itoh

with

e

Arch

Selva

JV ,

microscopic

Ophthalmol.

D,

etal.

McCormick

tendon.

K,

Inoue

decrease

Stoeckelhuber

of

Moll:

of

the

of

Arch

anatomy

of

the

1982;100:1313.

Tarsal

K,

SA.

height.

e

Ophthalmol.

etal.

Contact

meibomian

M,

Stoeckelhuber

histochemical

glands

Knop

in

E,

of

Knop

vivo

wip er

Moll

N,

and

in

Ophthalmol-

anatomy

of

the

1987;105:529.

lens

glands.

wear

is

associ-

Ophthalmolog y.

BM,

Welsch

ultrastructural

the

Zhivov

junc tion

confo cal

and

Wirtschaer

MCJ

Knop

Efron

Li

N,

eds.

the

N,

human

A,

U.

Human

glands

characterization

eyelid.

etal.

anatomy

and

of

of

e

t he

J

Inv

human

lid

Dermatol.

wip er

human

histolog ical

t he

Au

51.

J

the

JM,

major

epithelial

Visual

to

study :

e yelid

and

e yelid

muco-

margins:

anatomy

margins.

Weinstock

source

cells.

Inv

J

of

t he

Anat.

of

RJ,

etal.

Mucocu-

replacement

Ophthalmol

palpe-

Visual

Sci.

of

Nichols

and

Dilly

B,

etal.

JD,

in

e

Visual

Visual

Sci.

Sci.

wiper

contains

surface

lubrication

Lid

wiper

epitheliopa-

relationship

and

of

lid

symptoms.

wiper

Inv

epi-

Ophthal-

the

RR,

of

mucin.

conjunctiva),

(Quan-

(Preliminar y

1966;44:439.

etal.

human

Presence

of

ner ves

conjunctival

Spurr-Michaud

in

the

goblet

and

cells.

ocular

SJ,

etal.

surface

Charac-

glycocalyx.

Inv

1992;33:218.

Togni

B.

Ophthalmol

nature

epithelial

conjunctival

2001;42(10):2270.

M,

CR,

Inv

the

cells

and

glycoprotein

On

etal.

(Copenh).

Hodges

mouse

Dawson

outer

PB,

signs

of

goblet

Ophthalmol

cornea.

PN.

the

the

Y ankauckas

a

lid

ocular

2018;59:1878–1887.

Ophthalmol

of

Morgan

T,

Rios

IK,

e

for

2016;53:140–174.

Investigations

Acta

etal.

2012;31:668–679.

surface

receptors

Gipson

NA,

Res.

CA,

cr ypts

Leung

studies

Y ,

cell

ocular

Sci.

SV .

Diebold

in

Ophthal-

Eye

TN,

Blackie

Cornea.

Brennan

Y eh

Kessing

tiva

Physiolog y

NZ

as

goblet

blink.

Ophthalmol

Adler’s

52.

repair.

Ketcham

DR,

and

Retin

teristics

facial

2003.

Adler’s

Korb

cells

Pro

W ,

Inv

50.

A,

JD,

junction

conjunctival

their

on

1992.

ptosis

49.

meibomian

Ophthalmic

Mosby ;

WM

Mosby ;

for

workshop

subcommittee

of

etal.

Louis:

Hart

technique

S-H,

Clin

canthal

titative

and

cells

the

of

Surface

Visual

role

the

of

features

Sci.

the

of

the

conjunc-

1983;24:570.

subsurface

conjunctiva.

Br

J

vesicles

Ophthalmol.

1985;69:477.

1989;17(2):125.

ments

VM,

Arita

mol

of

(tensor

2011;52:1938.

Kaufman

ed.

In:

cadaveric

Orbit.

nor ma l

Casson

theliopathy

2001;77(6):225

international

report

Shovlin

In:

10th

eyelids.

Surgical

Anders on

Gioia

thy.

canaliculus

2005;112:710–716.

pathophysiolog y

Visual

Lucarelli

e

etal.

dysfunction:

Ophthalmol

DO,

of

30.

gland

Kikkawa

Hart

Millar

physiolog y,

Inv

Physiolog y

29.

N,

A

Whitnall’s

Marcet

Dortzbach

LA,

report).

Knop

YJ.

and

update.

and

Han

MJ,

during

canthal

(Abstract).

27.

Wobig

Francisco:

1999;40(13):3138.

in

2012;40:170–173.

lacrimal

form

Ophthalmolog y.

the

of

Ophthalmol.

O,

Horner’s

Kominami

muscle).

Exp

Miyaishi

system.

portion

T,

Asians:

etal.

MJ,

muscles

2009;116:1831–1831.e2.

goblet

D,

Lee

Man n i ng

eyelid

taneous

Surg.

e1.

Selva

M,

in

San

the

2011;218:449–461.

etal.

Nakano

tendon

Caucasians.

H,

Shinohara

the

H,

bordered

lacrimal

26.

canthal

Kakizaki

Kakizaki

and

Takahashi

Reeh

of

1981:38.

DJ,

W ,

fascia.

Goold

bral

2010;150:741–743

tendon

25.

H,

YS,

Hawes

lid

2009;62:232–236.

23.

Nam

an

anatomy :

2012;31:279–285.

Nam

C,

c ut aneous

palpe-

2009:391–393.

Lateral

In:

Structure

1975;93:1189.

2003;121(1):28.

eyelid–

lateral

CC.

27

System

2009;116:379–384.

epicanthal

2017;62:365–374.

Absence

Chan

Ev inger

ated

of

Ophthal-

and

Paik

Johnson

Ophthalmol.

Anatomy.

aponeurosis

SK,

lateral

ed.

41.

etal.

histolog y

Plast

Malhotra

eyelids.

anatomical

lower

2016;27:1101–1103.

Chirurg

K,

Ng

pebral

attach-

whites.

plates.

lids,

Ocular

human

Anatomy

Caucasians.

Orbit.

K,

HW ,

DG,

Arch

Lacrimal

1991;32:387.

Caucasian

1979:290.

in

e

me chanisms

upper

2010;26:265–268.

height

Elnaddaf

Surg.

Takahashi

review.

Hwang

Lim

an

a

36.

Asian

to

35.

42.

Ann

Kakizaki

in

JL.

Ophthalmic

og y.

Y ano

M,

Cotofana

junction.

raphe

Kang

a

22.

etal.

comparison

Surg.

receptors

K.

Craniofacial

Goold

bral

21.

&

2α

Hwang

Mojallal

Wobig

eyelid.

and

2009;23:183–187.

re-

images

2015;25:81–84.

cheek

20.

F

T.

BS,

Mimouni

prostaglandin

mol.

structures

aponeurosis

Shape

Iwamoto

In:

Y ork:

Nesher

anatomy

resonance

1999;117:907.

Reconstruc

K.

RK,

with

Asamoto

levator

Plast

Eyelid

2016;27:496–497.

orbit.

New

17.

the

D,

etal.

1992;110(11):1598.

Dortzbach

study

A,

magnetic

eyelid

Ophthalmol.

BN,

Hwang

Surg.

upper

Ophthalmol.

H,

sites

Jesmanwicz

and

anatomical

Ophthalmic

15.

JC,

high-resolution

ligament

eyelid:

ment

Wu

Cogan

upper

levator

Dynamic

T,

Adnexa

Ophthalmolog y ;

1993;18:1023.

12.

the

eds.

eyelids.

2002;42(2):1.

JL.

Ocular

Kuwabara

of

of

1976:181–237.

examination

2

C.

clinic a l

e

le vator

ap oneurosis.

sig nic ance.

Arch

Att ach-

O phthalmol.

53.

Sullivan

aer

WR,

vitamin

thalmol.

McCulley

A

therapy

1973;75:720.

JP ,

in

Dohlman

xerosis

of

CH.

the

Return

of

goblet

conjunctiva.

Am

J

cells

Oph-

CHAPTER

28

54.

Kim

EC,

sporine

Am

55.

J

Choi

A

JS,

0.05%

Ophthalmol.

Kruse

FE,

Tseng

dierentiation

lium.

56.

Inv

Steuhl

KP ,

Sitz

Ophthalmol.

A l lensmit h

mator y

A

comparison

for

Retinoic

cultured

U,

cells

CK.

Adnexa

treatment

2009;147:206–213.

SC.

of

Ocular

drops

Ophthalmol

Langerhans

57.

Joo

eye

2

limbal

Visual

Knorr

within

acid

Sci.

M,

Lacrimal

of

vitamin

of

dr y

eye

A

and

System

cyclo-

76.

1992.

clonal

peripheral

growth

corneal

77.

and

tival

1994;35:2405–2420.

Age-dependent

conjunctival

cel ls

in

Grei ner

t he

JV ,

nor ma l

B ai rd

RS.

Numb er

c onjunc t iva .

Am

J

of

78.

Clayton

79.

Hosaka

80.

O phthalmol.

Jakobiec

Foundations

of

Knop

Chin

Ocular

In:

Clinical

adnexa:

T asman

W ,

introduction

Jaeger

Ophthalmology,

vol.

EA,

1.

to

81.

eye.

E.

Inv

Chi

of

Conjunctiva-associated

Ophthalmol

EY ,

Bunt

A.

conjunctival

Visual

Sci.

tissue

in

and

Arch

W eingeist

82.

Ocular

62.

Sirigu

the

e

Structure

P ,

Shen

Efron

of

Sci

64.

J.

N,

66.

LeDoux

IA.

eds.

of

Anat.

D ar tt

eyelid.

Brown;

KM,

by

thin

glands:

section

microscopes.

Inv

DA,

Seifert

P ,

Ho d ges

J.

MJ,

St

N.

In

vivo

tarsal

puzzle:

RB,

confocal

plate.

85.

86.

rats.

pieces

together.

Parasympathetic

Inv

Ophthalmol

MJ,

accessor y

87.

inner-

88.

Visual

Len.

Sci

89.

meibo-

MJ,

G,

Z ou k h r i

Biolog y

S,

J

SD.

Akpek

of

Bitton

in

C,

etal.

human

90.

Immunolo-

glands

of

N,

Doğan

on

Clin

M.

ner ve

Y .

e

LC,

acinar

gland

and

in

2009;35:203–208.

etal.

Interferometr y

thickness

in

dr y

eye.

in

Am

J

etal.

Measurement

Visual

t he

a

Sci.

optical

of

tear

coherence

2013;54:5578–5583.

pre cor ne a l

c ont i nuous

te ar

te ar

(C ope nh).

f i lm .

f i lm

Fac tors

over

in

t he

1965;8(suppl

Tong

ocular

BMC

L.

Intra-obser ver

surface

Ophthalmol.

Dohlman

CH,

Am

inter-obser ver

in

measuring

lipid

2015;15:53.

Kuwabara

Trans

and

interferometer

T,

Acad

etal.

Dr y

eye

Ophthalmol

secondar y

Otolar yngol.

Hamill

eyes.

LT.

Arch

JR.

Factors

aecting

Ophthalmol.

Anatomy

of

the

tear

tear

lm

breakup

in

1973;89:103.

system.

Int

Ophthalmol

Clin.

Takahashi

Y ,

glands

Jordan

A,

Watanabe

in

the

Plast

Baum

A,

eyelid

Matsuda

and

Reconstruc

JL.

Basic

H,

etal.

conjunctiva:

Surg.

tear

a

Anatomy

of

secre-

photographic

review.

2013;29:215–219.

ow.

Does

it

exist.

Ophthalmolog y.

Wawrzynski

JR,

tomography

imaging

Smith

J,

of

Sharma

the

A,

etal.

proximal

Optical

lacrimal

coherence

system.

Orbit.

e

of

Wolfring

in

91.

Te ars

Eye.

and

vol.10.

t hei r

in

pattern

accessor y

Ocular

M,

eyelash

Kabataş

and

A,

Keane

Ta k a h a s h i

of

Acta

Y,

Pharmacolog y.

94.

Blepharitis

features

EU,

the

etal.

the

Pearce

and

of

symptoms.

EI,

etal.

Tear

Eye

MJ,

H,

Characterizing

segment

optical

the

lac-

coherence

2016;94:154–159.

Na k a n o

c a n a l i c u lu s

and

O pht h almi c

HS,

Ha n

MH,

me chan is m

the

Dartt

PL,

Alm

Mosby ;

MG.

Al-Faky

anomalies:

95.

Wu

T,

eta l.

lacr ima l

P l a st

eta l.

us i ng

O pht h almi c

DA,

A,

A n at omy

of

pu n c t u m :

R e c on s t r u c

t he

a

Sur g .

Ev a lu at i on

dy nam i c

P l a st

of

lacr ima l

f lu oro s c opi c

R e c on s t r u c

Sur g .

and

Ophthalmolog y.

YH.

Cook

eds.

BE,

Adler’s

etal.

e

lacrimal

Physiolog y

of

the

system.

Eye.

10th

In:

ed.

2003.

Blinking

the

drainage

mechanics

of

the

lacrimal

drainage

1981;88(8):844.

Physiological

lacrimal

sac.

demodex

Eye

Cont

96.

W ,

and

meibomian

Contact

Lens.

97.

J

van

Dis

BL.

Med

den

the

Y ,

Chen

closing

Eye

Selvin

of

Tu

and

South

normal.

etal.

utility

of

system. Br

ultrasound

J

biomicroscopy

Ophthalmol.

2013;97:

1325–1329.

and

eect

Ky u n g

Louis:

Doane

ing

ocular

AC,

anterior

Ophthalmol.

s tu d y.

d r ai nage

Lucarelli

in

Preferred

2019;126:56–93.

follicle

M J,

system.

ed.

1995:583.

etal.

Lee

St

glands.

3rd

Day

using

Ka k i z a k i

lacr ima l

Kaufman

ner vous

lacrimal

PA,

region

2011;27:164–167.

2017;43:64–67.

blepharitis

HM,

punctal

d a c r y o c y s t o g r ap hy.

s e c re t i on .

Amsterd am :

2018;11:211–222.

AŞ,

Timlin

2011;27:384–386.

ductal

93.

Farid

Tomlinson

function

Jones

te ar

Distribution

bers

Clinical

blepharitis

Pract.

S,

O phthalmol

deciency.

MA,

ve r t i c a l

Moll.

92.

EK,

E.

of

tomography.

2005.

lacrimal

D.

the

Ophthalmolog y.

Optomet.

Lemp

rimal

Holland

1997;16:298.

Pattern®.

McCann

gland

and

Mannis

1999;68(4):411.

Butter worth-Heinemann;

Amescua

CLS,

m a c ro s c opi c

Blocker

Boston:

Kabataş

JH,

Schubert

JD,

review.

Seborrhea

Mosby ;

EM,

Bartlett

Aumond

EJ.

cathelicidin

Spitznas

Jaanus

Y ,

lm

1980;95:1.

Krachmer

Louis:

Res.

peptidergic

Res.

MA,

mucous

tor y

Vision

2006:18–8 2.

S,

Tan

thickness.

normal

microsco-

Optomet

combining

etal.

in

Holland

In:

and

RR ,

The

2018;378:2212–2223.

e1.

Ophthalmol

Ac ta

conjunc-

2014;33:428–432.

tarsal

Eye

tear

maint ai n i ng

lacrimal

and

1971;75:1223.

84.

and

Ophthal-

Med.

Kaya

of

main

corneal

2016;61:616–627.

Ogasawara

A,

the

ultrahigh-resolution

t hi ck ness

and

Ophthalmic

Messmer

the

Stuppi

and

Eye

1.

Inv

sur face.

Y ,

Lemp

to

ed.

1973:243.

meibomian

J

Is

the

1973;13(1):3.

and

glands

Doughty

Exp

Fis chb arg

infestation

75.

viewed

Zinn

2008;190:230–237.

of

a

Little,

Human

as

Pritchard

Murphy

defensins

organization

Practice

74.

Q,

vol

M,

JP ,

Curr

73.

P .

In:

2009;28:483–498.

Mannis

Bergmanson

tissue

72.

M,

dysfunction.

Cornea.

E ls e v ier ;

71.

Boston:

electron

meibomian

Res.

Zhou

JH,

gland

rabbit

70.

cells

conjunctiva

meibomian

Stoeckelhuber

In:

acinar

adnexa.

2001;42(11):2434.

Ann

69.

e

the

calization

68.

Clinician.

transmission

Eye

MS,

of

Krachmer

EJ,

ocular

1992;33(7):2284.

palpebral

Retinal

mian

67.

the

Zhao

layer

Ophthalmol.

2009;86:1303–1308.

vation

Sci.

Sci.

of

Al-Dossarit

the

Butovich

Pro

65.

Visual

the

of

Pinto-da-Silva

ultrastructure

mol

py

for

RL,

freeze-fracture

63.

glands

T,

Alex

using

The

repeatability

histochemical

83.

TA.

Engl

M.

of

81):92.

the

2000;41:1270–1279.

Ultrastructure

concretions.

lymphoid

1980;98:720.

61.

N.

spre ading

Lip-

N

precorneal

RM,

thickness

E h lers

Ophthalmol.

eye.

of

Wang

2011;151:18–23.

tomography.

lids,

eds. Duane’s

Philadelphia:

Dr y

S,

Contributions

Kawamorita

Werkmeister

cor ne a l

Knop

GN,

studies

T .

orbit.

1994.

N,

human

60.

Iwamoto

and

pincott;

59.

FA,

Surv

evaluation

lm

conjunctiva,

JA.

E,

Ophthalmol.

i n f l am-

Pugazhendhi

epithelia.

of

the

W ,

indispensable?

German

distribution

epithelium.

1978;86:250.

58.

Stevenson

gland

epithe-

1995;92(1):21–25.

MR ,

Lemp MA, W oley DE. e lacrimal apparatus editor. In: Hart

WM Jr, ed. Adler’ s Physiology of the Eye. 9th ed. St Louis: Mosby;

syndrome.

e3.

regulates

and

et al.

human

and

on

Y ,

Disord.

Systemic

J.

A

Study

volume

and

of

the

impact

morpholog y

of

of

eyelid

the

open-

lacrimal

2018;4:1–6.

eects

of

topical

ophthalmic

medications.

1983;76:349–358.

Bosch

eyelids,

1999;83:347.

etal.

the

W A,

and

Leenders

the

eects

I,

of

Mulder

P .

sex

age.

and

Topographic

Br

J

anatomy

Ophthalmol.

CHAPTER

98.

Lin

an

PY ,

Tsai

elderly

SY ,

Cheng

Chinese

Ophthalmolog y.

99.

Schaumberg

of

dr y

eye

CY ,

etal.

population

Prevalence

in

Taiwan:

of

the

dr y

eye

Shihpai

among

Eye

DA,

Sullivan

DA,

among

Buring

US

Van

mol.

Haeringen

NJ.

JE,

women.

etal.

Am

J

Prevalence

102.

1997;81:824–826.

and

the

lacrimal

system.

Br

J

Ophthal-

Cox

R,

Fukuoka

SM,

Ocul

Ophthalmol.

103.

Aging

Arita

Adnexa

and

S,

and

Lacrimal

Morishige

function

of

N.

New

29

System

insights

meibomian

into

glands.

the

Exp

Eye

Res.

2017;163:64–71.

2003;110(6):1096.

syndrome

Ocular

morpholog y

study.

2003;136(2):318.

100.

101.

2

Den

Nichols

Sur f.

S,

mian

JJ.

e

neurobiolog y

of

the

meibomian

glands.

2014;12:167–177.

Shimizu

gland

K,

Ikeda

changes

2006;25:651–655.

and

T,

etal.

aging,

Association

sex,

or

tear

between

function.

meibo-

Cornea.

3

Cornea

e

outer

connective

tissue

coat

of

the

eye

has

the

appearance

CORNEAL of

is

8

two

joined

the

spheres.

cornea

mm.

e

and

e

has

larger,

a

smaller,

radius

posterior

of

anterior

transparent

cur vature

opaque

sphere

of

is

approximately

the

sclera,

which

e

cornea

tance.

sclera

lm,

globe

are

at

24.5

the

mm

limbus.

e

approximate

anteroposterior,

24

mm

diameters

vertical,

and

of

24

the

mm

is

transparency

has a radius of approximately 12 mm (Fig. 3.1A). e cornea and

merge

ANATOMY

AND

HISTOLOGY

sphere

e

and

the

principal

and

anterior

the

refracting

avascularity

surface

posterior

of

the

surface

component

provide

optimal

cornea

borders

is

the

of

the

light

covered

eye.

Its

transmit-

by

the

aqueous-lled

tear

ante-

rior chamber. At its peripher y, the cornea is continuous with the

1–3

horizontal;

these

do

not

change

much

beyond

age

1

year.

conjunctiva

layers

that

stroma,

CORNEAL

e

the

the

Descemet

sclera.

the

From

cornea

membrane,

anterior

are

and

to

posterior,

epithelium,

the

Bowman

endothelium

(Fig.

ve

layer,

3.3).

DIMENSIONS

transparent

sclera

and

compose

cornea

encroaches

appears

on

the

from

superior

the

and

front

to

inferior

be

oval,

aspects.

as

e

Epithelium

e

outermost

corneal

layer

is

stratied

corneal

epithelium

of

9

anterior

horizontal

diameter

is

12

1

diameter

cornea

is

11

mm

appears

(Fig.

circular,

2

mm,

the

anterior

vertical

ve

to

seven

It

further

cells

thick

and

measuring

approximately

50

10

µm.

4

3.1B).

with

and

If

viewed

horizontal

from

and

behind,

vertical

the

diameters

is

broken

down

into

surface

squamous

cells,

wing

cells,

and basal columnar cells. e epithelium thickens in the periphery

1

of

11.7

In

mm.

and is continuous with the conjunctival epithelium at the limbus.

prole,

cal

shape,

ter

near

cornea

the

the

at

the

cornea

cur vature

peripher y.

the

anterior

1

surface

is

has

6.5

5

an

being

e

elliptic

steeper

radius

surface

is

of

7.8

rather

in

the

than

center

cur vature

mm

a

and

of

at

spheri-

and

the

the

at-

central

e

two

It

surface

cells

consists

posterior

contains

is

deeper

squamous

thick

a

of

and

cell

displays

nonkeratinized

attened

nucleus

layer

a

of

ver y

corneal

smooth

squamous

and

fewer

epithelium

anterior

cells,

cellular

each

is

surface.

of

which

organelles

than

6

mm.

e

central

corneal

thickness

535

to

cells.

Cell

size

varies

but

a

supercial

cell

can

be

50

μm

11

555

μm,

whereas

the

corneal

peripher y

is

640

to

670

μm

thick

in

diameter

and

5

μm

in

height.

e

plasma

membrane

of

the

7–9

(Fig.

3.1C).

surface

epithelial

adjoins

will CLINICAL

Astigmatism

imaged

mucin

in

is

as

a

condition

a

single

in

which

point.

This

light

rays

results

coming

from

from

unequal

a

point

refraction

source

of

apical

curvature.

retina,

not

determined

give

an

est

that

occurs

of

when

the

the

meridian

(Fig.

3.2B)

contain

90

30

the

when

greatest

degrees),

in

which

degrees

is

but

of

lie

or

the

in

of

the

the

oblique.

of

the

tear

lm.

Many

Loss

component

of

the

projections

that

glycocalyx

located

enhancing

the

are

45-

not

and

by

Irregular

meridian

(Fig.

meridian.

the

the

the

can

These

If

is

be

cells

increase

the

on

surface

area,

also

projections

Tight

are

(Fig.

stability

microvilli,

of

and

the

the

tear

lm.

ridgelike

e

nger-

projections

are

3.4)

junctions

(zonula

occludens)

join

the

surface

cells

12

along

their

lateral

walls,

near

the

apical

surface.

ese

junc-

will

and

axes

is

a

greatest

short-

presenta-

differs

Thus

the

and

3.2A),

steepest;

180-

astigmatism

to

common

Against-the-rule

is

rays

surface

surface

curvature

most

135-degree

corresponding

of

meridian.

along

the

light

outermost

tures

provide

a

from

the

layer

barrier

to

intercellular

movement

of

substances

astigmatism.

vertical

meridian

horizontal

corneal

astigmatism

vertical

focus

measurements.

to

The

the

helps

because

the

radius

apart.

curvature.

horizontal

along

longest

and

eye

of

topography

With-the-rule

lies

the

contribution

curvature

radius

in

of

light

curvature

degrees

differences

meridians

apart.

90

the

found

called

the

when

curvature

shortest

is

of

corneal

meridian.

occurs

the

lie

refracts

astigmatism

radius

the

radius

power

which

keratometry

occurs

the

steepest

to

The

of

curvature

when

astigmatism

ing

by

horizontal

has

refractive

(±30

clinically

of

cornea,

contributes

spherical.

astigmatism

radius

tion

The

approximation

Regular

glycocalyx

are

light

microplicae

the

the

a

stability.

the

radius

generally

of

tear

of

like

onto

layer

poor

surface

different meridians of the refracting element, each meridian having a different

of

secretes

COMMENT: Astigmatism

the

not

the

result

cells

the

lm.

produced,

cells

cells

but

is

A

highly

allowing

not

by

the

eective,

passage

between

provided

prevent

of

them.

uptake

excess

semipermeable

uid

and

uid

from

membrane

molecules

Additional

numerous

of

adhesion

through

between

is

the

the

desmosomes.

vertical

the

greatest

90-degree

less

tear

and

astigmatism

meridians

(±15

from

occurs

the

tear

that

axes

degrees),

common

differences

the

nd-

are

not

CLINICAL

Fluorescein

layer.

as

When

long

as

COMMENT: Evaluation

dye

can

be

instilled

the

zonula

in

used

the

to

tear

occludens

of

evaluate

lm,

are

it

will

intact.

Corneal

the

barrier

not

If

Surface

function

penetrate

the

tight

the

of

the

surface

epithelial

junctions

are

tissue

disrupted,

the dye can pass easily through Bowman layer and into the anterior stroma. An

epithelial

with

the

defect

cobalt

will

blue

usually

lter

of

appear

the

slit

a

vivid

lamp

green

(Fig.

3.5).

uorescence

when

viewed

CHAPTER

cells

(Fig.

3.6).

e

diameter

of

a

3

31

Cornea

wing

cell

is

approximately

mm

11

20

μm.

21

e ach

D esmos omes

ot her,

and

and

gap

desmos omes

junc tions

join

wing

join

cells

wing

to

cells

sur face

to

and

13

bas al

cells.

The

inner most b as a l

a

sing le

8

to

l ayer

of

c el l

columnar

l ayer of

c el ls,

t he

w it h

cor ne a l

epit helium

d i ameters

r ang ing

is

f rom

11

8

mm

10

μm

displ ace d

sur face.

cent

(Fig .

The

to

t he

Thes e

t he

ap ex

round e d,

w ing

underly ing

less

3.7).

toward

numerous

api c a l

cel ls ,

and

b as ement

here

and

gap

and

desmos omes

cont ain

or ie nte d

sur face

t he

b as a l

membrane

t han

junc t ions

cel ls

and

j oi n

in

t he

t he

ova l- shap e d

at

of

r ig ht

e a ch

su r fa ce

( b as a l

w ing

c el l

att aches

l ayer,

cel ls .

to

l i es

l ami na) .

cel l

c olumnar

nucl ei

ang les

t he

adj a-

to

t he

A lt houg h

d esmos omes

Interd i g it at ions

A

l ayer

of

w ing

e

mm 1 1

12

basal

attaches

From

the

the

t he

cells

cells

secrete

to

the

b as a l

the

cel ls

w it h

network

basement

underlying

hemidesmosomes,

branching

mm

con ne c t

t he

adj ac e nt

cel ls.

that

tissue

anchoring

runs

from

membrane,

which

by hemidesmosomes.

brils

the

form

basal

a

complex

epithelial

cells,

14

through

If

the

Bowman

basement

layer

to

penetrate

membrane

is

into

damaged,

the

anterior

healing

of

stroma.

the

epithe-

15

lium

can

take

up

to

6

weeks.

B CLINICAL

Recurrent

anchoring

cally

COMMENT: Recurrent

corneal

brils

slough

basement

tissue.

are

off.

There

Recurrent

dystrophy.

is

or

a

or

Matrix

causing

in

attachment

may

can

be

Erosion

which

the

basement

erosion

it

Corneal

condition

poor

the

corneal

abrasion

is

abnormal

membrane

supercial

brane

erosion

the

corneal

between

membrane

occur

caused

after

by

an

metalloproteinases,

hemidesmosomes

epithelium

the

and

epithelium

incomplete

and

its

stromal

healing

basement

normally

or

periodi-

underlying

epithelial

which

to

of

a

mem-

maintain

the

extracellular matrix by causing degradation and remodeling, are upregulated

in

recurrent

corneal

erosion

and

may

cause

this

break

down

of

the

epithelial

16

attachments.

Age-related

535

to

555

µm

epithelium

thickness

changes

can

continues

of

the

to

play

a

secrete

basement

role

the

in

recurrent

basement

membrane

corneal

erosion.

membrane

doubles

by

60

The

throughout

years

of

age.

In

corneal

life.

The

addition,

17

reduplication

basement

membrane

of

640

to

670

be

Corneal dimensions. A, Radius of curvature of cornea and

the

front

of

the

eye. The

sclera

encroaches

on

the corneal periphery inferiorly and superiorly . Dotted lines show the

extent

of

section

the

of

cornea

cornea

in

the

showing

vertical

central

dimension

and

posteriorly .

peripheral

used.

C,

Sagittal

epithelium

surface

without

For

cases

middle

t hree

layer

layers

of

of

t he

cor ne al

w ing

cel ls.

epit helium

es e

cells

is

made

have

up

in

treatment

sion

to

are

which

pro cess es,

in

the

and

are

concave

p oly hedral,

p oster ior

and

sur faces

have

t hat

can

reduplication

of

the

occur

with

occurs,

anchoring

the

brils,

aging.

As

thickness

allowing

the

of

the

sloughing

to

can

tear

to

shearing

the

prevent

thins

from

effect

multiple

topical

pain

from

cause

is

of

cells

eyelid

while

opening

a

faulty

may

Bandage

the

basement

to

may

to

the

membrane,

membrane

or

the

of

adhe-

corneal

epithelial

tissue

breakdown

soft

of

eyelids.

enhance

through

the

require

healing

closing

scar

sensory

adhering

cases

tissue

made

reduce

from

and

of

treatments

allowing

subepithelial

may

of

infection.

basement

are

network

Acute

defective

the

and

producing

steroids

the

dense

number

overnight.

perforations

by

A

opportunistic

debridement

epithelial

the

disrupted.

alleviate

suspected

adhesion

or

because

help

lm

protect

applied

is

(Fig.

the

3.8).

bonds

of

the

epithelium

and

basement

membrane

by

inhibiting

matrix

me-

wing-li ke

convex

t

the

basal

which

induce

tetracycline

over

Autologous

anter ior epithelial

sur faces

membrane

as

painful

night

include

talloproteinases.

lateral

the

or

length

very

as

the

might

between

between

to

of

epithelium

at

ointment

lenses

Oral

e

the

are

the

Ointment

puncture

thickness.

in

contact

layers

two

exceed

erosions

antibiotic

C

from

areas

thickens

layers.

endings

corneal

B, View

can

epithelial

nerve

sclera.

focal

µm

Corneal

Fig. 3.1

in

membrane

t he

bas al

attachment.

serum

supplies

bronectin

which

promotes

CHAPTER

32

3

Cornea

A

B

Fig. 3.2

Corneal

wavelength

colors

indicate

corneal

e

topography

red)

a

Patrick

indicate

atter

astigmatism.

(Courtesy

Bowman

(i.e.,

B,

showing

areas

corneal

Corneal

Caroline,

of

a

map

steeper

cur vature.

A,

topography

C.O.T .,

Pacic

layer

the

corneal

Corneal

University

the

cornea

is

approximately

8

to

19

μm

the

of

in

Optometr y,

rather

that

it

Colors

shorter

demonstrating

against-the-rule

stroma

stroma

curvature.

whereas

topography

College

the

of

surface

cur vature,

demonstrating

Layer

second

of

corneal

Forest

than

is

corneal

a

longer

with-the-rule

astigmatism.

Grove,

true

acellular

of

wavelength

OR.)

membrane.

and

contains

It

diers

collagen

from

brils

the

of

a

8–10

thick

a

(Fig.

dense,

brous

arranged

a

in

diameter

not

3.9).

a

of

ordered

Bowman

sheet

of

into

to

25

(anterior

inter woven

mucoprotein

20

layer

ground

nm,

bundles.

run

in

B owman

limiting

collagen

brils

substance.

various

layer

e

lamina)

randomly

brils

directions,

sometimes

is

is

have

and

are

referred

smaller

lar

and

diameter.

reects

epithelium.

brils

e

the

pattern

contour

Posteriorly,

gradually

adopt

as

a

of

the

of

the

the

bases

layer

more

anterior

of

surface

the

transitions

orderly

basal

into

is

irregu-

of

the

stroma,

cells

the

arrangement

and

to merge into bundles that intermingle with those of the stroma

18

to

as

a

membrane,

but

it

is

more

Cor neal

correctly

a

transition

layer

to

(Fig.

3.10).

e

posterior

epithelium

Cor neal

surface

Bowman

not

clearly

stroma

endothelium

Anterior

is

layer

Descemet

Cor neal

chamber

Fig.

3.3

Light

begin

micrograph

of

corneal

layer s.

membrane

dened.

CHAPTER

CROSS-SECTIONAL

VIEW

OF

THE

CORNEAL

EPITHELIAL

tear

CELL

3

33

Cornea

LAYER

film

glycocalyx

apical

layer

microvilli

superficial

cells

wing

cells

basal

cells

basement

hemidesmosomes

membrane

Fig.

M,

3.4

Cross-sectional

Soong

HK.

Corneal

view

of

Anatomy,

tight

the

junctions

corneal

Physiology,

epithelial

and

cell

Wound

layer.

healing .

(From

In:

Farjo

Y anoff

M,

A,

Mc

Duker

Dermott

JS,

eds.

rd

Ophthalmology,

B owman

and

is

layer

not

layer

is

believed

usually

is

produced

to

replaced

3

ed.

prenatally

regenerate.

by

St

Louis,

by

the

erefore

epithelial

cells

or

MO:

if

Mosby;

20 08,

epithelium

injured,

stromal

scar

Figure

layer

4.1 .1).

and

the

No

tis-

B owman

whether

long-term

it

is

eects

layer

necessar y

have

removed

been

by

to

maintain

corneal

documented

photorefractive

in

function.

patients

keratectomy,

a

with

pro-

19

sue.

However,

shearing,

B owman

penetration,

layer

or

is

ver y

infection.

resistant

Although

to

damage

B owman

by

layer

cedure

is

Corneal

thought to provide biomechanical rigidity and shape to the cor-

lose

nea,

as

speculation

continues

regarding

the

function

of

B owman

performed

their

naked

since

ner ves

Schwann

ner ves

the

corneal

the

conjunctiva

late

passing

cell

(see

the

1980s.

through

covering

Fig.

peripher y

or

the

3.6).

and

and

B owman

pass

Bowman

does

not

into

layer

have

a

layer

the

tapers

typically

epithelium

and

counterpart

ends

in

at

either

sclera.

Stroma

e

middle

layer

of

the

cornea

is

approximately

450

to

500

μm

9,11,20

thick, or about 90% of the total corneal thickness (see Fig. 3.3).

e corneal stroma (substantia propria) is composed of collagen

brils,

keratocytes,

and

extracellular

ground

substance.

e collagen brils have a uniform 25- to 35-nm diameter and

18

run

parallel

e

200

to

to

one

300

another,

lamellae

are

forming

stacked

at

bundles

throughout

called lamellae.

the

stroma

and

lie

parallel to the corneal surface. Adjacent lamellae lie at angles to one

another, but with signicant interweaving, particularly in the ante-

21,22

rior cornea (Fig. 3.11).

collagen

brils,

running

Each lamellae contains uniformly straight

in

the

same

direction

and

arranged

with

regular spacing because of the surrounding proteoglycans and gly-

cosaminoglycans (Fig. 3.12). Each lamella extends across the entire

cornea, and each bril runs from limbus to limbus. Near the limbus Fig.

3.5

Following

a

paper

cut

to

the

cornea,

uorescein

dye

is

the instilled

and

an

epithelial

defect

is

seen

as

green

collagen

bril

diameter

increases

and

anchoring

uorescence 21

through

a

cobalt

blue

lter.

circumferentially between the sclera and cornea.

lamellae

run

CHAPTER

34

3

Cornea

Fig.

3.6

The

polygonal

Three-dimensional

processes

for

a

these

wing

Golgi

and

ll

surface

(a)

are

stromal

JA,

of

and

a

is

JE.

of

this

time

the

corneal

that

are

involved

basal

for ward

differs

is

from

of

seen

A

at

merge

the

the

random

Human

surface

of

then

of

(e)

the

vesicles

the

as

is

a

most

in

barrier

shows

precorneal

cell

naked

seen

Bowman

Philadelphia:

an

supercial

lm.

A

basal

corneal

layer.

(From

of

of

Hogan

of

ner ve

basement

the

stromal

the

micro-

epithelial

epithelial

arrangement

Saunders;

net

the

bet ween

two

and

passage

corneal

near

into

wing

separating

prevents

cell

time

changes

extensive

tear

cells.

transformed

space

that

ner ve

regular

is

the

sheath

between

supercial

The

in

of

W ing

cells. T urnover

cytoplasm

intercellular

a

layer s

apparent.

gradually

develop

Schwann

layer.

disposition

The

surface

its

passes

Bowman

Eye.

of

cell

 ve

are

basal

transition,

forming

cell

loses

basal

this

cells.

retention

Some

with

apical

During

surface

lymphocyte

(f).

size

Numerous

ner ve

It

relative

columnar

cell.

showing

their

occludens,

in

the

epithelium

and

stroma. The

epithelium.

to

Histology

(c);

layers.

in

zonula

into

layer

cells

the

surface

appears

by

corneal

dome-shaped

prominent.

closed

Bowman

the

surface

the

at

more

membrane

collagen

during

glycogen

lm

the

and

by

thin,

supercial

cur ving

Weddell

and

drawing

basal

formed

into

cells

tear

the

basement

seen

days,

microvilli

(d)

toward

the

becomes

through

membrane

The

7

then

layers,

and

passes

of

spaces

surface

precorneal

cells

is

and

apparatus

plicae

(b)

the

cells

cell

outermost

the

shape

cells.

lamellae

the

MJ,

(g)

corneal

Alvarado

1971 .)

18

e

arrangement

stroma.

In

the

of

anterior

the

lamellae

one-third

varies

of

the

slightly

stroma,

within

the

the

lamellae

wide

and

incidence

1–2.5

of

μm

thick).

cross-linking

e

and

is

anterior

more

cornea

rigid,

has

helping

a

higher

to

main-

24

are

thin

(0.5–30

μm

wide

and

0.2–1.2

μm

thick),

and

18

branch

the

and

inter weave

posterior

more

two-thirds

of

than

the

in

the

stroma,

deeper

the

they

tain

the

corneal

regular,

and

the

lamellae

become

larger

is

arrangement

is

the

reason

23

layers.

In

arrangement

is

that

stromal

causes

swelling

Descemet

15

more

cur vature.

(100–200

μm

cally

as

striae.

is

directed

membrane

to

posteriorly.

fold,

which

can

is

be

swelling

seen

clini-

CHAPTER

Surface

Wing

cells

cells

Bowman

3.10

Light

Light

micrograph

of

corneal

epithelium

showing

micrograph

layer,

and

of

supercial

the

Bowman

3.7

stroma

keratocyte

Fig.

Fig.

layer

layer

Anterior

Stromal

35

Cornea

cells

Basal

Bowman

3

anterior

layer

of

stroma.

lamellae

as

corneal

There

they

is

a

epithelium,

change

cur ve

in

for ward

Bowman

the

to

direction

merge

with

(arrows).

co-

lumnar basal cells, wing cells, and squamous surface cells of the

cornea.

Bowman

layer

and

the

anterior

stroma

are

also

e

evident.

collagen

stroma,

pact

brils

adjacent

with

a

to

of

the

innermost

Descemet

random

layers

membrane,

arrangement

of

the

become

similar

to

what

corneal

ver y

is

com-

found

in

25–27

Bowman

of

layer.

Descemet

injecting

toplasty,

air

e

brils

membrane

into

this

the

area

and

add

corneal

(8–15

interlace

strength

tissue,

μm)

of

with

as

is

attached

to

Keratoc ytes

Descemet

(corneal

to

the

done

posterior

21

stays

the

anterior

cornea.

in

26

When

lamellar

stroma

zone

kera-

separates

and

27

membrane.

broblasts)

are

attened

cells

that

lie

28

between

e

and

cells

occasionally

are

not

within

distributed

the

lamellae

randomly,

their

(see

Fig.

density

is

3.7).

higher

24

in

the

anterior

stroma.

processes

joined

as

the

by

Keratocytes

gap

junctions

have

along

the

29

well

as

anteroposterior

extensive

lateral

branching

extensions,

30

branches.

ese

cells

become

active when there is injur y to the corneal tissue. Other wise, they

maintain

cellular

matrix

in

3.8

In

recurrent

corneal

erosion,

defective

adhesion

number

epithelium

and

basement

membrane

complex

to

stroma

exists.

One

treatment

option

involves

It

create

(From

needle

focal

areas

Krachmer

Mosby;

through

of

JH,

the

scarring

Palay

1995.)

epithelium

that

DA.

help

and

passing

to

Cornea

anterior

cause

Color

a

white

blood

in

pathological

substance lls

collagen

contains

cells

may

cells,

be

found

lymphocytes,

leukocytes,

which

and

between

can

macro-

increase

conditions.

the

areas

proteoglycans,

St

with

one

or

more

ere

Louis:

cornea.

are

tan

Decorin

four

main

sulfate)

is

(molecules

more

proteoglycans,

between

brils,

macromolecules

attached

lamellae,

consisting

glycosaminoglycan

proteoglycans

that

abundant

lumican,

Tear

contain

in

the

normal

in

the

chondroitin

anterior

keratocan,

and

and

of

a

side

human

layer

Stroma

Descemet

and

membrane

endothelium

Anterior segment optical coherence tomography demonstrating the layers of the cornea.

derma-

e

mimican,

film

Bowman

and

stroma.

Epithelium

3.9

extra-

to

welds. ”

three

Fig.

and

glycosaminoglycans

hy-

stroma

“spot

Atlas.

Other

polymorphonuclear

protein

chain. podermic

synthesizing

including

underly-

core ing

slowly

of

cells. the

by

components,

including

and

Ground Fig.

stroma

metalloproteinases.

lamellae,

phages,

the

matrix

other

contain

CHAPTER

36

3

Cornea

A

B

Fig.

3.11

the

Corneal

lamellae

and

the

third

(c)

is

B,

Cross-sectional

in

diameter

round

seen

the

most

mature

Eye.

and

granular

in

stromal

layers.

The

cut

(a)

are

the

ber

longitudinal

(c)

is

from

Saunders;

of

each

of

other

of

the

the

MJ,

showing

obliquely,

lamella

within

Hogan

lamellae

cut

views

tissues

(From

is

This

(b)

obser ved

collagenous

View

(a)

longitudinally.

and

(×104,0 0 0).

Philadelphia:

A,

lamella

separated

mass

of

lamellae.

upper

splits

t wo

by

into

space

lamella

t wo

Alvarado

(b)

in

may

different

is

cut

lamellae

brils

measuring

cut

and

three

next

lamellae. The

a

eye

the

(arrow)

to

cross-section.

JA, Weddell

JE.

a

directions

(×28,0 0 0).

340

50 0

Such

st age

of

cross-section,

measure

20 0

represent

in

in

Histology

to

Å.

40 0

A

masses

are

formation

of

the

Å

large,

of

Human

1971 .)

31

keratan

sulfate

and

are

more

abundant

in

posterior

stroma. that

Decorin

aids

in

interbrillar

spacing

and

adhesion

which

the

stromal

keratocan,

lizes

the

lamellae.

Keratan

regulates

the

diameter

of

the

elasticity

is

decreased

and

that

an

alteration

of

lumican,

stabi-

collagen

32

and

decorin

proteoglycan

levels

results

in

interlamellar

displace-

35–37

ment.

The

process

usually

begins

in

the

central

cornea.

The

stroma

32

brils,

and

lumican,

in

particular,

controls

collagen

bril

diameeventually

33

degenerates

and

thins,

and

the

affected

area

projects

outward

34

ter keeping it within a very limited range.

Proteoglycans have a

signicant role in maintaining corneal tensile strength and glycos-

in

a

cone

shape

because

weakened

area

of

aminoglycans contribute to the relatively high stromal hydration.

downgaze

when

Glycosaminoglycans

as

the

of

the

cornea

force

(Fig.

exerted

3.13A).

by

The

intraocular

cone

shape

is

pressure

most

on

the

evident

in

31

are

hydrophilic,

negatively

charged

carbo-

Munson

sign

the

lower

(Fig.

eyelid

3.13B).

conforms

With

to

the

progression,

38

hydrate

bril.

molecules

ey

attract

located

and

at

bind

specic

with

sites

water,

around

each

maintaining

collagen

the

stroma

and

Descemet

membrane

(Fig.

cone

folds

shape;

occur

this

in

the

is

known

posterior

39

3.13C).

precise Spectacles may be used for a time for correction of refractive error, but with in-

34

hexagonal lattice relationship between individual brils.

creasing irregular astigmatism, rigid gas-permeable contact lenses usually are

40

necessary

CLINICAL

Keratoconus

are

lie

are

is

a

corneal

among

maintained

parallel

rupted.

achieve

correct

vision,

fective

cornea

best

penetrating

corrected

vision.

keratoplasty

may

When

be

contact

performed

lenses

to

no

replace

longer

the

de-

COMMENT: Keratoconus

dystrophy

that

results

in

progressive

stromal

to

by

each

Although

the

possible

the

arrangement

other

the

causes.

and

the

pathology

Normally

and

corneal

is

not

corneal

density

surface.

of

In

completely

the

shape

and

collagen

keratoconus,

understood,

it

strength

brils

this

is

with

a

donor

cornea.

thin-

ning and an outward bulging of the central cornea. Environmental and genetic

factors

to

is

that

dis-

thought

One treatment for progressive keratoconus is corneal collagen cross-linking. In this

procedure the corneal epithelium is removed, and the stroma is saturated with topi-

cal

riboavin

(vitamin

B2).

The

cornea

is

then

exposed

to

ultraviolet

radiation

that

interacts with the riboavin creating chemical bonds between and within the colla-

32 41

gen brils. The corneal collagen stiffens, halting the progression of keratoconus.

CHAPTER

3

37

Cornea

A

B

C

Fig.

Its

3.12

A,

Corneal

collagen,

Collagen

brils

Successive

between

rated

which

the

tive

with

others

cornea.

hazy.

for

distance.

Philadelphia:

ver y

regular

the

an

of

another

equal

in

uid

in

Saunders;

and

parallel

the

one

an

As

gratings.

of

a

way,

orderly

of

ground

MJ,

corneal

result

and

brils.

by

substance

Hogan

of

of

C,

as

well

as

the

restriction

of

in

light

produces

collagen

light

to

stromal

brils

is

(400‒700

less

nm),

transparency.

than

one-half

destructive

distance

If

the

of

the

has

been

specic

ference

reduced

spacing

the

of

rays

components

membrane

separated

are

by

reecting

of

the

wavelength

small

In

brils

from

epithelium,

arranged

such

the

adjacent

irregularly,

the

such

brils

the

cornea

Histology

in

by

form

of

are

opaque

this

disar -

becomes

disturbing

the

a

system

destruc-

an

cornea

of

sepa-

substance

Because

and

a

by

seen

is

inter -

Human

Eye,

the

cornea

and

disrupts

the

collagen

spacing

leading

to

loss

of

destructive

brils, Corneal

scarring

occurs

when

collagen

brils

are

remodeled

with

between

of

occurs,

the

allows

wide,

disordered

which

lowers

bers.

During

visible

and

the

that

stroma,

layer,

wound

healing,

keratocytes

become

active

21

the

refractive

index.

This

may

cause

a

temporary

corneal

haze

light as

that

which

occurs

following

refractive

surgery.

ver y

inter-

Although

and

scattering

light

the

destructive

brils.

B owman

distances

of

brils

light

ground

collagen

cornea.

are

lamellae

through

disturbed.

JE.

the

scattered

interference,

clouding

of

stromal

of

the

broblasts

42

signicantly.

between

of

of

tissue.

lamellae.

stromal

between

distance

interference

24

is

of

many

length

Each

components

JA, Weddell

such

scattering

full

passing

elimination

connective

forms

Three

brils.

Orientation

brils

the

arrangement,

of

interference.

contribute

run

brous

days,

1971 .)

diameter

the

this

rays

100

another.

collagen

destructive

Alvarado

dense,

of

and

one

other

of

brils,

to

resulting

position

eliminated

orderly,

half-life

another

angle

Scattered

glycoproteins,

not

from

to

at

position

of

estimated

orientation

organized

the

is

composed

an

distance.

proper

that

light

(Modied

arrangement

an

is

with

cornea

diffraction

Mucoproteins,

shows

Edematous

brillar

are

across

B, Theoretic

by

scattered

cornea

protein

lamella

maintaining

Diagram

rangement,

a

array

interference.

responsible

e

one

stable

run

lamellae.

three-dimensional

interact

a

within

lamellae

the

from

lamellae. The

is

the

Descemet

particles

scattering

is

are

mini-

Descemet

Descemet

ment

Membrane

membrane

membrane

of

the

(posterior

limiting

endothelium.

It

is

lamina)

is

produced

the

base-

continually

23

mal

in

these

layers.

13

nea

is

Less

than

1%

of

the

light

entering

the

cor-

and

therefore

by

to

age

40

years.

approximately

Descemet COMMENT: Corneal

are

a

number

of

reasons

the

In

15

children,

μm

over

membrane

it

a

is

life,

5

such

μm

that

lifetime

consists

of

thick

it

(Fig.

two

and

has

doubled

will

increase

e

anterior

3.14).

laminae.

Opacity

lamina, There

throughout

17

scattered.

CLINICAL

thickens

43

cornea

can

lose

its

transparency,

approximately

3

μm

thick,

exhibits

a

banded

appear-

become

ance

and

is

a

latticework

of

collagen

brils

secreted

during

opacied, and cause light scatter. Corneal edema changes the refractive index

embr yonic

development.

e

posterior

lamina

is

nonbanded

CHAPTER

38

3

Cornea

A

B

C

Fig.

3.13

etr y,

A,

Forest

cornea

Forest

in

Keratoconus.

Grove,

OR.).

downgaze.

Grove,

OR.).

(Courtesy

B,

Munson

(Courtesy

C,

Patrick

sign;

Edward

Descemet

folds

Caroline,

the

B.

lower

Mallett,

associated

and homogeneous; it is the portion secreted by the endothelium

C.O.T .,

lid

Pacic

conforms

O.D.,

with

Pacic

Universit y

to

the

Universit y,

elastic

rior

in

Family

of

Optom-

keratoconic

Vision

Center,

Descemet

membrane

and

the

endothelium

are

not

the

typical

hemidesmosomes.

no

elastic

such

property.

chamber.

the

46

life.

Although

arranged

of

keratoconus.

44

throughout

College

shape

a

If

bers

way

torn,

Descemet

are

that

the

present,

Descemet

membrane

membrane

is

the

collagen

membrane

will

very

curl

brils

are

exhibits

into

resistant

the

to

an

ante-

trauma,

Endothelium

e

innermost

cent

to

the

layer

anterior

of

the

cornea,

chamber

and

the

is

endothelium,

composed

of

a

lies

adja-

single

layer

13

proteolytic

be

of

regenerated if damaged. A thickened area of collagenous connec-

of

tive tissue can be seen at the termination of Descemet membrane

face,

in

(Fig.

the

limbus;

e

and

enzymes,

this

method

the

and

some

circular

of

pathological

structure

attachment

neighboring

layers

is

is

conditions.

It

can

called Schwalbe line.

between

poorly

Descemet

membrane

understood.

Short

ne

attened

each

cell

from

3.15).

are

rests

which

seven-sided

80%

cells.

It

is

on

normally

Descemet

microvilli

Endothelial

cells

can

hexagonal.

e

μm

thick.

membrane,

extend,

cells

be

5

are

found

the

normal

is

basal

the

apical

anterior

polyhedral:

in

hexagon

lines

and

e

considered

the

sur-

chamber

ve-sided

cornea,

part

but

and

70%

most

to

eca-

47,48

brils

have

extend

been

from

the

identied

posterior

with

electron

stroma

into

microscopy

anterior

that

Descemet

cious

shape

regular

to

provide

arrangement

area

of

coverage

these

cells

is

without

gaps.

described

as

the

e

ver y

endothe-

45

membrane.

nective

seen

in

e

tissue

anchoring

component

Descemet

brils

of

membrane,

the

and

characteristic

of

hemidesmosome

so

the

adhesions

the

are

con-

not

between

lial

mosaic

(Fig.

A lt houg h

ment

3.16).

D es cemet

membrane,

t he

membrane

nature

of

t he

is

c ons ide re d

junc t i ons

a

j oining

b as e -

it

to

CHAPTER

3

39

Cornea

d

e

A

d

e

B

Fig. 3.14

old

Thickness

child.

Light

approximately

a

little

more

JA, Weddell

t he

endot helium

j oin

t he

l atera l

are

wa l ls

the

than

JE.

t he

Descemet

same

the

Histology

cel ls,

of

g ap

the

the

of

Human

B,

Eye

the

Eye.

of

with

(e)

Descemet

50-year -old

Philadelphia:

prov ide

increasing

and

endothelium

i nterd ig it at ions

junc t ions

changes

endothelium

(×500).

thickness

E xtens ive

and

membrane

showing

thickness

double

und ef ine d.

of

of

micrograph

cells

(e)

adult.

migrate

thinning.

and

e

A,

Eye

Descemet

(×800).

Saunders;

age.

membrane

(From

1971:

spread

cell

18-month-

which

membrane

Hogan

p.

of

(d),

MJ,

are

(d)

is

Alvarado

94.)

out

density

to

cover

(cells

per

a

defect,

unit

with

area)

of

resultant

the

cell

endothe-

13

intercel lu l ar

commun i c at i on.

Tig ht

junc t iona l

complexes

lium

decreases

normally

with

aging

because

of

cell

disintegra-

2

j oining

t he

endot heli a l

cel ls

are

lo c ate d

ne ar

t he

cel l

ap ex ;

tion.

Density

ranges

from

3000

to

4000

cells/mm

2

t hes e

are

a

s er ies

49

of

mac u l a

o cclu dens

rat he r

t han

z onu l a

1000

to

2000

cell

density

400

to

necessar y

2

is

bar r ier

slig ht ly

at

age

80

49

children

to

55–57

years.

e

minimum

50

o ccludens.

e

47

cells/mm

in

for med

le aky.

by

L arge

ad hesions

molec ules

b etwe en

can

endot helial

p enetrate

t he

cells

intercel-

500

for

58

adequate

function

is

in

the

range

of

59

cells/mm

Disruptions

to

the

endothelial

mosaic

can

include

endo-

51

lular

spaces.

nutr ients,

ous

be

incomplete

including

humor.

must

is

g lucos e

Excess

moved

out

water

of

t he

bar r ier

and

t hat

al lows

amino

acids,

accompanies

cor ne a

if

t he

prop er

ent rance

f rom

t he

t hes e

of

aque-

nut r ients

hydrat ion

is

to

be

thelial

cell

loss

or

(pleomorphism)

an

or

size

pump

function

ism

morphological

or

increase

can

be

in

the

variability

(polymegathism)

detrimentally

changes,

(Fig.

aected

although

the

of

cell

3.17).

by

e

shape

active

polymegath-

endothelial

barrier

60

maint ained.

ical

in

are

ac tive

continually

infoldings

in

pumps

maint aining

nisms

s ar y

Ionic

for

to

hydrat ion

t hroug hout

move

incre as e

t he

s olute

t he

pres ent

ions

t he

numb er

of

concentration

t he

of

t he

t he

endot helium

stroma.

endot helia l

across

sur face

ionic

in

t he

cel l

are a

by

es e

cells

needed.

t hes e

and

f unc t ion

L ateral

space

Wit h

pumps,

cr it-

me cha-

membranes.

providing

pumps

caus ed

are

neces-

function

is

excessive

allow

loss

excess

pumps

may

t he

concentration

gradient,

t hus

a

uid

movement

across

t he

endot helium.

e

is

r ich

in

cellular

organelles.

Mito chondr ia

can

aqueous

be

to

unable

disrupt

ow

to

moderate

the

into

loss

intercellular

the

stroma.

compensate

for

of

An

junctions

e

this

cells.

and

endothelial

loss

of

barrier

ows

COMMENT: Hassall-Henle

endothelium

can

produce

mounds

of

Bodies

and

basement

Guttata

membrane

material,

endot helial which

cell

cells

a

balance The

of

of

by

changes

water

maint aining

compromised

function.

CLINICAL

down

not

reec t

are

seen

as

periodic

thickenings

in

Descemet

membrane

that

bulge

hig h into the anterior chamber. Those located near the corneal periphery are called

met ab olic

ac tivity

and

are

more

numerous

in

t hes e

cells

t han Hassall-Henle bodies. These bodies are a common nding, and their incidence

in

any

ot her

cells

of

t he

e ye

except

t he

ret inal

photore ceptor increases

with

age.

Such

deposits

of

basement

membrane

in

the

central

cor-

13

cells.

Endothelial

cells

in

the

arrested

be

one

cells

adult

phase

factor

do

not

possess

in

the

that

cell

divide

and

proliferative

cycle.

maintains

this

e

replicate.

capacity

cell-to-cell

layer

in

the

Endothelial

but

are

in

contact

an

may

nonproliferative

e lack

of proliferation may

be

necessar y

for the

maintain

its

barrier

and

pump

functions.

The

endothelium

endothelial

tata

are

in

children,

corneal

visible

as

guttata

covers

may

dark

These

endothelium

3.18).

that

barrier

biomicroscope.

(Fig.

Even

called

layer

52

to

are

the

52–54

state.

nea

is

be

these

are

indicative

mounds

compromised.

areas

may

merely

and

when

be

viewed

interpreted

displaced

is

Both

endothelial

thinned

and

specular

holes

posteriorly

in

from

bodies

reection

the

the

dysfunction.

altered,

Hassall-Henle

with

as

of

and

and

with

endothelium,

plane

of

the

gut-

the

but

reection

40

CHAPTER

3

Cornea

a

b

c

Fig. 3.15

(a),

Three-dimensional drawing of the deep cornea showing the deepest corneal lamellae

Descemet

branches

meridional

that

form

posed

on

the

These

another

from

chamber.

contains

View

with

form

3.5

µm

in

thickness

space

(From

of

in

MJ,

of

one

7

to

the

deeper

this

by

100

sections.

µm

folds

anterior

in

at

chamber

lamellae

has

Å

is

and

JA, Weddell

are

Microvilli

closed

by

nucleus

JE.

and

is

intersecting

intercellular

The

split,

membrane

Endothelial

length.

(e)

mitochondria.

Alvarado

stromal

Descemet

membrane

another

10

marginal

rod-shaped

Hogan

The

membrane.

meridional

and

and

near

lattice

from

pattern

cells,

(c).

Descemet

separated

posterior

exactly

cells

(d)

are

tight

is

Histology

of

superim-

polygonal,

into

project

junctions

round

and

the

in

laments

protrude

junctions

some

seen

the

into

(f). The

attened

Human

Eye.

1971 .)

specular

Patrick

with

linear

abundance

axis.

endothelium

Collagenous

are

a

Intercellular

Saunders;

(Courtesy

and

merge

planes.

the

an

anteroposterior

Fig. 3.16

(b),

to

nodes

to

approximately

Philadelphia:

saic.

tangential

chamber

anterior

the

posteriorly

nodes.

cytoplasm

in

and

one

measuring

anterior

membrane

cur ve

reection

Caroline,

C.O.T .,

through

Pacic

the

biomicroscope

University

College

of

showing

Optometr y,

the

endothelial

Forest

Grove,

mo-

Ore.)

CHAPTER

3

Cornea

A

B

Fig.

3.17

A,

Endothelium

of

healthy

25-year -old

noncontact

lens

wearer.

Endothelial

cell

density

is

2

2000 cells/mm

. B, Endothelium of 40-year -old patient who has worn polymethyl methacr ylate contact

2

lenses

gon

effects

Fig.

for

23

Health

of

3.18

years.

Endothelial

Sciences

hard

and

cell

University,

soft

contact

Endothelium

of

a

density

Portland,

lenses

patient

is

1676

Ore.; B

on

the

with

cells/mm

from

corneal

Fuchs

.

(A

MacRae

courtesy

SM,

endothelium.

endothelial

Scott

Matsuda

Am

J

M,

MacRae,

Shellans

M.D.,

S,

Ore-

etal. The

Ophthalmol.1986;102:50.)

dystrophy.

Numerous

guttata

are

2

evident

M.D.,

as

dark

Oregon

areas.

Health

The

endothelial

Sciences

cell

Universit y,

densit y

Portland,

is

160 0

Ore.)

cells/mm

.

(Courtesy

Scott

MacRae,

41

CHAPTER

42

3

Cornea

wit h CLINICAL

COMMENT: Effects

of

Contact

approximately

7000

no ciceptors

p er

s quare

mi l limeter

Lenses 31

in Clinical

studies

indicate

that

epithelial

thinning,

stromal

thinning,

and

a

number

of

keratocytes

61

of

contact

are

associated

with

long-term

extended

studies

show

that

contact

lens

wear

and

changes

in

the

polymegathism

gas-permeable

or

regularity

have

soft

been

of

the

endothelial

documented

contact

lens

wear,

after

mosaic.

only

although

6

cell

of

either

density

cor ne a

lens

Pleomorphism

years

of

t he

cor ne a,

e ven

just

as

pain

b ecaus e

of

t he

density

of

touch,

no ciceptors.

als o

recognizes

changes

in

temp erature.

C ont ac t

can

63–67

induce

recognized

e Numerous

Stimulation

wear

62

lenses.

cor ne a.

de-

is creased

t he

we ar

over

time

and

aging

caus e

a

de cre as e

in

cor ne al

s ensitivity.

rigid

remained

Unimpaired

sensor y

inner vation

is

necessar y

to

maintain

67

normal.

gery,

Endothelial

or

shape,

age

or

can

stress

lead

to

resulting

from

endothelial

contact

remodeling,

lens

wear,

including

disease,

change

in

sur-

proper

size,

corneal

ner ves

have

a

structure

and

neurotrophic

function.

eect

(i.e.,

e

they

68

with

and

corneal

increased

aid

in

tissue

anesthesia

epithelial

and

a

loss

of

ner ve

adhesion,

impaired

wound

Individuals

mitosis,

73

may

have

decreased

74

healing.

INNERVATION In

cornea

and

corneal

72

endings

reduced

43

cell

CORNEAL

71

maintenance).

permeability,

sensor y

inuence

both.

metabolism

e

corneal

is

densely

inner vated

with

sensor y

bers.

Some

70

addition

receives

some

to

the

rich

sympathetic

sensor y

inner vation,

inner vation

that

may

the

cornea

provide

some

Various

neu-

43

to

80

large

enter

the

ner ves,

branches

peripheral

of

stroma.

the

e

long

and

long

short

and

short

ciliar y

ner ves,

ciliar y

ner ves

regulator y

eect

rotransmitters,

on

chloride

including

(Cl

)

channels.

substance

P

and

acetylcholine,

are

68

are

branches

mic

division

of

of

the

the

Approximately

nasociliar y

trigeminal

1

mm

ner ve,

a

branch

of

the

ophthal-

ner ve.

aer

they

found

in

the

recognition,

pass

into

the

peripheral

cor-

cornea.

ey

cellular

are

believed

proliferation,

stroma,

the

ner ves

lose

their

myelin

sheath,

but

the

cover-

have

a

role

transport,

in

and

pain

wound

healing, as well as cellular signaling that helps to maintain trans-

43

neal

ion

to

parency

and

cellular

75

homeostasis.

68–70

ing

from

occurs,

the

and

distributed

radially

Schwann

three

around

and

give

cell

ner ve

the

rise

remains.

networks

corneal

to

a

Considerable

are

formed.

circumference,

midstromal

plexus

branching

Stroma

enter

and

bundles,

the

a

cornea

subepithe-

When

normal

more

corneal

ner ve

peripheral

central

ner ves

pattern

cornea

are

is

branches

can

take

damaged

regained

are

longer

in

in

the

about

damaged,

and

central

4

cornea,

weeks,

but

reinner vation

result

in

a

less

to

dense

the

when

the

ner ve

71

lial

plexus.

and

gives

e

rise

epithelium

to

and

subepithelial

a

subbasal

Bowman

plexus

plexus

layer

penetrates

that

and

runs

Bowman

between

ultimately

gives

the

o

layer

basal

branches

network

than

epithelial

can

arise

is

found

plexus

from

can

in

the

occur

already

normal

by

two

existing

but

cornea.

Repair

methods:

damaged

new

of

the

ner ve

supercial

sub-

bers

ner ves

71

that

supply

As

the

Schwann

the

corneal

sensor y

cell

epithelium

ner ves

covering

is

pass

lost,

(Fig.

3.19).

through

and

the

or

Bowman

bers

layer,

terminate

the

as

With

endings

surface

position.

ner ve

As

in

the

cell

turnover,

they

reinsert

ending

located

between

pattern

Descemet

tightly

the

ner ve

between

changes

packed

endings

the

new

slightly.

membrane

or

epithelial

the

No

retract

surface

ner ve

have

not

abrasion

of

t he

cor ne a,

and

a

CLINICAL

cells,

the

Corneal

endings

are

with

can

sup er cial

one,

painf ul

e

b ecaus e

density

of

of

t he

s ens or y

density

ner ve

of

t his

endings

s ens or y

in

t he

deeper

a

piece

be

A

COMMENT: Assessing

of

be

assessed

nonavored

measured

small,

can

dental

quantitatively

ne

lament

is

Corneal

clinically

oss.

by

This

using

introduced

a

rigidity

depends

on

the

length

of

approximately

400

times

t hat

of

t he

epider mis

more

exible

the

lament)

that

initiates

t he

skin,

epithelium

Basal

epithelium

Subbasal

nerve

plexus

terminals

Bowman

layer

Subepithelial

plexus

Stromal

nerve

midstromal

from

Stroma

plexus

Fig.

ner ves

that

Sensitivity

touching

initiate

the

a

the

device,

side

to

cornea

blink

an

touch

gently

response.

It

esthesiom-

lament,

the

longer

the

the

cornea.

lament

inner va-

Squamous

Sensory

will

from

epit helium

of

by

measuring

the

cornea.

is

stromal

is

(the

tion.

from

damaged.

sensitivity

Because

quite

sprout

70

shi

endothelium.

e ven

been

might

cells.

eter.

Any

bers

free

13

ner ve

new

3.19

Corneal

innervation.

a

blink,

the

more

sensitive

the

CHAPTER

CLINICAL

COMMENT: Loss

of

Corneal

New

Sensitivity

al

corneal

include

dry

the

nerves

viral

eye

and

disease,

trigeminal

sensory

presentation

diabetes,

endings

can

in

loss

infection,

innervation

nerve

epithelial

resulting

herpetic

to

in

include

permeability,

or

of

corneal

chemical

intracranial

the

cornea.

maintaining

punctate

sensory

burn,

injury

involvement

The

condition

corneal

function

keratopathy,

neovascularization,

innervation.

corneal

that

nally

Causes

(Fig.

surgery,

conrms

the

role

the

thinning,

epithelial

carry

the

of

the

but

vessels

Anti-VEGF

and

from

ulceration

ing

generally

but

membranes,

protect

the

Corneal

or

that

includes

the

to

perforation.

use

of

(joining

Treatment

articial

the

tears,

upper

and

can

be

placement

lower

supply

the

and

to

factor

the

structures

appear

medications

to

monitoring

as

can

form

of

may

new

and

lines

enzymes

vessels

with

the

that

suppress

degrade

migrate,

enter

the

These

will

are

cornea

and

no

(Fig.

VEGF

with

cases

longer

known

biomicroscopy

in

the

and

neovascularization.

vessels

atrophy.

on

cells

neovascularization

extensive

resumes,

white

to

First,

endothelial

prevent

remain

used

the

patients

cornea

will

ne

be

then

as

3.20C).

severe

87

neovascularization.

challeng-

of

eyelids

proliferate

causative

capillaries.

capillary,

43

Cornea

amniotic

together

to

cornea).

surgery

severs

ticularly

important

complications,

can

or

surgeon

starts

lead

tarsorrhaphy

sensitivity

cataract

can

perilimbal

the

Careful

86 73

corneal

of

cells

B).

oxygen

blood,

ghost

increased

defect,

endothelial

3.20A and

When

of

clinical

sprout

membrane

elimination

compromises

because

epithelial

persistent

or

vessels

basement

Neurotrophic keratitis is a degenerative disease caused by the loss of subbas-

3

corneal

to

such

around

be

2

temporarily

laser-assisted

nerves.

aid

as

in

in

after

ocular

keratomileusis

Regeneration

wound

healing,

neurotrophic

weeks

impaired

situ

of

to

and

corneal

prevent

keratitis.

postoperatively

the

In

surgery,

(LASIK),

dry

LASIK,

reaches

nerves

eye,

nerve

the

such

because

and

is

to

as

the

par-

avoid

regeneration

central

cornea

by

68

month

6.

CORNEAL

BLOOD

e

avascular

cornea

is

SUPPLY

and

obtains

its

nourishment

by

diusion A

from

the

aqueous

capillary

sels

is

is

networks

an

angiogenic

by

and

as

located

important

surrounded

76

humor,

factor

well

in

the

in

as

conjunctival

limbus.

corneal

conjunctival

Absence

of

transparency.

capillary

antiangiogenic

and

loops,

factors

a

episcleral

blood

balance

maintains

ves-

Although

its

it

between

avascular

77

state.

e

vessels,

healthy

preventing

cornea.

e

limbus

forms

encroachment

compact

a

of

composition

physical

barrier

conjunctival

of

the

stroma

to

tissue

blood

into

impedes

the

vessel

76–78

growth.

that

and

V ascular endothelial growth factor (VEGF), a protein

stimulates

promotes

the

multiplication

vascular

growth,

is

of

vascular

found

in

the

endothelial

cornea;

cells

however,

VEGF receptor-1, also found in the cornea, binds and diminishes

79

the

ability

of

VEGF

to

induce

vascularization

in

the

cornea.

Corneal avascularity helps to establish “immune privilege” that B 80

gives

some

protection

against

immune

rejection

of

gras.

e

cornea is normally devoid of antigen processing but under certain

conditions, such as inammatory disease, or with mechanical irri-

tation

(such

as

contact

lens

wear),

immunologically

active

mac-

81–83

rophages, Langerhans cells, can migrate from the limbal area.

CLINICAL

In

response

in

an

attempt

blood

oxygen.

thick

lens

It

can

wearers

increases

is

is

edge.

in

oxygen

to

vessels

cularization

a

COMMENT: Corneal

to

deprivation,

supply

termed

usually

be

a

The

sign

indication

of

a

incidence

who

body

oxygen-depleted

neovascularization.

an

compared

those

the

Neovascularization

the

with

wear

that

poorly

of

produce

areas.

In

the

tting

may

a

contact

cornea

or

those

wearing

for

is

poorly

neovascularization

lenses

This

rigid

extended

new

lens

not

of

wearer,

higher

neovas-

contact

in

soft

gas-permeable

periods

vessels

abnormal

receiving

moving

is

blood

growth

or

enough

lens

lenses

lenses

or

contact

with

C

and

low

Fig. oxygen

permeability.

Persistent

corneal

infection

or

inammation,

3.20

A,

Early

neovascularization

from

conjunctival

loops.

B,

suture

Several large vessels have invaded the corneal stroma. C, Corneal knots,

or

wounds

also

may

induce

neovascularization

in

the

body’s

attempt

to

ghost

vessels

remain

after

the

vessels

empty.

(A

Courtesy

increase blood supply. Diseases that stress cells can cause activation of VEGF,

Family 84

promoting

growth

of

new

blood

Vision

Center,

Pacic

University,

85

vessels.

B,

C

Courtesy

Christina

Schnider,

O.D.)

Forest

Grove,

Ore.

CHAPTER

44

3

Cornea

epithelium

CORNEAL

dients.

e

cornea

into

tears

is

mediated

by

ion

ow

and

osmotic

gra-

FUNCTION

has

two

primar y

functions:

to

refract

light

and

to

water

As

ions

are

passage

exchanged

follows,

and

moving

the

concentration

down

its

is

altered,

concentration

gradi-

+

transmit

tion

light.

include:

Factors

(1)

the

that

aect

cur vature

the

of

amount

the

of

anterior

corneal

corneal

refrac-

surface,

ent.

Cl

extrusion

driving

forces

and

for

sodium

water

(Na

)

transport

absorption

across

the

are

the

major

epithelium

and

91

(2)

the

the

change

tear

in

lm),

posterior

refractive

(3)

corneal

corneal

surface,

index

from

thickness,

and

(5)

the

air

(4)

to

cornea

the

change

(actually

cur vature

in

of

refractive

the

index

from cornea to aqueous humor. e total refractive power of the

eye

focused

at

innity

is

between

60

and

65

diopters

(D),

endothelium.

ment

rins,

occurs

However,

through

identied

in

an

additional

water

human

transport

corneal

avenue

of

channels

epithelial

water

called

and

move-

aquapo-

endothelial

cell

membranes.

with

Aquap orins

are

small

integral

membrane

proteins

resid-

88

43

to

48

D

attributable

to

the

cornea.

ing

in

t he

plasma

membrane.

S ome

are

water-s elec t ive

and

92

In

tant

of

the

transmission

that

minimal

incident

light

of

light

scattering

is

through

and

minimized

the

cornea,

distortion

by

the

it

occur.

smooth

is

impor-

Scattering

optical

surface

ot hers

als o

osmotic

brane.

transp or t

water

e

g lycerol.

transp or t

most

e y

channels

constr ic ted

for m

across

p or t ion

t he

of

t he

bidire c tional

plasma

mem-

channel

mig ht

92

formed

by

the

corneal

epithelium

and

its

tear

lm

covering.

e

allow

only

regular arrangement of the surface epithelial cells provides a rel-

a

atively

endot helium,

ties

smooth

between

e

absence

surface,

cells

of

and

the

producing

blood

tear

lm

negligible

vessels

and

the

lls

in

scatter

slight

of

irregulari-

incident

maintenance

of

the

water

sing le

light.

erol

correct

and

s elec tive

and

 le

water

channel

and

p erhaps

and

is

smal l

epit helium;

ow.

found

kerato c ytes;

ot her

conjunc tival

mole c ule

in

Aquap or in-1,

cor ne al

aquap or in-3

s olutes

and

and

is

transp or ts

found

aquap or in-5,

is

epit helium,

a

in

g lyc-

cor ne al

water

s ele c-

92

spatial

arrangement

tering

and

of

distortion

components

as

light

rays

account

pass

for

through

minimal

the

scat-

tissue.

tive

channel,

e

a

signicant

and

te ar

is

found

pat hway

in

cor ne al

for

water

epit helium.

movement

Aquap or in-5

into

t he

is

hyp er tonic

13,43

cornea

scatters

less

than

1%

of

the

visible

incident

light,

lm,

and

water

moves

f rom

t he

st roma

into

t he

aque-

92

the

majority

of

that

scatter,

the

confocal

microscope,

as

determined

occurs

because

by

of

examination

the

with

epithelium

and

ous

t hroug h

channels

aquap or in-1.

but

have

43

amounts

plasm

to

role

in

cel lular

f unc tion

not

pro cess es,

on ly

as

p ar t ic ularly

93

endothelium.

large

s ome

Aquap or ins

Epithelial

of

appear

cells

and

water-soluble

stromal

proteins,

homogeneous

and

keratocytes

which

help

to

enable

diminish

contain

the

in

cyto-

light

scat-

cell

migration.

e

corneal

contribute

to

epithelium,

the

precise

stroma,

control

and

of

endothelium

corneal

each

hydration.

e

42,89

tering.

ese

attributes

of

maintaining

proteins,

the

long

the

called

corneal

recognized

transparency

of

lens

the

cr ystallins,

cr ystallins,

share

many

important

in

lens.

spacing

between

collagen

brils

is

important

in

maintaining

produced

joining

water

Because the stroma makes up 90% of the cornea, the regularity

of

barrier

the

cell.

surface

inux

entering

by

from

the

in

tight

cells

the

cornea

Aquaporins

the

of

tear

from

both

junctions

the

lm.

the

corneal

All

lm

and

occludens)

epithelium

molecules

tear

apical

(zonula

must

basal

(water

pass

prevents

included)

through

membranes

the

provide

+

corneal

transparency.

e

negatively

charged

molecules

located

channels

for

water

passage.

the

anion

Cl

e

cations,

Na

and

potassium

+

around each collagen bril maintain this precise arrangement by

(K

their

branes

bonds

with

water

molecules,

and

corneal

transparency

is

)

and

by

various

,

move

mechanisms,

88

optimal

when

the

stroma

is

75%

to

80%

across

nels,

cotransporters,

and

Na

epithelial

including

+

water.

the

ion

cell

mem-

selective

chan-

+

/K

adenosine

triphosphatase

91

(ATPase)

Corneal

Relative

precise

Hydration

corneal

control

e

deturgescence

of

stromal

(78%

water

extracellular

content)

water

requires

content

and

is

stroma

proteoglycans

a

swelling

dependent upon: (1) the barrier functions of the epithelium and

the

endothelium; (2) the anionic characteristics of molecules within

binding

the stromal matrix that account for the tendency of the stroma to

philic

imbibe

the

thelial

ion

water ;

and

in

(3)

cotransporters,

tinually

by

and

the

entering

the

cell

and

the

junctions

both

water

endothelial

and

transport

energ y-using

cornea

joining

epithelium

ion

membranes

the

and

through

through

(including

ion

pumps).

the

endothelial

endothelium

ion

leaky

cells.

help

the

Fluid

barrier

Ion

epi-

channels,

is

con-

formed

transporters

maintain

the

con-

pumps.

imbibes

within

pressure

that

glycosaminoglycan

properties

of

environment

regular

The

f rom

Dis cont inuit y

b et we en

t he

water

chains

l ayer

molecules,

and

of

fo c a l

ad hesion

of

to

i nto

t ig ht

the

large

matrix

It

is

the

that

thus

anionic

produce

sulfonation

accounts

for

ensuring

responsible

for

the

the

of

water-

hydro-

maintaining

transparency.

a l lows

a que ous

t yp e

in.

that

stroma

contributing

t he

o ccluding

pulls

the

because

extracellular

side

these

in

endot heli a l

s olutes

le a ky,

spacing

water

the

a

slow

t he

le a k

cor ne a

junc t i on

disr upt ions

mole c u les

of

t hat

have

for mi ng

f lui ds

b e c aus e

of

j oi ns

b e en

t hes e

and

t he

t he m .

obs er ve d

t ig ht

junc -

94

centration

from

the

into

the

port

of

gradient

stroma

anterior

change

into

the

chamber

that

tear

can

lm

facilitate

through

through

the

water

the

movement

epithelium

endothelium.

Net

and

trans-

t ions.

t he

The

rate

swel ling

water

exit

of

le a kage

pressure

t hroug h

of

t he

i nto

t he

t he

cor ne a

st roma

end ot helium

and

to

is

d ep end ent

must

be

mai nt ain

up on

b a l anc e d

by

home ost as is

95

solute

into

the

anterior

chamber

exceeds

that

into

the

tears and corneal deturgescence is primarily reliant on endothe-

90

lium

and

minimally

Movement

through

the

of

on

out

endothelium

of

and

ere

brane.

the

into

pre vent

96

epithelium.

water

and

cornea

the

from

aqueous

or

the

stroma

through

the

are

e dema.

aquaporins

throughout

the

endothelial

cell

mem-

97

e

mechanisms

that

transport

ions

across

the

endo-

thelial membrane include ion selective channels, cotransporters,

exchangers,

and

ionic

pumps.

CHAPTER

Hydrogen CLINICAL

COMMENT: Fuchs

dystrophy

(see

Fig.

3.18)

is

(also

a

45

Cornea

by-product

of

glycolysis)

can

also

Dystrophy

build Fuchs

ions

3

a

bilateral,

noninammatory

loss

of

up,

causing

a

decrease

in

intracellular

pH.

Acidication

endo+

can thelial

function.

It

is

inherited

and

progressive

and

may

be

caused

by

prompt

a

change

in

K

channels,

resulting

in

a

rapid

and

mutation +

27

of

the

gene

that

codes

for

collagen

massive

38

VIII.

The

pathological

changes

start

loss

of

intracellular

K

,

which

causes

cell

shrinkage

and

in 104

apoptosis. central

cornea

decreases

and

and

guttata

+

cells

tata

lose

/K

ATPase

in

number,

visible

beaten

form

extend

as

to

the

Descemet

periphery.

membrane

Endothelial

cell

excrescences.

with

metal.

pumps,

some

specular

Stromal

although

will

fuse,

reection,

edema

the

and

is

occurs

barrier

the

described

with

the

function

disruption

Endothelial

as

remains.

of

having

reduction

of

the

the

ion

If acidication involves keratocytes, cellular damage

density

+

increase

mosaic,

of

Na

gradually

As

gut-

can

cause

a

dysfunction

edema

moves

into

the

epithelium,

it

can

cause

a

painful

edema,

and

scarring

and

vascularization

can

follow.

production,

resulting

in

scar

appearance

movement.

microcystic

If

Treatment

COMMENT: Overnight

Corneal

Swelling

epiDuring

thelial

collagen

endothelial

CLINICAL the

in

formation.

sleep,

the

cornea

swells

because

of

the

limited

oxygen

available

to

the

options 105

endothelium. include

hypertonic

ointments

to

decrease

corneal

edema

or

either

The

cornea

is

thickest

upon

awakening

but

returns

to

baseline

penetrating 105

within keratoplasty

or

endothelial

keratoplasty

to

replace

the

dysfunctional

a lial

the

rst

2

hours

of

waking.

With

stromal

hydration

increase,

there

is

endothedecrease

in

swelling

pressure,

and

for

a

short

time,

the

endothelial

pumps

cells. exceed

the

water

leak,

resulting

in

decreased

edema

and

reattainment

of

nor-

106

mal

Corneal

hydration.

Metabolism

e metabolically active cornea depends on a stable supply of oxyCLINICAL

gen

and

glucose.

Oxygen

is

derived

primarily

from

Corneal

oxygen

dissolved

in

the

tear

lm,

with

small

amounts

the

aqueous

humor

and

limbal

capillaries.

In

closed

is

approximately

two-thirds

of

the

oxygen

is

manif es t e d

by

a

Edema

c ha ng e

is

direc ted

poster ior ly

an d

th e

in

a n t e ri o r

c o rn e a l

s u rf a c e

t h i c kn e s s .

curvature

eye

The

swell-

remains

the

107

same

conditions,

edema

obtained ing

from

COMMENT: Corneal

atmospheric

(because

of

the

f ix ed

n at ur e

of

Bo w m a n

layer).

The

more

closely

supplied packed

lamellae

in

the

ant er io r

c o r n ea

ma y

m a ke

the

a n te r i o r

stroma

mo re

98

by

capillaries

including

cornea

with

the

glucose,

from

the

rest

amino

aqueous

from

acids,

the

aqueous.

and

humor

Most

vitamins,

through

the

readily

leaky

lesser

amount

Glucose

is

is

obtained

from

metabolized

by

limbal

aerobic

enter

the

endothelium;

99

a

nutrients,

acid

c ycle

(TCA

or

Krebs

c ycle),

lam ellae

The

reduction

ling

of

The

corneal

and

the

via

the

tricar-

anaerobic

hexose

used

B ecause

stant

gen,

the

state

and

by

monophosphate

the

basal

of

cornea

cells

of

replication,

35%

of

the

is

shunt.

the

metabolized

corneal

they

glucose

have

via

the

hexose

About

epithelium

signicant

processed

monophosphate

85%

are

in

stores

within

cellular

provides

components

epithelial

e

shunt

nucleotides

e

necessar y

for

for

the

of

102

its

requires

metabolic

the

the

a

of

con-

glyco-

epithelium

hexose

Each

A

minor

cludens

edema

of

of

mitochondria,

6

1.5

×

there

the

10

is

+

Na

an

body

replacement

of

stores

cell

of

energ y

contains

to

a

large

each

/K

can

cell

is

estimated

to

have

ATPase

in

increase

pump

pumps.

the

In

certain

permeability

the

function

number

and

of

of

diseases,

the

in

larger

sp a ce s

c ur v at ur e

s t r o ma

of

t he

a l l o wi n g

po s t er i o r

more

fluid

b e-

surface

can

collection.

an d

r em ains

linear ly

t he

t he

a pp ear a nc e

sa me .

c or re la te d

An

wit h

of

vertical

c a u se

in c r e a s e

co r n e a l

in

folds

b u ck-

c o rn e a l

t h i ck n e s s .

(striae).

hydration

N o r ma l l y

1%

of

inc ide nt

li gh t ,

bu t

w it h

fluid

r e t e n ti o n

light

the

s ca t t e r

can

pumps

compensating

per

for

the

of

the

results

decrease

It

is

in

corneal

a

epithelium

localized

visual

acuity

uncomfortable

area

when

and

it

can

causing

of

edema

separates

be

painful.

loss

and

of

cells

More

the

zonular

haziness.

causing

oc-

Epithelial

surface

extensive

ir-

epithelial

also

allow

uid

entrance

into

the

stroma.

edema

causes

the

to

collagen

moderate

hypertonic

by

than

generalized

around

a

caused

greater

the

that

stromal

brils.

corneal

loss

of

caused

edema.

the

Fluid

Moderate

edema

endothelial

by

loss

function

the

edema

temporarily

be

is

is

generally

epithelial

accumulates

stromal

can

of

in

the

stromal

usually

cleared

barrier

of

a

and

matrix

symptom-free.

with

instillation

solution.

which

endothelial

layer,

cell,

thus

increased

103

membrane

pos t er io r

mem br ane

abrasion

barrier

Corneal

of

43

increase

expanding

and

+

the

the

Mild

number

with

mono-

synthesis

constant

signicant

function.

s t r o ma,

increases.

magnitude

endothelium

p o s t er io r

the

cells.

maintain

the

and

scatters

abrasions

phosphate

in

the

diameter

positively

regularities.

shunt.

t he

anaerobically.

90

is

than

glycoly-

101

glucose

in

Descemet

cornea

sis,

edema

15

tween

is

boxylic

to

100

capillaries.

glycolysis

resistant

Age,

thelial

lular

permeability.

disease,

number,

surgery,

causing

cell

thinning.

function

or

cells

can

to

As

be

injury

can

spread

the

cell

reduced

result

out

to

in

architecture

and

a

cover

reduction

the

loss

changes

endothelial

cell

to

of

endothelial

with

resultant

cover

function

more

can

be

cell

endo-

area,

cel-

adversely

affected by either a change in the size or the shape of the cell. The loss of cells

When

the

oxygen

supply

is

reduced

in

the

hypoxic

cornea,

can

the

rate

of

anaerobic

glycolysis

increases

causing

an

increase

result

level

the

concentration

amount

the

can

stroma

chamber.

the

and

is

osmotic

of

move

lactate.

into

then

is

a

the

through

slow

balance,

As

lactate

tears.

the

process

pulling

accumulates,

e

rest

must

endothelium

and

water

lactate

into

the

only

move

into

builds

corneal

the

up,

a

can

edema.

tear

A

poorly

exchange

t

and

contact

lens

diminishes

that

the

does

present

at

the

tear/cornea

interface

can

produce

shiing

not

a

and

CLINICAL

Very

high

of

loss

of

of

pump

the

layer,

and

damage

at

the

cellular

function.

COMMENT: High

intraocular

water

pressure

into

the

on

Intraocular

the

corneal

order

stroma

of

Pressure

50

from

mm

Hg

the

anterior

or

higher

can

move

chamber

and

allow

the

endothelial

transport

system.

This

is

an

ocular

emergency

oxymust

hypoxic damage.

condition.

permeability

a

anterior

and

gen

in

small

stroma,

amount

result

through

overwhelm

adequate

increased

also

excessive

inducing

in

in

be

treated

quickly

to

prevent

permanent

corneal

and

optic

nerve

CHAPTER

46

Epithelial

Cell

3

Cornea

Replacement

Epithelium

Maintenance of the smooth corneal surface depends on replace-

Because

ment

occurring

tosis

the

of

the

surface

cells

(programmed

tear

lm.

cell

Turnover

approximately

7

to

10

that

are

death)

time

and

for

days,

constantly

continually

the

which

undergoing

entire

is

being

corneal

more

rapid

apop-

shed

into

epithelium

than

for

is

other

neal

of

the

in

injur y,

released

ecules

high

the

mitosis

from

play

rate

basal

stops,

damaged

key

of

roles

cell

layer

in

and

corneal

growth

mitosis

is

constantly

epithelium.

factors

and

epithelial

and

stromal

initiating

and

continuing

108,109

epithelial

turnover,

of

With

cor-

cytokines

cells.

ese

the

are

mol-

processes

114,118

tissues.

necessar y for corneal repair.

Hemidesmosomes in the basal

119

is

sion,

and

to

renewal

of

migration,

proliferation

become

the

stratied

epithelium

dierentiation,

wing

occur

cells,

in

the

and

and

basal

wing

involves

senescence.

layer.

cells

Basal

move

up

cell

Cell

cells

to

divi-

division

move

become

up

sur-

layer

are

dissembled

Changes

in

cell

in

the

shape

brane

along

the

cytoskeleton

as

those

extensions

cells

leading

occur

at

(lopodia)

the

edge

allowing

wound

enabling

of

for

edges

the

cell

the

a

wound.

rapid

change

develop

to

mem-

migrate

and

114,120,121

face

cells.

brane

Only

have

the

the

cells

ability

to

in

contact

divide;

the

with

cells

the

that

basement

are

mem-

displaced

into

cover

of

the

the

wound.

Cell

hemidesmosomes,

migration

the

requires

cytoskeleton

precise

structure,

control

and

cell-

110

the

wing

cell

layers

lose

this

ability.

As

the

supercial

squa-

to-matrix

adhesion,

which

preser ves

the

structural

integrity

of

118

mous

cells

and

the

and

are

below.

age,

they

cytoplasm

sloughed

Limbal

around

the

corneal

condenses.

o,

stem

corneal

basal

degenerate,

cell

being

cells

e

located

A

cytoskeleton

cells

constantly

peripher y

layer.

the

are

slow

in

their

replaced

a

the

lose

0.5

to

source

migration

disassembles,

1

attachments

from

mm

for

of

the

the

wide

renewal

basal

cells

layers

band

of

the

occurs

epithelial

Adhesion

sheet

to

sheet.

molecules

adhere

to

hemidesmosomes

cover

the

injur y.

allow

the

the

leading

basement

and

also

Growth

to

edge

membrane

pull

factors

cells

as

of

in

the

stimulate

the

the

epithelial

absence

sheet

the

of

moves

to

production

of

matrix components that enhance this cell-to-substrate adhesion.

111,112

from

the

peripher y

than

moving

toward

the

center

of

the

cornea.

Rather

Fibronectin

is

likely

a

key

factor

in

the

substrate

that

establishes

122

central

radially,

the

cells

move

centripetally

toward

the

cornea.

adhesion

during

cell

migration.

Proliferation

is

suppressed

until migration occurs, but then proliferation is enhanced in the

118

Despite

cells

constantly

being

sloughed,

the

barrier

function

region

is maintained as the cell below moves into position to replace the

one

that

has

been

shed.

Tight

junctions

are

present

exclusively

behind

Once

to-cell

the

the

defect

junctions

between the squamous cells that occupy the supercial position.

Mitosis

e

are

thesis

the

cell

advancing

is

are

resumes

front.

covered

by

a

constructed

and

glycogen

single

layer

between

of

cells,

neighboring

utilization

and

cell-

cells.

protein

syn-

93

not

protein

present

components

in

the

basal

necessar y

cells

but

to

are

form

these

increasingly

junctions

present

as

increases.

density

is

Cell

proliferation

reached

and

the

continues

stratied

until

nature

of

normal

the

tissue

123

cells

move

up

to

the

surface

where

the

zonula

occludens

junc-

is

reestablished;

apoptosis

prevents

epithelial

hyperplasia.

108

tions

become

complete.

Biochemical

bonds

hold

the

basal

cell

to

its

substrate

before

113,124

e

ing

up

basal

the

cell

layer

is

continually

hemidesmosome

into

the

anchoring

wing

cell

brils

junctions

layers.

connect

e

remain

losing

as

cells

plaque

present

and

reestablish-

divide

sites

in

to

the

and

move

which

the

stroma

for

hemidesmosomes

by

proliferation

scar

are

in

formed.

the

Basal

limbus.

cells

Epithelial

are

replenished

healing

generally

is

free.

Repair

to

corneal

epithelial

tissue

proceeds

quickly.

Minor

113

reattachment.

epithelial

abrasions

heal

in

24

to

48

hours

with

hemidesmo-

119,125

somes

Corneal

Wound

Repair

reformed.

however,

If

complete

the

healing

basement

with

membrane

replacement

of

is

damaged,

the

basement

113,124

C or ne a l

to

injur y

rep air

var ious

init i ates

d amage d

t issue.

biomole c u les ,

integ r ins,

c ytok ines ,

loproteinas es

remo deling

are

t he

a

c as c ad e

T hes e

such

and

as

of

pro c ess es

mat r ix

g rowt h

prote olyt ic

ext racel lu l ar

me chan isms

are

mat r i x,

di re c te d

Mat r ix

t hat

are

me t a l-

i nvolve d

re cr uit ment

of

in

cel ls,

integ ra l

and

c y tok i ne

membrane

maint aining

b et we en

g lycoproteins

cor ne a l

cel ls

and

ac t ivat i on.

f unc t i on .

t hat

S ome

e xt racel lu l ar

C or ne a l

have

integ r ins

mu lt iple

f aci lit ate

mat r ix;

s ome

are

role s

in

i nterac t ions

have

and

hemidesmosomes

can

take

months.

Bowman

Layer

Bowman

replaced

layer

will

either

by

not

regenerate

stroma-like

if

brous

damaged

tissue

or

by

but

will

be

epithelium.

in f l am-

15

mator y

membrane

by

met a l loprote inas es ,

fac tors.

en zy mes

de si g ne d

a

role

in

Stroma

When

corneal

increase

in

injur y

number,

broblasts.

ese

extends

and

cells

some

cause

into

are

the

the

stroma,

stimulated

wound

bed

to

to

keratoc ytes

become

contract,

myo-

allow-

114

mat r ix

t ion

t he

ass embly ;

of

s ome

intercel lu l ar

ext racel lu l ar

i mp ac t

cel l

junc t ions;

env i ron ment

ad hesion

and

and

ot he rs

and

s ens e

com mun i c ate

t he

for ma-

change

to

t he

in

c el l

ing

for

more

rapid

characteristics

nents

of

the

of

wound

the

stroma

coverage

newly

dier

formed

slightly

by

the

epithelium.

connective

from

those

tissue

of

the

e

compo-

original

114

nucleus

are

by

an

sig na ling

t ion

b et we en

proliferat ion

a lterat i on

mole c u les

cel ls

and

and

in

t hat

w it h

t he

c yto skeleton .

faci lit ate

cel lu l ar

su r round i ng

d i f ferent i at ion

are

Cytok ines

com mun i c a -

t issues .

me di ate d

by

C el lu l ar

g rowt h

tissue.

larger

the

e

than

sclera,

ment

diameter

the

and

brils

regenerated

original

the

are

of

not

alignment

as

precise.

115–117

fac tors.

brils,

corneal

comparable

and

stromal

to

those

organization

ese

factors

collagen

of

found

the

increase

is

in

replace-

the

prob-

126

ability

that

a

scar

will

result.

e

tensile

strength

of

the

CHAPTER

collagen

brils

in

repaired

cornea

is

diminished

and

may

3

47

Cornea

take Anterior

lamellar

keratoplasty

can

be

performed

to

replace

the

anterior

layers

127

months

to

approach

the

typical

strength.

Once

healing

is of

complete,

the

myobroblasts

undergo

apoptosis

or

revert

the

cornea

with

donor

tissue.

This

allows

the

patient

to

retain

their

own

back endothelium.

The

risk

full

incision

of

vision

threatening

complications

is

reduced

when

a

114

to

keratoc ytes.

Descemet

Descemet

aged,

and

it

the

thickness

is

not

necessary.

Membrane

membrane

can

be

is

a

secreted

strong,

and

resistant

reformed

membrane.

by

stromal

If

dam-

keratocytes

endothelium.

Absorption

e

cornea

of

Ultraviolet

transmits

light

Radiation

with

wavelengths

between

310

and

43,129

2500

Endothelium

Ver y

little

nm.

Wavelengths

epithelium

mitosis

occurs

in

the

endothelium.

With

cell

loss,

the

those

and

B owman

between

300

to

below

layer

320

300

and

nm

nm

do

are

are

not

absorbed

penetrate

absorbed

by

by

the

deeper ;

the

corneal

130,131

neighboring

of

loss,

cells

cells

and

a

remodel

generally

decrease

into

the

in

enlarge

and

endothelial

hexagonal

atten

cell

shape,

to

cover

density

and

the

area

results.

e

pump

and

barrier

stroma.

e

wavelengths

of

structures

(the

to

from

ability

of

the

ultraviolet

lens

and

cornea

radiation

retina),

to

is

but

absorb

the

protective

the

cornea

is

shorter

to

deeper

vulnerable

130

functions

are

reestablished.

of

ion

pumps

in

to

compensate

an

for

In

certain

endothelial

the

loss

of

cell

conditions,

can

pumps

increase

that

occur

the

number

dramatically

when

cells

are

damage

induces

ese

this

oxidative

free

constant

stress

radicals

are

by

exposure.

generating

highly

Ultraviolet

reactive

reactive

radiation

oxygen

because

of

an

species.

unpaired

103

lost.

Normally

However,

corneal

recent

stripping

shows

endothelium

evidence

that

does

associated

central

not

replicate

with

endothelial

aer

central

cells

birth.

Descemet

are

electron

and

thelium

has

ultraviolet

capable

of

trations

section

of

can

shown

to

dant

can

damage

some

radiation

of

cellular

protection

structures.

against

absorption.

ascorbate

(vitamin

Its

C)

the

cells

and

e

corneal

damage

have

epi-

caused

high

glutathione.

by

concen-

Ascorbate

59

repopulating.

Descemet

Aer

surgical

membrane,

the

removal

of

endothelial

a

4-mm

cells

were

128

repopulate,

and

corneal

edema

cleared

within

1

to

6

months.

absorb

that

ultraviolet

can

reduce

radiation

free

and

radicals

is

also

and

a

cellular

neutralize

antioxi-

their

activ-

130

ity.

Glutathione

is

both

a

reducing

agent

and

a

free

radical

132

Endothelial

cell

recover y

is

more

likely

if

the

diameter

of

the

scavenger.

Cr ystallins,

present

in

the

cellular

c ytoplasm,

also

89,132

membrane

removed

is

small,

as

there

is

less

surface

area

for

absorb

ultraviolet

radiation

and

are

free

radical

scavengers.

128

the

endothelial

the

diseased

cells

to

Descemet

cover.

It

is

membrane

theorized

halts

the

that

removal

inhibition

of

of

endo-

e

or

epithelial

reverse

cell

also

has

ultraviolet

a

cellular

radiation

repair

damage

system

to

to

minimize

deoxyribonucleic

132

thelial

cell

replicate.

proliferation

Alternatively,

and

healthy

removal

of

endothelial

the

cells

dysfunctional

can

then

cells

may

acid.

59

provide

space

whether

the

migration

thelial

for

the

healthy

repopulation

or

proliferation

of

cells

to

replicate.

endothelial

from

the

cells

It

is

occurs

remaining

uncertain

because

peripheral

of

endo-

CLINICAL

Because

violet

cells.

can

result

snow.

COMMENT: Keratoplasty

epithelium

radiation

sunlamps,

CLINICAL

COMMENT: Photokeratitis

the

in

a

painf ul

tanning

Cellular

and

B ow m a n

absor banc e,

la y e r

a

are

the

o ve r e x po s u re

phot o k e r a t it is.

be ds ,

defens e

acute

w elde r ’s

T hi s

a rc ,

m ec ha n is ms

or

are

can

the

p r i ma r y

to

occur

highly

o v e rc o me

sites

ultraviolet

w it h

ultra-

exposure

r e f le ct i v e

c a u s in g

for

r a d i a ti o n

rays

to

from

disruption

of

+

In

conditions

that

cause

cornea

thinning

and

perforation

is

a

possibility,

when

the

epithelial

tight

ju nc t ions ,

ind u ci ng

e d em a .

H y p e r a c ti v a ti o n

of

the

K

+

central

corneal

scarring

(perhaps

from

injury

or

infection)

causes

loss

of

vi-

channels

in

cell

membr anes

r e su lt s

in

a

m as s ive

l o ss

of

i n t r a ce l l u l a r

K ,

104

sual

acuity,

cornea

can

or

when

be

the

replaced

endothelium

by

a

donor

is

compromised

cornea.

The

and

cornea

function

is

is

normally

lost,

the

devoid

of

which

in

caus es

cell

keratopathies

shr ink age

affec t ing

a nd

t he

a po pt o s is.

ep it he lium

C hronic

an d

a n t e r io r

exposure

st r o ma

or

can

r es ult

can

ca u se

133

antigen

graft

processing

rejection

is

because

usually

of

quite

the

absence

of

blood

vessels

and

so

the

rate

of

endothelial

pleomorp his m .

low.

Full thickness penetrating keratoplasty has been the traditional method for replac-

ing

diseased

and

compromised

corneas.

However,

this

procedure

has

signicant CLINICAL

COMMENT: Corneal

Reshaping

complications, such as irregular cornea and irregular astigmatism (sutures run the Surgical entire

circumference

of

the

corneal

donor

button

and

are

often

left

in

place

procedures

that

remove

a

portion

of

the

corneal

stroma

and

thus

for change corneal curvature are performed to reduce refractive error. The amount

years), infection, wound rupture, and occasionally graft rejection or failure. of

New

surgical

have

replaced

corneal

some

that

procedures

recovery

keratoplasty.

replaced

with

and

a

donor

is

only

caused

by

the

diseased

membrane

the

In

and

endothelium

the

cornea

patients

may

compared

endothelium.

of

dysfunction,

sutures

outcome

and/or

and

for

portion

procedures.

endothelial

need

predictable

membrane

the

keratoplasty

eliminate

more

Descemet

a

replace

penetrating

decompensation

keratoplasty

visual

methods

are

endothelial

allow

with

where

a

faster

penetrating

removed

and

stroma

desired.

usually

to

In

by

be

removed

photorefractive

mechanical

is

determined

keratoplasty

means.

Then

by

the

(PRK),

Bowman

the

target

refractive

epithelium

layer

and

the

is

correction

removed

anterior

rst,

stroma

are

ablated by a laser. Bowman layer does not regenerate, and the basement mem-

brane of the epithelium must be laid down on the remaining stromal surface. In

LASIK,

folded

the

a

ap

back,

edges

of

is

made

and

the

consisting

stroma

ap

is

seal

of

removed

as

the

epithelium

by

a

laser.

epithelium

and

Bowman

The

ap

heals.

In

is

both

layer.

laid

back

This

ap

down,

procedures,

is

and

anterior

CHAPTER

48

stroma

is

removed.

Some

3

Cornea

endothelial

cell

loss

is

reported

but

has

not

been

CLINICAL

COMMENT: Clinical

Aging

Changes

in

the

Cornea

134–138

found

to

effects

be

clinically

resulting

signicant.

from

loss

of

Speculation

Bowman

layer

with

continues

PRK,

about

although

long-term

none

has

yet

Aging

produces

tal

vision.

to

changes

Iron

in

corneal

deposits

in

the

appearance,

corneal

but

most

epithelial

are

cell

not

detrimen-

cytoplasm,

more

152

been

may

determined.

be

one

of

The

the

role

of

Bowman

considerations

layer

when

in

ultraviolet

deciding

radiation

between

PRK

and

absorption

LASIK.

concentrated

in

Hudson-Stähli

Degeneration The

reduction

of

corneal

thickness

may

have

other

clinical

effects,

that

removal

of

anterior

stroma

eliminates

an

area

having

basal

cells,

line,

often

evident

of

Bowman

produce

layer

at

the

a

horizontal

level

produces

of

the

the

pigmented

lower

limbal

line,

eyelid

girdle

of

the

margin.

Vogt.

This

consideryellowish

ing

the

white

opacity

is

located

at

the

3

and

9

o’clock

positions,

inter-

signicant palpebrally.

A

clear

interval

separating

the

opacity

from

the

limbus

may

or

24

rigidity

and

stability.

Studies

have

shown

a

correlation

between

corneal may

thickness

and

the

measurement

of

intraocular

139

thickness

of

the

as

and

the

increased

any

incidence

risk

implications

141

of

stromal

important

refractive

of

for

the

pressure

glaucoma

The

intraocular

risk,

in

between

seen.

corneal

140

glaucoma.

inaccurate

and

be

clinician

pressure

patients

must

be

readings,

who

have

had

aware

as

well

removal

Corneal

white

ring

arcus

is

deposit

is

the

most

located

separated

common

within

from

the

the

corneal

aging

peripheral

limbus

by

a

change.

stroma

zone

of

is

clear

An

annular

evident

cornea.

(Fig.

The

yellow-

3.21).

This

deposits

are

142

tissue.

in

of

not

Pachymetry

diagnosis

of

(measurement

glaucoma,

of

especially

corneal

in

those

thickness)

who

have

is

had

surgery.

cholesterol

40

AGING

CHANGES

IN

cholesterol

esters

and

can

result

from

age

or

elevated

blood

cholesterol levels. With time the arcus can extend anteriorly to Bowman layer.

There

PHYSIOLOGICAL

and

is

no

years,

clinical

signicance

hyperlipidemia

should

in

be

elderly

persons,

but

in

those

under

age

suspected.

THE REFERENCES

CORNEA

1.

Alterations

to

cellular

integrins

in

the

corneal

epithelium

War wick

7th

occur

with

age

and

result

in

a

reduction

in

the

adhesion

necessar y

causes

a

for

breakdown

intercellular

in

the

junction

barrier

construction.

function

of

the

ed.

Eyeball.

Eugene

Philadelphia:

Wol ’s

Saunders;

Anatomy

of

the

Eye

and

Orbit.

1976:30–180.

mol2.

ecules

R.

can

is

corneal

epi-

Augusteyn

biometr y.

3.

Jonas

JB,

RC,

Exp

Nankivil

Eye

Res.

D,

Mohamed

A,

etal.

Human

ocular

2012;102:70–75.

Ohno-Matsui

K,

Holbach

L,

etal.

Association

between

143

thelium.

with

Although

age,

Bowman

total

layer

corneal

thins

thickness

with

age,

remains

with

a

loss

of

the

same

axial

length

thickness

Arch

Clin

8

of

about

density

32%

can

from

age

adversely

20

to

aect

80

years.

wound

Decreased

healing

and

keratocyte

collagen

4.

Van

5.

Badmus

produces

spaces

that

can

disrupt

transparency

Buskirk

opacities.

resulting

Descemet

in

membrane

Hassall-Henle

bodies,

increases

located

in

in

membrane.

include

a

Aging

decrease

in

changes

cell

in

the

density,

globe

diameters.

Graefe’s

2017;255:237–242.

anatomy

AI,

vertical

of

the

limbus.

Adegbehingbe

Eye.

B O,

1989;3:101.

etal.

of

cur vature

ratio

and

refractive

Axial

status

in

length/

an

population.

Niger

J

Clin

Pract.

adult

2017;20:1328–1334.

thickMartola

EL,

Baun

JL.

A

clinical

study

on

central

and

peripheral

peripheral

corneal

thickness.

Arch

Ophthalmol.

1968;79:28.

endothe7.

lium

e

Ajaiyeoba

radius

corneal

Descemet

EM.

SA,

Nigerian

6.

ness,

Ophthalmol.

and

and

55,143

create

Exp

horizontal

bril

corneal

degradation

and

polymegathism,

Feizi

S,

Jafarinasab

MR,

Karimian

F ,

etal.

Central

and

periph-

and eral

corneal

thickness

measurement

in

normal

and

keratoconic

55–57,144

pleomorphism.

ere

is

no

eyes

evident

change

in

the

wavelengths

transmitted

using

three

corneal

pachymeters.

J

Ophthalmic

Vis

Res.

2014;9:296–304.

145

by the aging cornea.

rule

to

e anterior cornea shis from with-the-

against-the-rule

astigmatism

with

age;

however,

the

8.

146–148

terior

cornea

remains

relatively

decrease

in

corneal

sensitivity

corresponds

to

a

loss

of

López

de

J,

Karanis

Bowman’s

la

Vis

Sci.

Fuente

Evaluation

of

total

in

the

density

Fagerholm

in

the

P ,

etal.

human

Age-related

cornea

in

vivo.

Invest

2013;54:6143–6149.

C,

Sánchez-Cano

corneal

thickness

A,

Segura

and

F ,

corneal

etal.

layers

with

although some studies have shown no spectral-domain

dierence

G,

layer

cor-

149–151

neal ner ves with age;

of

Ophthalmol

stable.

9.

A

Germundsson

thinning

pos-

of

subbasal

ner ve

plexus

ber

optical

coherence

tomography.

J

Refract

Surg.

number 2016;32:27–32.

55

with

age. 10.

Schmoll

T,

Unterhuber

measurements

Optometry

11.

Gutho

inner

Vis

RF ,

vision

of

Sci.

Kolbitsch

the

layer,

C,

etal.

Precise

epithelium,

and

thickness

tear

lm.

2012;89:E795–E802.

Zhivov

of

A,

Bowman’s

A,

Stachs

O.

cornea—a

In

vivo

major

confocal

review.

Clin

microscopy,

Exp

an

Ophthalmol.

2009;37:100–117.

12.

Crewe

in

JM,

Armitage

organ-cultured

WJ.

human

Integrity

corneas.

of

epithelium

Invest

and

Ophthalmol

endothelium

Vis

Sci.

2001;42:1757–1761.

13.

Hogan

JA,

MJ,

Saunders;

14.

Torricelli

lial

Alvarado

Weddell

Fig.

3.21

The

white

limbal

band

of

corneal

arcus.

JA.

e

cornea.

Histolog y

of

the

In:

Hogan

Human

MJ,

Eye.

Alvarado

Philadelphia:

1971:55–111.

basement

DelMonte

J

eds.

AAM,

Ophthalmol

15.

JE,

Cataract

Singh

V ,

membrane:

Vis

DW ,

Sci.

structure,

MR,

etal.

function,

e

and

corneal

disease.

epithe-

Invest

2013;54:6390–6400.

Kim

Refract

Santhiago

T.

Surg.

Anatomy

and

physiolog y

2011;37:588–598.

of

the

cornea.

CHAPTER

16.

Sakimoto

T,

Sawa

degradation

17.

Alvarado

J,

basement

and

Komai

gen

Murphy

Vis

C,

Sci.

Ushiki

brils

Sci.

19.

Y ,

Metalloproteinases

membrane

Ophthalmol

18.

M.

processing.

in

T.

the

Cornea.

Juster

of

the

R.

in

corneal

Age-related

human

39.

diseases:

2012;31(1):S50–S56.

corneal

changes

in

40.

the

epithelium.

41.

three-dimensional

human

cornea

and

organization

sclera.

Invest

of

Ophthalmol

Wilson

SE,

or

Hong

Vis

42.

Pekel

and

G,

JW .

Bowman’s

dispensable

Y ağc

anterior

to

layer

corneal

structure

function?

A

and

43.

function:

hypothesis.

Cornea.

Meek

KM,

Retin

22.

Eye

Acer

sclera

S,

in

etal.

Comparison

emmetropic

and

of

corneal

myopic

eyes.

44.

layers

Winkler

brate

M,

corneal

23.

Goldman

tions

J,

LJ,

anterior

Br

25.

J

Sci.

Vis

Pels

ned:

a

Faraj

novel

structure

and

transparency.

45.

Prog

ST,

the

etal.

A

comparative

evolution

of

a

study

refractive

of

Lombardo

G,

Dohlman

in

lens.

46.

Invest

croscopy

Clin

27.

Exp

accounts

C,

etal.

swollen

Structural

human

47.

altera-

corneas.

Said

GF .

for

specic

maintenance

architecture

of

corneal

of

48.

the

DG,

of

Human

layer

M,

Ophthalmol.

the

Serrao

(Dua’s

S,

endothelial

Schlötzer-Schrehardt

Poole

CA,

corneal

layer).

anatomy

rede-

49.

in

the

etal.

Two-photon

keratoplasty

gras.

optical

Graefe’s

mi-

50.

Müller

LJ,

Pels

organization

Sci.

30.

U,

Bachmann

BO,

corneal

Tourtas

stroma.

T,

etal.

31.

quiet

Ehlers

the

32.

Ma

MC,

NH,

living

Clover

cornea

N,

Eye.

J,

vol.10.

Y ,

KM,

stroma.

34.

GF .

GM.

using

Novel

corneal

Keratoc yte

vital

dyes.

51.

Cell

aspects

keratocytes.

of

the

Invest

S c ott

e

Elsevier ;

Wei

52.

Sci.

ultrastructural

Ophthalmol

53.

Eye

Hai g h

ke r at i n

c or ne a l

P ,

Assoc.

cornea.

MJ.

Keratocytes:

no

54.

more

In:

Fischbarg

J,

ed.

e

Biolog y

55.

Biomechanics

association

and

with

structure

corneal

of

the

disorders.

C.

e

M.

of

collagen

in

the

“Sma l l”

f ibr i ls

at

t he

“a”

c ol l age n

ass o c i ate s

and

“c”

w it h

b ands .

57.

i nte r a c -

Davidson

AE,

36.

Mas

Tur

V ,

Ophthalmol.

Sharif

conus:

R,

Rep .

38.

Bron

AJ,

etal.

e

pathogenesis

58.

Barr y

intriguing

Retin

of

Jayaswal

R,

etal.

59.

pathophysiolog y,

A

review

and

S,

therapeutic

Eye

Keratoconus.

Res.

J,

etal.

Pathogenesis

potential

of

1988;7(3):163.

Cont

e

with

riboavin

and

development

of

cellular

2008;19:82–93.

cornea

and

of

the

the

Eye:

sclera.

In:

Clinical

Kaufman

Application.

2003.

Campbell

changes

with

RJ.

age

e

in

ultrastructure

normal

of

corneas.

Arch

Schmidt

KC,

human

etal.

cornea.

High-voltage

Invest

electron

Ophthalmol

Vis

Sci.

Spurr

SJ,

etal.

Hemidesmosomes

formation

1983;9(97):849–857.

e

eect

of

of

age

on

power

human

analysis.

corneal

Acta

thickness.

Ophthalmol

1993;71(1):51.

Toward

Sci.

GO

quantitative

Bourne

of

analysis

techniques

of

and

corneal

their

endothelial

application.

WM,

and

Edelhauser

pathologic

HF ,

etal.

structure

and

e

corneal

function.

1982;89(6):531.

WM,

corneal

to

a

review

normal

Petroll

of

a

1989;66:626.

3rd,

the

Andrews

endothelial

apical

PM,

etal.

e

cytoskeletal

junctional

spatial

proteins

complex.

Invest

orga-

and

their

Ophthalmol

1995;36(6):1115.

GI,

Sibley

function

RC,

Hoee

the

corneal

of

Joyce

NC.

Eye

Joyce

NC,

in

Proliferative

Res.

FB.

Recent

studies

endothelial

layer.

on

the

Exp

nature

Eye

Res.

Harris

corneal

T ,

Joyce

old

and

DL,

Mello

of

DM.

endothelium:

Ophthalmol

Senoo

capacity

the

corneal

endothelium.

Prog

2003;22:359.

Vis

Sci.

NC.

Mechanisms

contact

of

inhibition

miotic

and

inhibi-

TGF-beta2.

2002;43:2152(Abstract).

Cell

young

cycle

donors.

Gambato

C,

Longhin

layers:

in

vivo

an

Exp

Mustonen

Abib

kinetics

Invest

cell

in

corneal

Ophthalmol

Barreto

Sarnicola

J

61.

C,

Farooq

update

endothelium

Vis

Sci.

2000;

J.

on

etal.

Aging

microscopy

and

study.

corneal

Graefe’s

Arch

2015;253:267–275.

MB,

Srivannaboon

Cornea.

AV ,

by

S,

in

etal.

vivo

Normal

scanning

slit

1998;17(5):485.

Behavior

Refract

evaluated

of

Surg.

Colby

K.

pathogenesis

corneal

endothelial

density

over

2001;27:1574.

Fuchs

and

endothelial

future

corneal

directions.

Eye

dys-

Contact

2019;45:1–10.

den

Bogerd

evidence

Bergmanson

Efron

N,

for

B,

Dhubhghaill

in

vivo

Clin

corneal

SN,

Koppen

endothelial

C,

etal.

A

review

regeneration.

of

Surv

2018;63:149–165.

JP .

Histopathological

Cornea.

Perez-Gomez

obser vations

wear.

Jr

Cataract

AG,

confocal

populations

microscopy.

FC,

Catania

McDonald

corneal

lifetime.

Van

RK,

E,

corneal

Ophthalmol.

polymegathism.

kerato-

prolactin-inducible

2018;67:150–167.

Cornea.

of

SM,

Biol.

P .

Ophthalmol.

Surv

60.

Hjortdal

ME,

implications

Retin

the

of

genetics.

disease.

2013;11:65–74.

the

Biol.

Physiolog y

WM,

normal

Grill

Cell

PA,

Sci.

Kaye

Lens.

of

2014;28:189–195.

C,

diagnosis,

Prog

AJ.

Hardcastle

2017;62:770–783.

Bak-Nielsen

the

protein.

S,

(Lond).

MacGregor

keratoconus:

37.

Hayes

Eye

Rock

Vis

Waring

a

r abbit

Bios c i

JL.

Sur f.

and

Dev

Elsevier ;

Bourne

MJ.

confocal

prote o g lyc an :

prote o g lyc an

Cell

Adler’s

morpholog y :

human

corneal

2004;78:503–512.

su l f ate

segment

1982;100:1942.

Herse

trophy :

keratoconus.

J

Doughty

Clin

Surv

56.

organization

keratoconus.

41:660.

of

1985;5:765.

35.

A,

from

1998;69:180.

2006:83–111.

etal.

and

Res.

c ol l age n

Siu

tion

Vis

2018;63:851–861.

Boote

Exp

JE,

t i ons :

J.

Doughty

of

1973;15:585.

networks

J

anterior

crosslinking

Ocul

cr ystallins

membrane:

IK,

vitro.

Inv

JP ,

Optom

implications

Ophthalmol.

Meek

Am

Hjortdal

Wang

cornea:

33.

Vrensen

human

J

PS,

Gipson

and

Bergmanson

cells.

Binder

Vis

Ul-

Ophthalmolog y.

Histopatholog y

aer

Corneal

Ubels

Louis:

DH,

relationship

1995;36(13):2557.

Snyder

the

L,

of

St

nization

Arch

1993;106:685.

29.

ed.

endothelium,

Ophthalmolog y.

2017;255:575–582.

posterior

Brookes

visualized

eds.

A,

Johnson

E.

Semin

HF ,

Alm

Optom

etal.

CC.

tting

principles.

Edelhauser

cell

cur vature.

2015;122:693–699.

28.

AI

Corneal

(Copenh).

e

lens

Spoerl

Ophthalmolog y.

Parekh

of

JV .

Statistical

Invest

2001;85:437.

LA,

imaging

trastructure

F ,

PL,

in

1968;7(5):501.

Vrensen

pre-Descemet’s

M,

Jester

Teng

1956;42:847.

1991;32:2234.

verte-

2013;120:1778–1785.

26.

Raiskup

microscopy

2015;56:2764–2772.

Sci.

E,

stroma

HS,

Tran

transparency

Ophthalmol.

Dua

G,

Benedek

aecting

Müller

Corneal

structure:

Vis

Ophthalmol

24.

C.

2015;49:1–16.

Shoa

Ophthalmol

Contact

Descemet’s

Cornea.

HM,

49

Cornea

1992;20(5):11.

Ophthalmol.

Knupp

Res.

C.

J.

10th

R,

2015;34:786–790.

21.

Astin

transparency.

2000;19(4):417.

20.

Katzin

Ophthalmol.

ultraviolet

colla-

1991;32:2244.

critical

HH,

J

Lens

Invest

1983;24(8):1015.

e

Chi

Am

3

of

Exp

I,

stromal

analysis

of

corneal

endothelial

1992;11:133.

Morgan

PB.

keratocytes

Optometry.

Confocal

during

2002;85(3):156.

microscopic

extended

contact

lens

CHAPTER

50

62.

Lui

ZG,

wear

Pugfelder

on

corneal

Connor

CG,

dothelial

Holden

BA,

extended

65.

Vis

Holden

BA,

eects

Res.

66.

Zagrod

ME.

J

long-term

and

contact

surface

lens

85.

regularity.

Sweeney

Sci.

DF ,

lens

lens-induced

functional

Physiol

Vannas

wear

on

Optic.

A,

the

corneal

signicance

and

en-

86.

1986;63:539.

etal.

Eects

human

of

cornea.

the

A,

M,

long-term

Oph-

87.

M,

MacRae

SM,

and

contact

Cruzat

Suda

aphakic

1988;106:70.

so

L,

etal.

wear

of

Epithelial

contact

and

lenses.

endothe-

Curr

88.

Eye

T,

etal.

extended

Corneal

contact

endothelial

lens

wear.

changes

Arch

M,

lenses

Y ,

ner ves

Lawrenson

Shellans

on

the

endings

in

the

health

Ruskell

limbal

S,

etal.

corneal

e

eects

endothelium.

of

hard

Am

J

90.

Oph-

P .

and

GL.

In

vivo

confocal

disease.

e

Ocul

structure

conjunctiva

of

the

microscopy

Sur f.

of

of

Müller

LJ,

human

71.

Marfurt

Pels

CF ,

Müller

LJ,

contents

73.

Bonini

Eye.

74.

Yu

E,

J,

Exp

2017;15:15–47.

corpuscular

human

P ,

etal.

eye.

J

92.

ner ve

factor

Zhang

M,

mediates

Exp

Olzi

Vis

Anatomy

organization

Sci.

of

of

D,

F ,

Eye

etal.

etal.

Res.

Liu

S,

Li

receptor

J,

Tan

corneal

subtypes

KI,

the

human

corneal

94.

Corneal

ner ves:

structure,

Ophthalmol

76.

Vis

Sci.

keratitis:

a

Vascular

repair.

endothelial

Invest

current

GK,

Vis

Sci.

Expression

human

and

cornea

function

and

of

muscarinic

conjunctiva.

its

PC.

pathogenesis.

Int

of

the

Ophthalmol

98.

cornea:

Clin.

Secker

and

79.

to

Beebe

DC.

mental

Semin

81.

JT.

Stem

Nozaki

Corneal

Cell

M,

VEGF

Dev

Mandathara

P ,

and

Biol.

Singh

stem

cells,

Deciency

MH,

and

II+

H,

N,

etal.

Corneal

Nature.

a

avascularity

review

pathophysiolog y

is

2006;443:993–997.

of

of

two

the

develop-

Said

Drug

In:

drug

Des.

J

Chin

therapies

Med

for

corneal

2017;90:653–664.

Hart

WM

Application.

Mandell

Berglin

the

KJ,

Sci.

human

Invest

Mergler

in

S,

and

AS.

and

of

9th

the

Jr,

ed.

ed.

St

cornea.

Adler’s

Louis:

Int

Res.

across

transport

eds.

corneal,

con-

2004;78:527–535.

in

the

Ophthalmolog y

Diseases

and

cornea.

In:

Research:

Drug

Delivery.

2008.

Aquaporin-3.dependent

corneal

cell

migra-

re-epithelialization.

Invest

2006;47:4365–4372.

L,

Severson

corneal

U.

EA,

etal.

endothelium

localization

Pleyer

transport

Eye

water

CJ,

during

Ophthalmol

into

uid

Exp

Ophthalmic

Pres;

Verkman

Vis

in

Physiolog y

Barnstable

Ophthalmol

and

Vis

e

and

evidence

Sci.

for

Expression

retinal

role

in

of

JAM-

pigment

barrier

func-

2007;48:3928–3936.

human

electrophysiolog y

corneal

and

ion

endothelium:

channels.

new

Prog

Retin

Eye

2007;26:359–378.

Zhang

J,

Patel

DV .

e

review

pathophysiolog y

of

molecular

and

of

Fuchs’

cellular

endothelial

insights.

Exp

Eye

2015;130:97–105.

Fischbarg

J.

Biolog y

the

of

Fatt

I,

and

carbon

e

corneal

Eye.

Bieber

MT,

vol.

Pye

dioxide

cells

F ,

avascular

tissues.

M,

McCulley

101.

Baum

at

endothelium.

10.

SD.

in

the

contact

J,

keratoconus.

etal.

Cont

A

pilot

Lens

study

Anter

on

Eye.

Dong

cells

N,

of

etal.

major

from

Cauterization

of

central

histocompatibility

limbal

basal

Elsevier ;

Steady

in

lens.

state

vivo

Am

J

In:

Fischbarg

J,

ed.

e

2006.113–125.

distribution

cornea

of

an

Optom

Arch

eye

Am

of

oxygen

covered

Acad

by

a

Optom.

102.

103.

JP ,

Larrea

X,

DG,

characterisation

of

2016;100:315–322.

Al-Aqaba

M,

etal.

Clinical

vascularization.

Br

evaluation

J

JP .

H KS .

e ds .

e

C or ne a l

e nd ot heliu m .

O phthalmolog y.

circulation

limbus).

Maurice

of

water

Büchler

Vis

DH,

Eye.

DM,

2nd

e d.

In :

Mosby ;

of

uid

at

the

limbus

(ow

and

dif-

1989;3:114.

McCarey

across

Lu

L.

P .

A

of

the

BE.

corneal

Sci.

e

active

and

passive

endothelium. Exp

Eye

Res.

channel

diusion

diusivity

model

and

of

the

cornea

consumption.

Invest

2009;50:1076–1080.

M,

Y ee

endothelium,

RW ,

etal.

Eects

of

Pump

age

function

and

cornea

of

the

guttata.

1985;92:759–763.

Stress-induced

K+

transient

oxygen

Matsuda

corneal

Ophthalmolog y.

104.

and

Ophthalmol.

JS,

assessment

Geroski

by

corneal

the

human

class

Cornea.

At lur i

1984;39:335.

cornea

complex

epithelium.

ML,

D u ker

the

transport

Kokkinakis

in

McD er mott

fusion

2010;29(1):73–79.

LA,

neovascularization

2004:422–430.

100.

2008;19:125–133.

recruitment

Langerhans

Faraj

J,

proliferation

Ophthalmol

induces

84.

Levin

Efron N, Al-Dossari M, Pritchard N. Confocal microscopy of the

Lin

BO.

Aquaporins

Humana

for

W ,

Corneal

therapeutics.

Recent

cornea.

epithelia.

Transporters

2018;41:219–223.

Chen

Lens.

1968;8:527–560.

lens

AS.

NJ:

Yanof f

bulbar conjunctiva in contact lens wear. Cornea. 2010;29(1):43–52.

83.

99.

2008;4:159–168.

transparency :

Stapleton

Langerhans

Rev.

epithelial

receptor-1.

Maintaining

physiolog y

Cell

corneal

82.

BK,

soluble

tension

Cont

1969;46:3–14.

Daniels

regulation.

Ambati

due

80.

GA,

and

gas-permeable

1983;23(1):27.

78.

OA.

Verkman

Res.

97.

Neovascularization

Hedbys

dystrophy–a

Invest

2007;48:2987–2996.

of

etal.

Biol

Clinical

Electrolyte

Res.

96.

Burger

concepts

etal.

e

Eye:

Candia

insights

Lim P , Fuchsluger TA, Jurkunas UV . Limbal stem cell deciency and

Klintworth

JL.

X,

Clin.

tion.

growth

Ophthalmol

S,

epithelium:

review.

corneal neovascularization. Semin Ophthalmol. 2009;24:139–148.

77.

Eye

1992:29.

Mishima

A

2003;76(5):521–542.

Neurotrophic

etal.

ner ve

etal.

on

the

TC,

Chem

Ophthalmol

tion

95.

Matis

DT,

93.

1996;37(4):476.

2008;49:3870–3878.

75.

Wang

Ubels

of

contact

oxygen

Chen Y , ompson DC, Koppaka V , etal. Ocular aldehyde dehy-

Ocular

2003;17:989–995.

CQ,

S,

Tombran-Tink

Anat.

2010;90:478–492.

Kruse

function.

Rama

Ultrastructural

Ophthalmol

S,

Res.

CF ,

GF .

Inv

Deek

Eye

Marfurt

and

S,

Vrensen

ner ves.

Cox

inner vation.

72.

Wang

Totosa

corneal

Lin

antiangiogenic

Liu

junctival

1991;177:75.

70.

HM,

2015;78:323–330.

JS,

Critical

lens

neovascularization.

Assoc.

Pepose

etal.

tear

1):S291–S295.

contemporar y

X,

AL,

and

drogenases: protection against ultraviolet damage and maintenance

91.

Hamrah

in

JG,

89.

Nguyen

of transparency for vision. Prog Retin Eye Res. 2013;33:28–39.

Matsuda

Qazi

corneal

Chang

Physiolog y

Oph-

1986;102:50.

A,

CC,

Mosby ;

Inaba

with

Hsu

HJ,

transmissibility

neovascularization.

Nilsson

extended

Y ang

preclude

and

Invest

KK,

oxygen

2018;44(Suppl

possible

1985;26:1489.

Vannas

Y eung

lens

to

Contact

Optom

thalmol.

corneal

69.

of

1985;4:739.

Matsuda

thalmol.

68.

Am

from

associated

67.

eects

cur vature,

2000;107:105.

contact

thalmol

lial

e

polymegathism:

mechanisms.

64.

SC.

Cornea

thickness,

Ophthalmolog y.

63.

3

corneal

activation.

epithelial

Prog

Retin

apoptosis

Eye

Res.

mediated

2006;25:

515–538.

105.

Mertz

GW .

Optom

Overnight

Assoc.

swelling

of

1980;51:211–214.

the

living

human

cornea.

J

Am

CHAPTER

106.

B onanno

JA.

mechanism

Identity

in

the

and

regulation

corneal

of

epithelium.

ion

transport

Prog

Retin

128.

Eye

Res.

2003;22:69–94.

107.

Rom

ME,

corneal

WB,

and

Meyer

CJ,

topography.

etal.

Relationship

Cont

Lens

Assoc

between

129.

Ophthalmol

J.

Hanna

C,

epithelial

109.

Hanna

110.

Kruse

layer

C,

human

130.

O’Brien

of

JE.

the

Bicknell

eye.

FE.

Arch

Stem

C ell

production

cornea.

DS,

Arch

O’Brien

Ophthalmol.

cells

and

and

migration

Ophthalmol.

JE.

Cell

in

the

in

the

131.

1961;65:695.

corneal

epithelial

o

R,

Eye.

maintenance.

112.

Tseng

SC.

J.

e

Invest

Concept

X,

Y ,

Z

hypothesis

Ophthalmol

and

Vis

application

Sci.

of

of

corneal

epithelial

stem

cells.

Gipson

and

Eye.

133.

IK,

Spurr-Michaud

anchoring

bril

and

SJ,

collagen

wound

Tisdale

appears

healing.

AS.

Hemidesmosome

synchronously

Dev

Biol.

Br

during

134.

1988;126:

MA.

Corneal

integrins

and

their

functions.

Exp

Eye

Res.

135.

2006;83:3–15.

KS,

Oh

mologous

Korean

116.

Pastor

J

JS,

Kim

IS,

Calonge

G,

A

Clinical

persistent

wound

ecacy

corneal

of

topical

epithelial

ho-

136.

Zelenka

M.

Epidermal

N,

Grant

healing.

growth

study.

M,

etal.

Acta

factor

Cornea.

Eects

Ophthalmol

and

corneal

PS,

in

Suzuki

Arpitha

the

the

K,

lens

of

growth

Suppl.

137.

factors

Tanaka

P .

and

Coordinating

cornea.

T,

Enoki

M,

membrane

epithelial

Crosson

closure.

Ter vo

the

122.

CE,

wound

Klyce

Invest

T,

van

ocular

Nishida

T,

epithelial

1992;

138.

cell

Semin

proliferation

Cell

Dev

Biol.

and

mi-

Stapleton

tosis

139.

etal.

and

Coordinated

junctional

healing.

Invest

reassembly

in

Gipson

of

the

proteins

during

Ophthalmol

Vis

140.

Sci.

SD,

Setten

surface.

B euerman

GB,

Ann

Nakagawa

migration

F ,

Kim

human

IK,

S,

of

Vis

RW .

Sci.

Corneal

epithelial

wound

repair

Ophthalmol.

Karamichos

corneal

T,

etal.

Wound

healing

of

141.

1992;24:19.

Awata

T,

cultured

Sci.

A,

of

corneal

Acta

Hopp

Estey

Biol.

the

ocular

media.

epithelium

Ophthalmol

against

Scand.

B,

etal.

to

400-nm

T,

etal.

UV

range.

absorbance

Invest

of

the

Ophthalmol

e

role

mechanisms

of

corneal

against

cr ystal-

oxidative

stress.

2008;19:100–112.

S,

Takise

S,

due

etal.

to

Morphological

ultraviolet

change

radiation

in

in

welders.

1984;68:544.

early

PF ,

corneal

Carr

in

JM,

Kasses

etal.

rabbit

J,

etal.

epithelial

Fibronectin

cornea

in

AA,

rabbit.

S,

promotes

situ.

Mechanisms

cells.

Tisdale

of

the

Invest

Silverstein

epithelium.

J

Cell

DS.

Laser

experience.

in

J

situ

keratomileusis

Cataract

Refract

to

Surg.

Adv

E xp

A,

etal.

corneal

of

142.

apop-

Med

143.

Reassembly

Vis

AM,

e

role

Kenyon

of

DR,

basement

Lakshman

N,

Sci.

144.

during

morpholog y

matrix

and

mechanical

Galbar y

and

EJ.

scleral

1986;27(10):1478.

the

Bhan

WM.

etal.

1989;

Adhesion

membrane.

Regulation

collagen

properties.

P .

tissue

Invest

of

JD,

etal.

cell

of

laser

endothelium

in

3

situ

years

2001;131:1.

studies

for

Eects

corneal

in

pat ients

hyp eropia.

J

aer

Ref ract

pho-

Surg.

Phototherapeutic

Scand.

on

K,

keratectomy :

Chuckpaiwong

the

12

years

of

experi-

2003;81(1):19.

corneal

V .

Eect

endothelium.

J

of

laser

Refract

in

Surg.

Beiser

JA,

Kass

MA,

Hypertension

etal.

Central

Treatment

corneal

Study

thickness

(OHTS).

Ophthal-

2001;108(10):1779.

A,

Browning

on

AC,

Shah

intraocular

pneumotonometer,

Tono-Pen.

KM,

laser

Invest

S,

etal.

pressure

Eect

of

corneal

measurements

Goldmann

Ophthalmol

J

Vis

Sci.

situ

AA.

applanation

Vis

Changes

keratomileusis.

Bourne

van

J

Shimizu

pressure

cell

K,

in

Shoji

eyes

Ophthalmol.

RG,

Sci.

with

tonometer,

2002;43(5):

J

in

intraocular

Refract

Surg.

pressure

2001;

WM,

etal.

Underestimation

laser

in

situ

of

keratomileusis.

B,

Tu

SJ,

etal.

Aging

and

the

cornea.

1997;81:814–817.

Nelson

changes

N,

aer

2002;46(6):645.

Mulholland

Ophthalmol.

over

LR,

a

Hodge

ten-year

DO.

Central

period.

corneal

Invest

endothe-

Ophthalmol

Vis

1997;38(3):779.

den

Berg

from

TJ,

320

Tan

to

KE.

700

Light

nm

for

transmittance

dierent

ages.

of

the

Vis

human

Res.

1994;

34(11):1453.

Naeser

K,

the-rule

by

Ophthalmol

Bahnassy

in

A,

J

Faragher

cornea

of

remodeling

Ophthalmol

RD,

the

Ophthalmol.

Kosalprapai

Savini

and

G,

Bregnhøj

oblique

corneal

JF .

Age-related

astigmatism.

changes

Acta

in

with-

Ophthalmol.

2018;96:600–606.

147.

Shao

X,

Zhou

astigmatism.

C onnective

wounds.

J

on

keratec tomy

Ocular

Arimoto

Sci.

Am

reorganization

Invest

Am

Ophthalmol

P ,

R ashad

lial

146.

Petroll

Stulting

Endot helial

keratomileusis

Japanese

Biol.

epithelium

Ophthalmol

JD,

(LASIK)

17(4):420.

Biol.

1968;65(3):339.

D,

Acta

Brandt

Br

structures

the

NS.

Simaroj

aer

2007;48:5030–5037.

Davison

MJ,

intraocular

corneal

broblast

extracellular

in

of

1389.

145.

regenerating

127.

role

defense

Siganos

myopia:

Fagerholm

and

1986;27(4):464.

Päällysaho

Med.

Spurr-Michaud

Khodadoust

Vis

endo-

endothelial

1962;1:776.

240-

endothelium

JG,

thickness

30:425.

126.

Dev

Ophthalmol.

Jabbur

the

Ophthalmol

anchoring

wound

125.

WJ,

Matsumura

molog y.

2002;506:827–834.

124.

Fuchs

2003;19:S237.

2008;

1983;97:1653–1657.

123.

I,

ence.

2000;41:2495–2500.

121.

Transmission

Sci.

damage.

the

cellular

Cell

Collins

in

basement

corneal

120.

of

without

2003;19:142.

1992;11(4):311.

19:113–124.

of

J

in

Black

the

Pallikaris

situ

gration

119.

Treatment

stripping

2002;43(7):2165.

N,

toref rac tive

202:60.

118.

Vis

Nógrádi

postoperatively.

disorders.

1992;6(1):12.

multicenter

Chegini

corneal

etal.

in

Ophthalmol.

healing.

Schultz

on

KA.

2016;35:1267–1273.

JR.

Protective

keratomileusis

bronectin

JC,

wound

117.

Colby

1997;23:39.

Stepp

Kim

L,

corneal

treat

253.

115.

Karai

the

development

114.

in

Semin

1989;3:141.

113.

A.

cornea

Sci.

Lassen

lins

1983;24(10):1442.

limbal

Wolter

radiation

Kolozsvári

Vis

132.

Friend

Podskochy

P ,

Descemet

Cornea.

Ophthalmol

human

regeneration.

by

51

Cornea

2004;82:714–717.

adult

1994;8:170.

111.

Veldman

EA,

ultraviolet

1960;64:536.

turnover

Boettner

Invest

1995;21(3):191.

108.

DS,

dystrophy

keratoplasty.

Keller

edema

Borkar

thelial

3

148.

Ueno

Y ,

anterior,

J

K-J,

Pan

Refract

Hiraoka

T,

posterior,

2014;30:192–197.

A-P ,

Surg.

etal.

Beheregaray

and

Age-related

changes

in

corneal

2017;33:696–703.

total

S,

etal.

corneal

Age-related

astigmatism.

J

changes

Refract

in

Surg.

CHAPTER

52

149.

Batawi

plexus

H,

Shalabi

analysis

2018;44(Suppl

150.

Tavakoli

for

M,

corneal

Ferdousi

a

Cornea

Joag

a

M,

new

etal.

Sub-basal

soware

corneal

technolog y.

Eye

ner ve

Cont

151.

M,

morpholog y

2015;38:838–843.

p opulation

vivo,

Petropoulos

multinational

Hollingswor t h

A

Lens.

1):S199–S205.

ner ve

microscopy :

N,

using

3

IN,

assessed

normative

etal.

using

data

Normative

corneal

set.

Care.

Perez-G ome z

slit-s canning

of

t he

I,

Mut alib

nor mal

confo cal

cor ne a

micros cop e.

HA,

etal.

using

O ptom

an

152.

Barraquer-Somers

epithelial

90:729.

iron

E,

Chan

deposition.

CC,

Green

WR.

Ophthalmolog y.

Corneal

1983;

in

Vis

2001;78(10):706.

values

confocal

Diabetes

J,

study

S ci.

4

Sclera,

Changes

corneal

in

the

stroma

corneal

tissue

continues

as

occur

the

at

sclera

the

and

limbus

the

where

corneal

the

epithe-

a

Conjunctiva,

factor

when

develops

emmetropization

between

ages

8

to

14

and

does

years

not

and

Limbus

occur.

is

Most

caused

by

myopia

elongation

3

lium

and

continues

Tenon

as

the

capsule

are

conjunctival

added

epithelium.

between

the

sclera

e

and

episclera

the

of

the

bulbar

conjunctiva.

vitreal

e

chamber.

sclera

ponents

can

is

a

dynamic

change

in

tissue;

response

the

to

connective

changes

in

tissue

com-

visual

envi-

the

3

ronment.

on

the

Animal

retina

can

studies

elicit

a

have

shown

signal

to

that

scleral

poor

tissue

image

quality

components

to

SCLERA strengthen

e

sclera

tissue

coat

forms

of

the

the

posterior

globe.

e

ve-sixths

sclera

of

maintains

the

the

connective

shape

of

the

best

or

location

peripheral

weaken

for

a

in

clear

portion

of

an

attempt

image.

vision

It

is

to

has

move

also

more

the

been

retina

found

important

to

the

that

the

than

central

9

globe,

vides

oers

an

resistance

attachment

thickness

of

the

to

for

sclera

internal

the

and

external

extraocular

varies

from

1

mm

forces,

muscle

at

the

and

pro-

insertions.

posterior

e

pole

to

vision

in

tifocal

contact

myopic

controlling

myopia.

lenses

defocus

or

or

Studies

of

orthokeratolog y

reduce

relative

patients

lenses,

hyperopia

in

the

1

0.3

mm

just

behind

the

rectus

muscle

10

insertions.

eral

area,

show

Scleral

Scleral

e

Histological

sclera

is

a

thick,

Features

dense

myopia;

connective

tissue

t

layer

that

is

con-

a

slowing

remodeling

the

scleral

of

myopic

causes

tissue

is

the

with

which

mul-

increase

midperiph-

11

progresssion.

axial

lengthening

weakened

and

thins.

that

In

occurs

in

progressive

myopia, existing collagen is degraded, the production of new colla-

12–14

tinuous

the

with

collagen

brils

are

the

corneal

brils

in

arranged

stroma

this

in

tissue

at

the

varies

irregular

limbus.

from

bundles

25

that

e

to

diameter

of

230

nm.

ese

branch

and

inter-

gen is reduced, and matrix proteoglycans are lost.

bute

the

these

alterations

extracellular

during

matrix,

but

myopia

an

Studies attri-

development

additional

piece

of

to

the

changes

puzzle

in

may

2

lace.

e

bril

size,

orientation,

and

arrangement

are

inuenced

be

the

role

played

by

scleral

broblasts.

If

stimulated

to

become

3

by

proteoglycans

in

the

extracellular

matrix.

Bundle

widths

and

myobroblasts,

they

can

provide

biochemical

signals

leading

13

thicknesses

than

the

vary,

deeper

with

the

bundles.

external

e

bundles

orientation

narrower

of

these

and

scleral

thinner

to

14

changes in collagen production and degradation of tissue.

lamellae

is very irregular compared with the corneal lamellae organization. CLINICAL

e

lamellae

in

the

outer

regions

of

the

sclera

run

The

parallel

to

the

surface,

with

interweaving

between

COMMENT: Scleral

Ectasia

approximately

them,

whereas

progression

often

causes

of

myopia

scleral

caused

thinning,

by

axial

particularly

elongation

at

the

in

a

posterior

highly

pole

myopic

where

the

eye

col-

4

in

the

inner

regions

the

lamellae

run

in

all

directions.

is

ran-

dom arrangement and the amount of interweaving contributes to

the

lel

strength

the

the

rectus

exit.

and

limbus

e

exibility

anteriorly.

muscle

collagen

of

insertions

of

the

the

e

eye.

In

pattern

and

general,

becomes

circular

extraocular

the

the

tendons

optic

at

the

the

bril

tissue

diameter

can

bulge

and

the

bundle

outward

size

causing

are

scleral

15

reduced.

As

the

sclera

thins,

ectasia.

paral-

meridional

around

muscle

brils

3

lagen

near

nerve

inser-

Scleral

e

Spur

scleral

spur

is

a

region

of

circularly

oriented

collagen

5

tions

merge

Elastic

and

bers

interweave

with

have

incidence

a

low

3

sometimes

they

are

within

less

4

6

brils

in

the

Fibroblasts

than

of

the

sclera.

sclera

between

and

bundles

that

entirety,

the

extends

scleral

from

spur

is

the

inner

actually

aspect

a

ring,

of

the

sclera.

although

on

In

its

cross-

7

bundles.

numerous

the

in

the

are

cornea.

present,

e

although

stromal

ground

substance is similar to the corneal ground substance but contains

section

and

it

4.2).

appears

At

the

wedge

spur’s

shaped,

posterior

resembling

edge,

its

a

bers

spur

(Figs.

blend

with

4.1

the

more obliquely arranged scleral bers. e posterior scleral spur

8

fewer

glycosaminoglycans.

merges

with

the

choroidal

e

tissue

innermost

in

the

aspect

of

suprachoroid

the

sclera

is the origin of the ciliar y muscle bers and most of the trabecu-

lar

layer.

meshwork

collagen

Scleral

Changes

in

refractive

emmetropic.

error

components

When

develops.

tropic

or

A

these

myopic

hyperopic

sheets

the

spur

attach

is

to

its

anterior

continuous

with

aspect,

that

of

the

such

that

the

trabeculae.

Myopia

Early childhood growth of the eye requires coordinated changes

in

of

eye,

and

eye

factors

size

are

for

not

eye

generally

and

changes

the

eye

to

coordinated,

is

in

larger

than

scleral

become

refractive

an

tissue

emme-

may

be

Scleral

e

the

size

Opacity

opacity

number

and

of

of

the

sclera

distribution

one-fourth

the

depends

glycosaminoglycans,

of

number

the

of

on

the

collagen

several

factors,

amount

brils.

of

e

glycosaminoglycans

including

water,

sclera

that

are

and

the

contains

present

in

53

CHAPTER

54

4

Sclera,

Conjunctiva,

and

Limbus

Conjunctiva

Episclera

Cornea Sclera

Schlemm

Trabecular

canal

Scleral

spur

Ciliary

body

meshwork

muscle

Iris

Fig.

the

cornea,

and

as

a

probable

4.1

consequence,

Scleral,

the

sclera

episcleral,

is

and

conjuncti val

relatively

e

canals

anatomy.

that

pass

through

the

sclera

carr y

ner ves

and

ves-

1

dehydrated

(68%)

compared

with

the

cornea.

e

greater

varia-

tion in bril size and the irregular spacing between scleral compo-

3

sels

the

eye.

rior

and

anterior

is

disease.

In

almost

through.

sclera

white,

the

is

but

it

may

newborn,

transparent

e

visible

sclera

appear

the

and

also

through

the

conjunctiva

colored

sclera

may

the

has

a

underlying

appear

as

a

result

bluish

blue

tint

vascular

in

and,

of

age

if

or

because

uvea

connective

it

shows

in

the

Likewise,

of

the

canals

are

by

which

designated

by

disease

their

can

exit

location.

or

e

enter

are

the

are

located

passages

for

around

the

the

posterior

posterior

ciliar y

scleral

poste-

arteries

foramen

presence

the

sclera

buildup

of

of

fatty

may

deposits,

appear

metabolic

which

yellow

waste

in

can

liver

occur

with

disease

4.4).

terior

to

from

the

Foramina

and

middle

equator

are

passages

age.

because

products.

Scleral

near

for

muscular

and

the

the

apertures

carr y

limbus

anterior

lie

approximately

and

the

at

vortex

the

ciliar y

veins.

muscle

vessels,

4

ner ves

mm

e

insertions

which

are

pos-

anterior

and

are

branches

arteries.

imal

blood

other

Canals

Blood

Supply

Because it is relatively inactive metabolically, the sclera has min-

supply.

tissues,

contains

Scleral

the

apertures

the

e

tissue

diseases that cause scleral thinning. e sclera might appear yel-

low

e

routes

Color

healthy,

is

possible

apertures

(Fig.

e

are

4

nents induce light scattering, which renders the sclera opaque.

Scleral

and

branches

no

but

Vessels

the

capillar y

from

the

pass

sclera

beds.

is

through

the

considered

Nourishment

episcleral

and

sclera

en

avascular

is

furnished

choroidal

route

to

because

vessels,

by

as

it

small

well

as

1

e

sclera

anterior

e

scleral

optic

which

is

contains

a

number

foramen

ner ve

bridged

passes

by

a

is

of

the

area

through

network

foramina

of

the

and

occupied

posterior

scleral

tissue

by

canals.

the

scleral

called

e

branches

of

the

long

posterior

ciliar y

arteries.

cornea.

foramen,

the lamina

Scleral

Innervation

Sensor y

inner vation

cribrosa (Fig. 4.3). e lamina cribrosa is similar to a sieve, with

branches

inter woven

is

of

the

short

is

supplied

ciliar y

to

ner ves.

the

e

posterior

remainder

of

sclera

the

by

sclera

1

optic

ner ve

collagen

bundles

brils

pass.

forming

e

canals

lamina

through

cribrosa

is

which

the

the

ser ved

by

branches

of

the

long

ciliar y

ner ves.

weakest

16

area

of

the

outer

connective

tissue

Aging

tunic.

Fatty

CLINICAL

COMMENT: Optic

Because

lamina

sue

inside

the

the

layer,

the

optic

it

is

the

eye.

nerve

A

cribrosa

area

that

cupping

may

be

is

the

will

out

likely

ectasia

in

Cupping

weakest

most

or

evident

Nerve

of

patients

area

be

of

with

may

in

the

cause

Sclera

the

sclera

to

appear

yellow.

Scleral

col-

lagen and elastic bers degenerate, and the concentration of cer-

the

affected

the

Changes

deposits

center

outer

by

area

elevated

connective

increased

of

the

tis-

surface

intraocular

tain proteoglycans is decreased causing scleral thinning and loss

pressure

3

of elasticity.

e bers of the lamina cribrosa become stier and

less

with

of

resilient

age.

Changes

in

the

laminar

pores

in

the

aged

pressure

lamina

cribrosa

may

cause

the

ner ve

bers

passing

through

the

and is one of the clinical signs sometimes noted in glaucoma. This cupping can

openings also

be

attributable

to

the

loss

of

nerve

ber

tissue

of

the

optic

nerve

to

become

more

vulnerable

to

injur y,

contributing

head. 17–20

an

increased

susceptibility

to

glaucomatous

damage.

to

CHAPTER

4

Sclera,

Conjunctiva,

and

55

Limbus

b

c

1

a

A

d

2

B

C

d

e

j

D

i

h

f

g

k

i

Fig.

4.2

stroma

(C).

in

Limbus. The

(2). T enon

Limbal

this

stroma

region.

which

extend

different

limbal

capsule

conjunctiva

(B)

occupies

Conjunctival

anteriorly

planes. Vessels

forms

the

area

stromal

to

the

a

(A)

thin,

(D)

and

vessels

the

formed

is

are

termination

forming

is

poorly

of

by

epithelium

dened

composed

also

seen

Bowman

intrascleral

(d)

and

(1)

connective

of

scleral

(a). They

layer

and

form

(arrow).

deep

and

scleral

loose

tissue

corneal

peripheral

Episcleral

plexus

connective

layer

(e)

over

the

tissues

corneal

vessels

are

tissue

episclera

that

merge

arcades

(c)

shown

are

(b),

cut

within

in

the

limbal stroma. The scleral spur has coarse and dense collagen bers (f). The anterior part of the longitu-

dinal

portion

Schlemm

(i)

are

outer

travel

of

ciliary

canal

to

toward

(h)

cords

the

muscle

and

of

loose

uveal

trabecular

(g)

merges

tissues

of

meshwork

meshwork

with

its

the

wall

(j). An

at

the

scleral

are

iris

spur

seen.

process

level

of

and

Sheets

(k)

the

is

trabecular

of

the

seen

anterior

to

meshwork. The

corneal

arise

portion

trabecular

from

of

the

scleral

iris

lumen

surface

spur.

of

meshwork

and

Descemet

membrane terminates (double arrows) at the anterior border of the limbus. (From Hogan MJ, Alvarado

JA, Weddell

JE.

Histology

of

the

Human

Eye,

Philadelphia:

Saunders;

capsule

by

1971 .)

strands

of

connective

tissue,

becomes

thinner

EPISCLERA toward

e

episclera

that

lies

scleral

just

is

a

loose,

outer

vessels

are

to

vascularized,

the

visible

sclera

(see

through

the

connective

Fig.

4.1).

tissue

e

conjunctiva.

back

of

the

eye.

layer

larger

e

the

epi-

anterior

CLINICAL

COMMENT: Scleritis

and

Episcleritis

Scleritis involves the deep episcleral vessels, and episcleritis affects the supercial

episcleral vessels. To differentiate between the two, the conjunctival tissue can be

ciliar y

arteries

branch

to

form

supercial

and

deeper

epi23

21

scleral

vessels.

manually

22

ere

are

capillar y

networks

in

the

vessels

just

anterior

to

the

rectus

muscle

inser tions

and

manipulated.

Supercial

episcleral

vessels

are

mobile

whereas

deeper

episclera are

more

rmly

attached

to

the

scleral

tissue.

In

addition,

supercial

ves-

surrounding sels will blanch with topical phenylephrine, but the deep vessels will not blanch.

the

peripheral

cornea.

e

episclera,

which

is

joined

to

Tenon

CHAPTER

56

4

Sclera,

Conjunctiva,

and

Limbus

and

oblique

groups.

thicker

and

contains

sion

of

the

sule

contains

Anterior

smooth

to

the

muscle

equator,

bers

Tenon

that

capsule

regulate

the

is

ten-

24

of

70

in

bril

to

extraocular

110

collagen

nm.

In

muscles.

brils

older

In

of

young

uniform

individuals,

people,

shape

there

is

Tenon

and

greater

variation

25

shape,

and

broblasts and

ratio

diameters

some elastic

compared

with

the

var y

bers

number

from

30

to

160

collagen

26

nm.

are present but in

of

cap-

diameters

Few

a ver y

small

brils.

CONJUNCTIVA

e

conjunctiva

is

a

thin,

translucent

mucous

membrane

that

runs from the limbus over the anterior sclera, forms a cul-de-sac

at

the

the

superior

eyelids.

globe.

are Fig.

4.3

e

It

and

inferior

ensures

conjunctiva

continuous

with

fornices,

smooth

can

one

and

turns

movement

be

divided

another :

(1)

of

into

the

anteriorly

the

eyelids

three

bulbar

to

line

over

sections

the

that

conjunctiva

The lamina cribrosa is seen as grey meshwork appear -

covers the sclera; (2) the tissue lining the eyelids is the palpebral ance

within

the

cup

of

the

optic

disc.

conjunctiva, or tarsal conjunctiva; and (3) the conjunctival for-

nix

is

the

cul-de-sac

connecting

the

palpebral

and

bulbar

sec-

tions (Fig. 4.5). Conjunctival stem cells are scattered in the basal

TENON

CAPSULE layer throughout the conjunctiva, but are more numerous in the

27

Outer

to

called

T enon

the

the

limbus,

space

cavity

episcleral

capsule

fusing

between

within

is

T enon

thin,

(fascia

with

which

a

the

bulbi).

sclera

capsule

the

brous

and

globe

can

at

sheet

It

connective

extends

the

the

of

optic

It

posteriorly

nerve.

episclera

move.

tissue

A

serves

protects

from

e bulbar conjunctiva is translucent, allowing the sclera to show

through, and is colorless except when its blood vessels are engorged.

a

fascial

Bulbar conjunctiva is loosely adherent to the underlying tissue up to

supports

within

the globe and attaches it to the orbital connective tissue.

e

in

a

collagen

brils

that

three-dimensional

form

Tenon

network

of

capsule

are

longitudinal,

28

region.

potential

as

and

fornix

3

mm

of

the

cornea,

where

it

becomes

tightly

arranged

e

horizontal,

Superior

the

conjunctiva

fascial

forming

extensions

of

the

the

fornices

levator,

tarsal

is

attached

plate,

rectus

muscle

Superior

Shor t

oblique

muscle

posterior

ciliar y

ar teries

Vor tex

vein

Lateral

rectus

Medial

muscle

rectus

muscle

Long

posterior

ciliar y

ar ter y

Optic

ner ve

Long

Inferior

ciliar y

ner ve

oblique

muscle Vor tex

Shor t

vein

ciliar y

ner ves Inferior

Fig.

4.4

short

the

Posterior

ciliar y

middle

sclera. The

arteries

and

apertures.

optic

ner ves

ner ve

pass

adherent

and

merges with the underlying T enon capsule and episclera.

passes

through

rectus

muscle

through

posterior

the

posterior

apertures;

and

scleral

vortex

foramen;

veins

long

pass

and

through

and

loosely

to

extraocular

CHAPTER

At

the

4

Sclera,

eyelid

Conjunctiva,

margin,

the

and

57

Limbus

nonkeratinized

squamous

cells

of

the

palpebral conjunctival epithelium are continuous with the keratin-

ized squamous epithelium of the epidermis of the eyelid. is area, Fornix

called

the

mucocutaneous

junction,

is

the

tissue

that

makes

con-

tact with the cornea as the eyelid blinks (see Fig. 2.15).

e

thelial

cosa.

conjunctiva

layer

and

Goblet

a

cells,

is

composed

connective

which

of

two

tissue

produce

layers,

a

stratied

stromal

layer,

mucous

component

the

the

epi-

submu-

of

the

and

are

Bulbar

tear

conjunctiva

lm,

are

distributed

found

in

located

within

throughout

the

the

the

conjunctiva.

conjunctival

conjunctiva.

ese

can

epithelium

Melanocytes

result

in

are

also

conjunctival

pig-

30

mentation

blood

or

vessels,

CLINICAL

The

normal

vessels.

seen

Palpebral

blood

amount

bright

that

vessels,

conjunctiva

ow

of

in

an

at

is

The

right

is

clear

individual

surface

uorescein

color.

run

in

conjunctival

conjunctiva

pink

Within

the

and

pooling

examined

blood

angles

is

and

as

might

might

smooth

be

by

everting

network

the

lid

a

the

is

ne

be

as

evident

vessel

to

stroma

are

Examination

displays

vessel

not

conjunctival

ner ves.

COMMENT: Biomicroscopic

The

palpebral

lymphatic

bulbar

The

nication.

small

melanoma.

network

seen

the

in

cornea,

the

eyelids

evident,

under

and

normal

and

and

of

blood

high

mag-

thus

eye.

should

arteries

a

The

appear

can

be

margins.

conjunctiva

Plica

e

plica

located

the

Semilunaris

at

semilunaris

the

medial

nictitating

lium

is

stroma

8

to

is

10

is

a

membrane

cells

highly

crescent-shaped

canthus

thick

(Fig.

seen

and

in

4.6).

lower

contains

vascularized,

It

fold

might

of

be

conjunctiva

a

remnant

vertebrates.

numerous

containing

e

goblet

smooth

of

epithe-

cells.

muscle

e

bers

31

and

Fig.

4.5

Three

partitions

of

the

adipose

tissue.

Because

there

is

no

deep

fornix

at

the

medial

conjuncti va.

side as there is at the lateral side, the evident function of the plica is

to allow full lateral movement of the eye without tissue stretching.

muscles,

with

ent

providing

movement

superiorly,

of

coordination

the

globe

inferiorly,

and

and

of

conjunctival

lids.

laterally,

e

movement

fornices

easing

are

movement

pres-

of

Caruncle

the e

globe

without

creating

undue

stretching

of

the

conjunctiva.

mound

semilunaris

fornix

extends

posterior

to

the

equator

of

the

globe.

the

posterior

eyelid

margin,

the

average

upper

is

tissue

called

that

the

overlies

caruncle

the

medial

(see

Fig.

edge

4.6).

of

e

the

plica

caruncle

is

Measured similar

from

of

e

and

to

conjunctiva

in

that

it

contains

nonkeratinized

epithe-

lower lium and accessor y lacrimal glands, but it also has skin elements:

conjunctival

fornix

depths

are

15.6

mm

and

10.9

mm,

respec-

31

hair

follicles

and

sebaceous

and

sweat

glands.

32

e

sebaceous

29

tively ;

these

depths

decrease

with

age. glands

are

a

likely

source

for

Plica

the

semilunaris

Caruncle

Fig.

4.6

Structures

located

in

the

left

medial

canthus.

occasional

accumulation

of

CHAPTER

58

matter

the

in

the

caruncle

medial

is

e

palpebral

palpebral

arcades

lower

lids.

bar

e

fornices

conjunctiva,

junctival

conjunctival

ese

arteries

eye.

e

branch

plexus

of

anastomose

formed

blood

Limbus

function

by

supply

posterior

supplied

then

a

its

the

conjunctiva

are

which

forming

arteries.

from

palpebral

arcades,

healthy

receives

Vessels

the

the

and

of

Vessels

conjunctiva

supply

of

Conjunctiva,

understood.

Blood

arcades.

peripheral

Sclera,

canthus

poorly

Conjunctival

4

in

by

and

vessels,

the

the

branches

both

the

posterior

the

the

and

from

enter

plexus

from

the

of

upper

branches

again

with

from

network

of

the

bul-

con-

anterior

anterior

cili-

ar y arteries. Conjunctival veins parallel the arteries but are more

Fig.

numerous.

ey

drain

into

the

palpebral

and

ophthalmic

A CLINICAL

Conjunctivitis

pterygium

is

any

inammation

of

the

conjunctiva

and

can

be

caused

by

is

of

is

a

usually

brovascular

factors.

Among

the

common

causative

agents

are

bacterial

or

overgrowth

allergic

reaction.

In

inammatory

conditions,

uids

often

As

with

a

of

bulbar

pinguecula,

conjunctiva

a

onto

pterygium

the

cornea

occurs

or

9-o’clock

position

within

the

interpalpebral

area

(Fig.

4.8).

in

The

the

trian-

viral gular

and

progressive.

a 3-o’clock

invasion

Pinguecula.

COMMENT: Conjunctivitis and

variety

4.7

veins.

pterygium

may

be

gray

in

appearance

with

an

extensive

network

of

blood

accumuvessels evident. The apex of the pterygium invades the cornea. This leading edge

late

in

the

loose

stromal

tissue

of

the

conjunctiva.

This

conjunctival

edema

is is

called

chemosis.

Dilation

and

engorgement

of

the

conjunctival

blood

composed

cells. also

occur

with

inammation

and

irritation.

This

vascular

change

is

of

a

zone

of

limbal

epithelial

tissue

known

A

zone

of

cells

follows

the

apex,

migrates

34

injection.

Both

chemosis

and

injection

are

present

to

varying

in

diseases

and

irritation

of

the

conjunctiva.

In

viral

altered

conjunctivitis,

the

basal

corneal

stem

basement

and

dissolves

Bowman

36

layer.

The

apex

is

the

only

site

of

rm

deattachment

grees

from

along

as membrane,

conjunctival

arising

vessels

to

the

corneal

surface.

Fibrovascular

tissue

with

the

same

abnormal

the 36–38

characteristics preauricular

lymph

node

often

is

prominent

on

the

involved

seen

in

pingueculae

underlies

the

epithelium

of

a

pterygium.

side. Anomalous

elastic

material

is

formed

and

cytokines,

such

as

interleukin,

tumor

39

necrosis

Conjunctival

conjunctival

lymphatic

and

vascular

endothelial

growth

factor

are

increased.

Pingueculae and pterygia show many of the same connective tissue changes but are

Lymphatics

different

e

factor,

vessels

are

arranged

in

diseases.

If

mutational

changes

occur

in

the

limbal

epithelium

at

the

cor-

supercial 38

neal edge of a pinguecula, it may become a pterygium.

and

deep

into

the

networks

within

the

submucosa.

ese

vessels

Exposure to irritants, such

drain as wind and dust, might initiate hyperplasia and be a precursor of both these degen-

lymphatic

vessels

of

the

eyelids.

ose

from

the

lateral erative changes. Molecular damage produced by chronic solar radiation, particularly

aspect

empty

into

the

preauricular

parotid

lymph

node,

and high-energy ultraviolet rays, is the primary causal factor in pterygium, with irritants

those

from

the

medial

aspect

empty

into

the

submandibular

39 40

being predisposing factors.

Biochemical studies have shown that oxidative stress

33

lymph

node

(see

Fig.

12.18).

can result in biochemical cellular changes that cause cellular proliferation, vascular-

41–43

ization, and the adhesion to the corneal surface that occurs in pterygium.

Conjunctival

Innervation Pingueculae

Sensor y

inner vation

of

the

bulbar

conjunctiva

is

through

moved:

long

ciliar y

ner ves.

Sensor y

inner vation

of

the

superior

(1)

when

conjunctiva

branches

of

palpebral

conjunctiva

infraorbital

tion

is

the

is

CLINICAL

ophthalmic

branch

carried

provided

by

of

is

by

ner ve.

provided

the

of

the

frontal

Inner vation

by

maxillar y

branches

the

the

ner ve.

and

of

lacrimal

All

trigeminal

COMMENT: Pingueculae

and

lacrimal

the

ner ve

sensor y

are

the

treated

apex

unless

approaches

inamed.

the

visual

Pterygia

axis,

inferior

and

the

informa-

cult

induced,

the

or

altered

(3)

for

cells

cosmetic

appear

concerns.

as

normal

oval

sal

and

layers,

change

is

may

vary

yellowish

whereas

considerably

(Fig.

the

hyalinization,

4.7).

epithelial

which

in

Two

size

and

can

with

either

to

only

irritants

be

discerned

condition

and

prescribed,

sun

as

histologically.

should

be

exposure,

well

as

advised

and

articial

of

Thus

the

pterygia

layers

occurs

remain

in

a

changes

but

unchanged.

zone

just

usually

occur

below

The

the

in

the

rst

are

ultraviolet-ltering

tears

and

ocular

round

submucosal

This

zone contains degenerating collagen and a granular material that probably results

34 35

from the breakdown of connective tissue components.

change

bers.

in

the

development

Precursors

thesized

elastic

of

elastic

bers

are

of

a

pinguecula

bers

found

and

is

the

abnormally

beneath

the

The second submucosal

formation

immature

zone

of

of

abnormal

forms

of

hyalinization.

elastic

newly

These

syn-

bers

degenerate, and elastic myobrils are greatly reduced, which prevents normal as-

34 35

sembly of elastic bers.

Fibroblasts in these regions show extensive alteration.

Fig.

4.8

of

re-

corneal

removal

the

is

dif-

abnormal

Pterygium.

recur.

these

protective

lubricants

submuco-

epithelium.

surgically

and

often

relationship

Pterygia

appearance

histological

are

signicant

Complete

cornea,

val tissue in the interpalpebral area, usually at the 3-o’clock or 9-o’clock position.

or

if

37

cells

be

ner ve.

is

because

A pinguecula consists of an opaque, slightly elevated mass of modied conjuncti-

Pingueculae

(2)

palastigmatism

pebral

rarely

the

as

Patients

conditions

lenses

should

needed.

CHAPTER

Corneal

Sclera,

Conjunctiva,

and

59

Limbus

epithelium

Bowman

Corneal

4

Conjunctival

epithelium

Conjunctival

stroma

layer

stroma Episclera

Scleral Descemet

Corneal

stroma

membrane

endothelium

Trabecular

Fig.

4.9

The

loose

lium.

Limbal

transition. The

connective

Episcleral

tissue

vessels

cut

of

in

cornea

the

is

to

the

conjunctival

cross

section

are

left,

and

stroma

outer

the

is

to

the

lies

conjunctiva

inner

to

the

dense

and

sclera

thickened

connective

circumferentially,

are

to

the

conjunctival

tissue

forming

of

the

an

meshwork

right.

epithe-

sclera.

annulus.

is

ring

structure

LIMBUS 46

is

e

limbus,

located

approximately

of

the

cornea.

junction

of

external

1.5

to

e

the

2

corneoscleral

mm

radius

cornea

scleral

at

and

wide

of

encircles

cur vature

sclera,

sulcus.

that

abruptly

creating

Internally

at

junction,

a

the

a

band

peripher y

changes

narrow

this

is

at

this

furrow,

juncture,

the

there

is

a

postulated

to

Descemet

and

the

the

help

maintain

membrane

posterior

connective

out

furrow,

the

appearance

canal

of

humor.

and

Schlemm,

ese

a

plane

terior

globe

and

cornea

(Fig.

4.9).

epithelium

lium,

larly

(2)

is

the

into

ver y

the

meshwork,

posterior

(4)

zone

the

limbal

area

ver y

thicker

corneal

to

(3)

wrap

Bowman

of

and

regular

of

layer

and

consists

layer

and

e

surface

the

the

at

correct

the

corneal

anterior

portion

anterior

limbal

becomes

sheets

boundar y,

interlaced

of

47

cur vature.

the

with

trabecular

meshwork. e corneal endothelium continues into the anterior

chamber

angle

trabecular

as

the

endothelial

e

covering

of

the

sheets

of

the

49

meshwork.

conjunctival

stroma

begins

in

the

limbus

and

has

no

counterpart in the cornea (see Fig. 4.9). is stromal tissue forms

mounds that project toward the surface epithelium at the limbus,

pos-

others

of

giving

an

undulating

conjunctival

these

ridges,

margin.

lium

a

the

called

Papillae

wavy

T enon

e

the

appearance,

is

basal

papillae,

give

capsule

episclera

appearance

stroma.

lies

inner

which

inner

inner

T enon

the

to

of

are

aspect

although

just

to

to

layer

also

of

the

anterior

the

found

the

capsule.

near

remains

conjunctival

Both

begin

of

eyelid

epithe-

smooth.

stroma,

in

the

follows

the

conjunctival

surface

the

surface

epithelium

the

and

limbus

terminate

corneal

epithe-

irregu-

endothelial

Descemet

and

layers

the

strands

the

spur.

cornea

Some

the

of

scleral

the

becomes

the

the

6

squamous

corneal

around

and

aqueous

conjunctival

stroma

the

the

4.2).

the

sclera.

columnar

scooped-

limbus

Fig.

to

edge

and

the

the

between

cornea

stroma,

discontinuous

(see

the

(1)

of

Bowman

perpendicular

the

regular

scleral

of

of

a

meshwork

in Chapter

boundar y

transitional

limbus:

becomes

discussed

has

drainage

membrane

through

between

for

termination

plane

which

trabecular

route

anterior

the

the

arranged

becular

a

continue

the

becomes

is

and

In

are

sulcus,

the

major

Descemet

passing

limbus

conjunctiva

the

of

boundar y

e

the

connecting

termination

scleral

contains

the

structures

Histologically,

of

internal

tapers

nonbanded

tissue

48

larger

the

of

sheet

the

tra-

membrane

terminate at the anterior border, and (5) the conjunctival stroma,

T enon

capsule,

Limbal

e

and

episclera,

Histological

epithelium

begin

within

the

limbal

Features

increases

at

the

limbus

from

a

16

thick

may

to

a

be

evident

layer

present

in

the

individuals.

e

neal

the

to

in

15

the

limbal

bundles

in

transparent

demarcation

the

the

be

the

(Fig.

layer,

tapers

and

and

sclera.

and

is

merges

identied.

cells

Melanocytes

in

may

be

darker-skinned

terminates.

from

change

e

ve

45

pigmentation

the

random

into

layer

44

4.10).

especially

transition

irregular

cornea

can

thick

basal

layer

contains

to

cells

conjunctiva,

Bowman

limbus

lamellae

lagen

10

area.

the

is

ver y

gradual

opaque

scleral

regular

organization

such

sclera,

brils

of

col-

that,

no

extend

cor-

line

as

of

further

anteriorly on the external than on the internal side of the limbus

(see

er y,

Fig.

a

4.9).

distinct

Within

group

the

of

limbal

collagen

stroma

brils

at

has

the

corneal

been

periph-

identied

that

Fig.

neal

4.10

Light

micrograph

epithelium

(right

side

of

(left

side

image).

of

showing

image)

to

the

transition

conjunctival

from

cor -

epithelium

CHAPTER

60

4

Sclera,

Conjunctiva,

and

Limbus

but do not continue into the cornea. T enon capsule, the episclera,

REFERENCES

50

and

the

conjunctival

stroma

fuse

in

the

anterior

limbal

area.

1.

Hogan

MJ,

Weddell

Limbal

Blood

Vessels

and

ders;

Capillar y

loops

from

Alvarado

JE,

eds.

JA.

e

Histolog y

of

Sclera.

the

In:

Hogan

Human

Eye.

MJ,

Alvarado

Philadelphia:

JA,

Saun-

Lymphatics

conjunctival

and

episcleral

vessels

1971:183–201.

form 2.

Harper

AR,

Summers

JA.

e

dynamic

sclera:

extracellular

matrix

networks in the limbus, which surround the cornea and provide remodeling

nourishment

to

the

avascular

corneal

tissue.

Limbal

veins

blood

the

from

radial

the

anterior

episcleral

veins,

conjunctival

which

then

veins

empty

and

into

drain

the

normal

ocular

growth

and

myopia

development.

colExp

lect

in

into

3.

anterior

Eye

Rada

Res.

Res.

JA,

2015;133:100–111.

Shelton

S,

Norton

T T.

e

sclera

and

myopia.

Exp

Eye

2006;82(2):185–200.

51

ciliar y

not

veins.

enter

Lymphatic

the

channels

located

in

the

limbal

area

do

4.

Komai

lagen

cornea.

Sci.

Palisades

of

5.

Vogt

Y ,

Ushiki

brils

in

T.

the

e

three-dimensional

human

cornea

and

organization

sclera.

Inv

of

col-

Ophthalmol

Vis

1991;32:2244.

ale

SEM

A,

Tillmann

and

B.

e

collagen

immunohistochemical

architecture

studies.

Ann

of

the

Anat.

sclera—

1993;175:215.

e palisades of V ogt are radial projections of brovascular tissue 6.

in

a

spokelike

fashion

around

the

corneal

periphery.

On

Marshall

GE.

Human

scleral

elastic

system:

an

immunoelectron

biomimicroscopic

study.

Br

J

Ophthalmol.

1995;79:57.

croscopy, these projections appear as thin, gray pegs approximately 7.

Alexander

RA,

Garner

A.

Elastic

and

precursor

bres

in

the

nor-

52

0.04 mm wide and 0.36 mm long

and are more prominent in the mal

human

eye.

Exp

Eye

Res.

1983;36:305.

superior and inferior limbus. e surface of the limbal area where 8.

the

palisades

palisades

senting

of

V ogt

includes

nerves,

Langerhans

melanocytes

arise

cells,

safeguard

remains

blood

at.

vessels,

melanocytes,

against

e

area

containing

lymphatics,

and

ultraviolet

limbal

antigen

stem

radiation

the

pre-

cells.

and

9.

e

the

con-

superiorly

and

52–54

limbal

stem

cells

are

located

mainly

and

thus

are

protected

by

the

eyelids.

e

stem

been

described

as

cords

of

cells

that

run

from

e

circulation

limbus).

Prentice

Eye.

Award

treatment

of

uid

at

the

limbus

(ow

and

dif-

1989;3:114.

Lecture

strategies

2010:

for

a

case

myopia.

for

periph-

Optomet

Vis

Sci.

Cooper

J,

O

myopic

Connor

B,

progression

multifocal

Watanabe

control

contact

lens.

R,

with

Eye

etal.

a

Case

unique

Cont

Len.

series

analysis

extended

depth

of

2018;44:e16–e24.

cells 11.

have

EL.

optical

focus

inferiorly

JP .

the

2011;88:1029–1044.

of

e

at

Smith

eral

10.

junctival blood vessel loops are a source of nutrition.

McCulley

fusion

the

Huang

J,

Wen

D,

Wang

Q,

etal.

Ecacy

comparison

of

16

inter-

paliventions

for

myopia

control

in

children:

a

network

meta-analysis.

55–64

sade

peripher y

into

the

limbal

stroma.

e

characteristics Ophthalmolog y.

that

identify

these

cells

as

stem

cells

are:

(1)

the

cell

has

12.

renewal

properties

(i.e.,

aer

cell

division

one

of

the

Met lapally

remains

a

stem

cell);

(2)

the

cell

is

undierentiated

but

has

dierentiation ability ; and (3) the cell is in an arrested state most

53

of

the

time,

but

can

be

stimulated

to

damage.

e

low

13.

mitotic

e

area

surrounding

the

stem

cells

pro-

64

vides

the

environment

necessar y

to

o c ular

growt h

and

CF.

S cleral

myopia.

mechanisms

Pro

Mol

Biol

underly-

Translat

S ci.

McBrien

NA,

Cornell

LM,

Gentle

A.

Structural

and

ultrastructur-

54

divide.

53

acid

Wi lds o et

2015;134:241–248.

al

maintain

the

stem

changes

Inv

ability of the stem cell helps to decrease possibility of deoxyribo-

nucleic

R,

daughter ing

cells

2016;123:697–708.

self-

14.

the

Ophthalmol

McBrien

control

65

to

NA,

of

sclera

Vis

Sci.

Gentle

scleral

in

a

mammalian

model

of

high

myopia.

2001;42:2179.

A.

e

matrix

role

of

biolog y

in

visual

information

myopia.

Curr

Eye

in

the

Res.

cell.

2001;23(5):313.

e

limbal

stem

cells

ser ve

as

a

reser ve

for

corneal

cell

pro15.

liferation

and

a

source

for

corneal

repair

in

disease.

Shen

in

movement

from

the

limbal

area

is

responsible

L,

Y ou

QS,

Xu

X,

etal.

Scleral

and

choroidal

thickness

Centripetal

for

the

secondar y

high

axial

myopia.

Retina

(Philadelphia,

Pa).

migra2016;36:1579–1585.

tion

and

replacement

of

corneal

epithelial

basal

cells

in

both 16.

66

normal

cell

replacement

and

wound

War wick

It

is

the

contact

Bowman

layer

64

with

the

facilitates

limbal

the

stroma

distribution

with

of

Eyeball.In:

Eugene

Wol ’s

Anatomy

of

the

Eye

and

speculated Orbit.

that

R.

67

healing.

no

inter vening

growth

factors

17.

and

7th

Albon

J,

ed.

Philadelphia:

Kar watowski

the

non-collagenous

the

human

WS,

Saunders;

Easty

DL,

components

of

1976:30–180.

etal.

the

Age

related

extracellular

changes

matrix

in

of

65

cytokines.

18.

in

the

with CLINICAL

COMMENT: Limbal

Stem

Cell

lamina

Sawaguchi

S,

optic

Yue

cribrosa.

BY ,

ner ve

head

laser-induced

Br

Fukuchi

of

J

Ophthalmol.

T,

etal.

normal

glaucoma—a

2000;84:311.

Collagen

monkey

scanning

eyes

brillar

and

electron

network

monkey

eyes

microscopic

Deciency

study.

Curr

Eye

Res.

1999;18(2):143.

Limbal stem cell deciency may occur because of injury, contact lens use, drug

19.

Albon

J,

Purslow

PP ,

Kar watowski

WS,

etal.

Age

related

com-

68

toxicity,

or

chronic

inammation.

In

limbal

stem

cell

deciency,

the

limbus

is

pliance nonfunctioning,

stem

cell

loss

occurs,

and

conjunctival

tissue

can

invade

of

the

lamina

cribrosa

in

human

eyes.

Br

J

Ophthalmol.

the

2000;84:318. cornea

leading

to

neovascularization

and

corneal

opacity.

Diagnosis

can

be

20. made

by

impression

cytology,

which

shows

goblet

cells

from

the

Albon

J,

Kar watowski

WS,

Aver y

N,

etal.

Changes

in

the

collag-

conjunctival

enous

matrix

of

the

aging

human

lamina

cribrosa.

Br

J

Ophthal-

68

epithelium

on

the

corneal

surface.

Because

a

key

feature

of

limbal

stem

cell

mol. deciency

is

corneal

neovascularization,

the

stem

cells

may

have

a

role

21. maintaining

the

antiangiogenic

state

of

normal

cornea,

and

when

stem

1995;79:368.

in

Axmann

patients are

lost,

neovascularization

ensues.

Treatment

involves

ocular

lubricants,

amniotic

membrane,

cal scraping

of

the

conjunctivalized

corneal

tissue,

use

of

an

S,

Ebneter

A,

Zinkernagel

MS.

Imaging

of

the

sclera

22.

with

scleritis

coherence

Meyer

PA,

and

episcleritis

tomography.

Watson

PG.

Ocul

Low

using

Immunol

dose

anterior

Inam.

uorescein

segment

transplantation

of

limbal

tissue.

conjunctiva

and

episcleral.

Br

J

Ophthalmol.

opti-

2016;24:29–34.

angiography

69

or

in

cells

1987;71:2–10.

of

the

CHAPTER

23.

Kuroda

terior

Y ,

Uji

scleral

tomography

24.

A,

Morooka

S,

inammation

with

multiple

etal.

using

Morphological

swept-source

B-scan

averaging.

features

optical

Br

J

in

an-

46.

Shauly

Y ,

Sci.

Meyer

Pe’ er

E,

J,

Jutley

C.

normals

Tenon’s

and

capsule.

infantile

ultrastructure

esotropia.

Inv

47.

of

in

G,

RP ,

Jiang

RN,

Miller

retinal

B,

etal.

Connective

detachment:

Ophthalmol

Fine

K,

Cell

in

D,

H,

etal.

Eye.

diagnosis

Y ano

&

Shields

CL,

Poselinni

M.

Row ;

J.

Hau

healthy

Ophthalmol.

BS,

S,

Prolif

Brownstein

the

Harper

an

tissue

ultrastructural

of

study.

anatomy

S,

of

Streaming

conjunctiva.

Anat

A,

etal.

Epithelial

stem

cells

of

2017;40:445–461.

S,

white

etal.

Upper

Caucasian

and

eyes:

lower

S,

Lam

of

K,

etal.

melanocytic

JA.

the

a

method

of

Usefulness

of

of

the

a

red

P ,

trophy

as

Jakobiec

the

Li

ZY ,

and

52.

Goldberg

objec-

ed.

Hagerstown,

of

the

caruncle.

Int

eyelid

and

chemosis

BC,

etal.

e

conjunctiva

and

edema.

53.

Md:

55.

Ophthalmol

Iwamoto

bases

T.

correlation

of

Elastodysplasia

ocular

pter ygia

and

and

57.

Surg.

RN,

BW ,

etal.

Elastic

pinguecula.

Inv

elastodys-

ber

components

Vis

corneal

limbal

epithelial

of

MK,

N,

Reid

by

Schultz

matrix

basal

TW .

pingueculae

GS,

etal.

Pter ygia

metalloproteinase

cells.

P53

59.

Sci.

Arch

expressing

Ophthalmol.

expression

pter ygia

and

in

limbal

tumors.

Curr

Dushku

man

the

40.

D,

Y am

JCS,

41.

protein

Kase

S,

basal

invasion

cells.

Curr

Developments

AKH.

Int

of

61.

Res.

Res.

current

Ophthalmol.

Ultraviolet

light

and

that

hu-

1994;13:473.

approaches

diseases.

M,

analysis

and

M,

Dushku

of

Sato

human

I,

etal.

beta-catenin

Jaworski

pter ygium.

CJ,

Mol

etal.

Vis.

Immunolocalisation

in

human

pter ygium.

in

Int

2006;12:55–64.

Br

J

Kau

age,

HC,

Tsai

CC,

JA,

MJ,

Lee

64.

Saunders;

45.

JE,

eds.

DO,

anatomy

and

of

collagen

Sci.

brils

1998;39(7):1125.

High-voltage

Inv

Edelhauser

pathologic

anatomy

AJ.

of

of

the

the

Limbal

B erta

A,

markers

Soc

electron

Ophthalmol

TB,

S,

the

Stem

Cy tol)

of

Y-T,

role

vogt.

Adachi

surface

G,

W ,

etal.

of

age

Vis

e

and

Eye.

limbus.

of

Sci.

corneal

function.

Vogt.

1989;3:101.

Eye.

1989;3:121.

Transact

SZ,

Am

the

adult

Limbal

A.

stem

optical

region

2009;75:54–66.

cell

Ophthalmol.

cornea:

(Cytome-

deciency

2009;24:139–148.

coherence

in

corneal

to-

epithe-

2016;95:e4234.

stem

cells

of

the

corneal

epi-

2000;44(5):415.

Dong

basal

proliferate:

of

applications.

Using

Limbal

Sotozono

epithelial

cells

and

C,

epithelium. Pro

Cheng

to

etal.

Cy tometr y

UV .

Medicine.

A.

Ophthalmol.

limbal

limbus.

human

therapeutic

Jurkunas

Hsieh

assess

Surv

HF ,

structure

palisades

etal.

to

Analy tic

TA,

palisades

B,

Friend

Sci.

etal.

Retin

GE,

cells

Characteristics

Eye

etal.

that

implications

Res.

Existence

can

on

be

of

the

hu-

2001;20(5):639.

of

slow-

preferentially

epithelial

stem

cells.

J,

ro

corneal

RA.

Comparison

epithelium

in

tissue

of

central

culture.

Inv

and

periph-

Ophthalmol

1987;28:1450.

Lauwer yns

o

cell

Ophthalmol.

RA,

Zieske

B,

van

type

in

Wiley

Eye.

JD,

Sci.

den

the

Oord

JJ,

human

De

Vos

cornea.

R,

Inv

etal.

A

new

Ophthalmol

epi-

Vis

Sci.

LA,

Sundarraj

N.

e

multipotential

cells

of

the

1989;3:109.

Bukusoglu

marker

of

G,

Y ankauckas

corneal

MA.

epithelial

Characterization

stem

cells.

Inv

of

a

Ophthalmol

1992;33(1):143.

Wolosin

JM,

stages

Xiong

in

the

X,

Schütte

M,

limbo-corneal

Shanmuganathan

V A,

characteristics

65.

Secker

and

CF ,

etal.

Increased

guanosine,

in

oxidative

human

DNA

pter ygium.

66.

dam-

67.

Eye.

JA.

e

Limbus.

Histolog y

of

the

In:

Hogan

Human

Eye.

MJ,

Alvarado

GA,

of

Daniels

regulation.

Kruse

Foster

the

FE.

JT.

Stem

Stem

cells

Lucarelli

physiolog y.

Shovlin

In:

JP ,

Kaufman

etal.

PL,

Ophthalmic

Alm

A,

eds.

facial

Adler’s

R,

Friend

J.

Inv

Chuephanich

P ,

the

cy :

69.

MJ,

o

maintenance.

of

Philadelphia:

1971:112–182.

Kikkawa

Sci.

Vis

etal.

Stem

epithelium.

cells

Pro

and

dierentia-

Retina

Eye

Res.

T,

limbal

Kulkarni

BB,

epithelial

etal.

cr ypt.

Morphologi-

Br

J

Ophthalmol.

2007;91:514–519.

68.

Alvarado

Weddell

orientation

Corneal

Cell

and

Rev.

epithelial

stem

cells:

deciency

2008;4:159–168.

corneal

epithelial

regeneration.

Eye.

1994;8:170.

8-hydroxydeoxy-

Hogan

Elsevier

2000;19(2):223.

E-

2006;20:826–831.

44.

collagen

Ophthalmol

annulus

etal.

neovascularization. Sem

human

tion

2007;91:1209–1212.

43.

Louis:

1989;57:201.

Ebato

Vis

63.

Microarray

of

St

1982;80:155–171.

E,

Int

to

Cotsarelis

cal

N,

in

Inv

Vis

cornea.

WM,

Azuara-Blanco

potential

2017;37:1073–1081.

ocular

Soc.

J

ocular

limbus.

vimentin-expressing

Eye

and

evidence

10

1983;34(6):1993.

2014;34:383–400.

Osaki

cadherin

H.

an

basal

pter ygium.

John-Ar yankalayil

and

42.

of

Kwok

Ophthalmol.

from

epithelial

Erdöl

treatment

Immunohistochemical

originate

limbal

Hacıoğlu

TW .

and

HS,

thelial

62.

Reid

pter ygia

altered

39.

N,

60.

altered

Eye

KC,

human

and

e

Bron

Tew

Kinoshita

eral

2001;119:695.

altered

limbal

pathogenesis:

1997;16:1179.

38.

A.

H-C,

Dua

Vis

John

invasion

Dushku

cells

N,

Changes

corneas.

Ophthalmol

circulation

Tóth

stimulated

1991;32(5):1573.

Dushku

ed

1982;89(6):531.

Fuchsluger

c ycling

pinguecula.

Ophthalmol

etal.

Schmidt

Bourne

EM.

e

corneal

Cell.

Streeten

in

Lin

P ,

man

1983;90:96.

inhibitors

ME,

normal

MF ,

L,

thelium.

Reconstruc

Y ,

Circumcorneal

Inv

normal

c ytometric

Part

Lim

lium

58.

FA,

Takács

tr y

54.

lymphatic

and

Plastic

KM.

limbus.

GO,

Ophthalmol

chroma-

conjunctiva.

PA.

mography

Mendelson

pathologic

Wallace

protease

Meyer

and

2nd

61

Limbus

Application.

keratoconus

Meek

of

3rd

51.

56.

lower

Ophthalmolog y.

37.

Huang

in

Rock

Buskirk

from

lesions

Histolog y.

Tumors

GI,

Waring

Van

conjunctival

2017;139:628e–637e.

36.

SJ,

Ophthalmolog y.

2016;30:1351–1358.

Ocular

Taylor

PS,

50.

1979:310.

postoperative

Austin

49.

2014;132:622–629.

Shields

RH,

human

Binder

Clinical

and

1991;32:2234.

1993;33(3):31.

Shoukath

with

48.

the

endothelium:

Greifner

Carpenter

depth

in

Clin.

35.

Tu

microscopy

Papini

surface.

G,

JAMA

34.

KM,

distribution

Newton

in

1992;24:365.

assessment.

gen

33.

cavity

Res.

Zajicek

fornix

32.

in

Lichtig

1996;245(1):36.

eye

tive

B,

Ludatscher

Revoltella

the

31.

brils

orbital

Rec.

30.

Miller

1992;33:651.

Ophthal

29.

Eye:

2005;46:1948–1956.

the

28.

the

Kakizaki H, T akahashi Y , Nakano T , etal. Anatomy of T enons capsule:

Vis

27.

Meek

of

Conjunctiva,

2003:16.

and

collagen

26.

Science;

2017;101:411–417.

T enons capsule anatomy. Clin Exp Ophthalmol. 2012;40:611–616.

25.

Sclera,

Physiolog y

coherence

Ophthalmol.

4

corneal

palisades

Haagdorens

cell

Cell

of

Y ,

Z

Supiyaphun

Vogt.

M,

Int.

X,

subbasal

deciency :

Stem

e

hypothesis

Ophthalmol

Van

C,

ner ve

Cornea.

Acker

current

Vis

SI,

Sci.

Aravena

plexus

of

corneal

epithelial

1983;24(10):1442.

in

C,

etal.

limbal

Characterization

stem

cell

decien-

2017;36:347–352.

Van

treatment

2016;2016:9798374.

Ger wen

options

V ,

and

etal.

Limbal

emerging

stem

therapies.

5

Uvea

Anterior e

of

middle

three

layer

regions

of

the

(from

eye,

the

front

to

uvea

(uveal

back):

the

tract),

iris,

is

Border

ciliar y

body,

and

e

surface

layer

choroid. e uvea is sometimes called the vascular layer because

condensation

its

to

largest

vessels,

structure,

which

the

supply

choroid,

the

outer

is

composed

retinal

Layer

composed

mainly

of

blood

layers.

be

a

of

separate

mented

of

the

the

iris,

the

stroma.

layer.

melanocytes.

It

In

is

e

anterior

fact,

composed

highly

border

some

do

of

layer,

not

broblasts

branching

is

a

thin

consider

this

and

processes

of

pig-

these

cells inter weave to form a meshwork in which the broblasts are

3,4

on the surface and the melanocytes are located below

(Fig. 5.6).

IRIS e

e

iris

oen

is

center

thin,

to

nation.

the

e

lighting

ies

the

iris

and

to

can

e

is

var y

large

of

0.45

located

the

mm

of

actually

Pupil

pupil

fairly

diameter

0.41

structure

diaphragm

pupil,

diameter

average

from

a

center.

conditions.

conditions

e

circular

with

aperture,

inferior

lit

a

compared

1

ver y

to

9

small

is

12

when

mm,

mm

in

lens,

nasal

its

in

0.75

accumulations

of

layer

may

var y

melanocytes

throughout

forming

elevated

sity

on

brightly

var-

from

with

melanocyte

and

illumination.

mm

iris,

the

freckle-like masses, evident in the anterior border layer. e den-

illumi-

thickness

the

of

e

depending

dim

and

the

retinal

(miotic)

measured

to

system.

slightly

regulates

(mydriatic)

iris

optical

located

size

from

is

anterior

an

thickness

the

are

and

arrangement

contributing

e

anterior

of

factors

border

the

in

meshwork

iris

layer

dier

among

irises

and

color.

is

absent

at

the

oval-shaped

iris

cr ypts. Near the root, extensions of this layer form nger-shaped

iris

processes

that

attach

to

the

trabecular

meshwork

(Fig.

5.7

and Fig. 4.2). e number of these processes varies, but they usu-

ally

do

not

impede

aqueous

outow.

e

anterior

border

layer

1,2

scleral

cular

(Fig.

for

spur.

ridge

5.1).

the

from

thickest

slightly

in

the

collarette

mm

the

the

root

iris

the

the

ridge

is

during

the

and

iris

of

from

jagged

divides

pupil,

to

region

membrane

collarette

encircles

the

1.5

raised

pupillar y

e

the

is

approximately

is

fetal

opment.

which

It

pupillar y

the

ciliar y

the

cir-

which

e

color

ends

at

the

root.

margin

site

devel-

pupillar y

zone,

5.2).

a

attachment

embr yological

into

(Fig.

collarette,

zone,

extends

of

these

Iris

Stroma

e

and

connective

nonpigmented

stance.

cells,

e

Sphincter

tissue

cells,

collagen

pigmented

whereas

the

Muscle

stroma

cells

is

composed

brils,

and

include

nonpigmented

of

pigmented

extensive

ground

melanocytes

cells

are

and

broblasts,

and

sub-

clump

lympho-

3

two

zones

e

of

the

such

oen

diers.

pupillar y

lens

that

and,

the

mination,

margin

in

iris

of

prole,

pupillar y

the

cytes,

root

the

iris

the

iris

margin

(Fig.

lies

5.3).

rests

has

on

a

anterior

truncated

anterior

e

the

root

to

is

its

the

surface

cone

shape

peripheral

thinnest

ter-

part

of

and

macrophages,

broblasts

widely

spaced

meshwork.

cells

and

have

in

the

Clump

are

likely

and

mast

many

are

altered

Although

branching

stroma,

cells

cells.

so

their

large,

melanocytes

processes,

branches

round,

macrophages

the

do

darkly

that

are

cells

not

are

form

a

pigmented

scavengers

of

the iris and joins the iris to the anterior aspect of the ciliar y body

(Fig.

5.4).

anterior

ous

e

and

humor

with

no

blunt

ciliary

in

divides

to

ow

the

anterior

chambers,

from

the

and

segment

the

posterior

pupil

into

the

of

the

globe

allows

the

anterior

into

aque-

chamber

resistance.

CLINICAL

With

iris

posterior

COMMENT: Blunt

trauma

body

damaged

to

creating

blood

the

a

eye

or

condition

vessels

and

Trauma

head,

the

called

nerves.

thin

iris

root

iridodialysis

Blood

may

may

(Fig.

tear

5.5),

away

which

hemorrhage

into

from

can

the

result

either

the

anterior or the posterior chamber, or both, and nerve damage may cause sector

paralysis

of

the

iris

muscles.

Histological

Features

e

divided

iris

layer,

and

62

can

(2)

be

stroma

dilator

and

muscle,

of

into

the

four

sphincter

and

(4)

Iris

layers:

muscle,

posterior

(1)

(3)

the

anterior

anterior

epithelium.

border

epithelium

Fig.

5.1

Davis,

Iris

collarette,

Pacic

University

trabeculae,

and

Family Vision

crypts.

Center,

(Courtesy

Forest

Grove,

T aylor

Ore.)

CHAPTER

Fig. 5.4

Fig.

The

nal

5.2

cornea,

of

terior

by

micrograph

anterior

Schlemm,

and

the

(a)

Light

slight

iris

root

chamber

and

posterior

part

iris

dilation

(b),

of

of

of

the

iris

angle,

the

the

ciliar y

pupil.

portion

body

furrows

The

of

anterior

trabecular

contraction

pupillar y

and

pupil

the

iris

chamber.

meshwork,

are

included.

are

An-

ciliary

of

arterial

circle

the

iris

(d)

are

shown.

The

pupillar y

and

collarette

Light micrograph of anterior segment section. The thinnest

of

the

iris

lie

at

the

junction

of

iris,

the

iris

Remnants

equator

the

and

free

pigment

of

ciliary

root,

the

is

evident

zonular

at

bers

its

are

attachment

seen

to

the

between

the

processes.

ruff

3,5

(e)

and

these

within

the

iris.

Clump

cells

are

usually

located

ciliar y

the

pupillar y

portion

of

the

stroma,

oen

near

the

sphincter

minor

muscle of

the

body.

lens

in portion

63

Uvea

accentuated

and

(c),

ca-

portion

5

t wo

(Fig.

5.8).

e

collagen

brils

of

the

iris

are

arranged

in

por-

radial columns (trabeculae) that are seen as white bers in lighttions.

The

anterior

border

layer

(f)

is

distinct

from

the

loosely

colored arranged

stroma.

the

the

of

stromal

The

iris;

the

chamber

Schlemm

MJ,

posterior

posterior

anterior

tissue

(m),

Alvarado

Philadelphia:

and

JA,

(g). The

(i)

and

latter

angle,

Weddell

Saunders;

anterior

forms

the

ciliar y

sphincter

(j)

(n)

are

Histology

(h)

lies

epithelium

dilator

trabecular

body

JE.

the

muscle

muscle.

meshwork

visible.

of

are

on

canal

Hogan

Human

irises

(see

Fig.

5.1).

e

iris

stroma

is

continuous

the

Eye.

stroma

e

circle

e

to

iris

of

iris

the

of

the

ciliar y

arteries

the

iris,

vessels

pupil

are

body.

branches

located

usually

margin

in

the

follow

(Fig.

a

of

a

circular

ciliar y

radial

5.9).

body

vessel,

near

course

Bundles

of

the

the

from

them

the

stromal

encircle

from

the

vessels

kinking

and

to

anchor

them

compression

in

during

place

the

Iris

body

Sclera

Lens

Periphery

of

root.

root

collagen

and

Cor nea

5.3

iris

the

anterior

segment

of

the

globe.

Fig.

5.5

Iridodialysis

at

the

iris

root

protect

extensive

Conjunctiva

Fig.

major

iris

1971 .)

brils

Ciliar y

with

the

W ithin

(l),

(From

the

in

(arrow).

iris

CHAPTER

64

5

Uvea

3

e

la

n

o

c

y

t

even

s e

the

if

severed

pupil

to

radially.

constrict

in

Contraction

miosis.

e

of

the

muscle

is

sphincter

causes

inner vated

by

the

M

parasympathetic

b

system.

b

la b o r ib F

s

t

s

b

a

CLINICAL

a

COMMENT: Iridectomy

In some cases of glaucoma, an iridectomy is performed to facilitate movement a a

of aqueous from the posterior chamber to the anterior chamber. In this surgical

a

procedure,

a

wedge-shaped,

full-thickness

section

of

tissue

is

removed

from

c

the

iris.

If

the

sphincter

muscle

is

cut

during

this

procedure,

the

ability

of

the

c

muscle

make

c

to

an

usually

contract

opening

not

Anterior

in

not

the

lost.

iris

Iridotomy,

without

a

similar

excising

procedure,

tissue

(Fig.

uses

5.11).

The

a

laser

muscle

to

is

involved.

Iris

Posterior

is

to

Epithelium

the

stroma

and

are

Dilator

two

layers

Muscle

of

epithelium.

e

rst

of

these, the epithelial layer lying nearest to the stroma, is the ante-

rior

Fig.

the

5.6

iris

Anterior

is

layers

covered

branching

by

processes

a

of

of

the

single

which

iris. The

layer

of

anterior

border

broblasts

interconnect.

(a),

layer

the

Branching

of

long,

lial

iris

joined

of

broblasts

form

variably

sized

openings

on

e

by

tight

iris

is

the

layer

of

broblasts

is

a

fairly

dense

and

a

few

broblasts. The

supercial

has

layer

of

been

removed

(b)

to

show

these

cells. The

iris

to

a

number

of

capillaries

(c),

which

may

be

and

of

pigmented

unique

myoepithe-

cuboidal

desmosomes,

epithelium

whereas

of

elongated,

contractile,

the

smooth

basal

muscle

quite

e

ve

muscle

layers

of

bers

dilator

extend

muscle

into

the

bers

stroma,

joined

by

forming

tight

junc-

bro-

(Fig.

5.12).

stroma

e contains

junctions

composed

is

of

tions blasts

is

surface.

aggregation

three melanocytes

which

portion

composed

processes. Beneath

apical

process-

portion

es

epithelium,

cells.

close

dilator

muscle

is

present

from

the

iris

root

to

a

point

in

to

the stroma below the midpoint of the sphincter. e stroma septhe

ogy

surface.

of

the

(From

Human

Hogan

Eye.

MJ,

Alvarado

Philadelphia:

JA,

Weddell

Saunders;

JE.

Histol-

arating

1971 .)

band

the

of

muscle,

sphincter

connective

small

and

dilator

tissue.

projections

muscles

Near

insert

the

into

is

a

particularly

termination

the

stroma

of

or,

the

dense

dilator

more

accu-

6

movement

plete

that

circular

occurs

vessel,

with

the

miosis

minor

and

circle

mydriasis.

of

the

iris,

An

is

incom-

located

in

remnant

of

rately,

into

dilator

the

muscle

sphincter

connects

muscle

through

(Fig.

5.13).

Peripherally,

tendon-like

strands

to

the

mus-

7

the

iris

stroma

embr yological

and

form

e

and

is

tions.

part

posterior

of

the

sphincter

composed

As

its

to

the

development.

name

lies

the

is

are

a

not

fenestrated

barrier.

within

smooth-muscle

implies,

and

capillaries

blood-aqueous

muscle

of

collarette

Iris

the

joined

sphincter

is

a

(see

by

Fig.

tight

circular

5.8)

junc-

muscle,

0.75 to 1 mm wide, encircling the pupil and located in the pupil-

3

lar y

zone

anchored

of

the

rmly

stroma

to

the

(Fig.

5.10).

adjacent

elastic

tissue

just

anterior

to

the

ciliar y

muscle.

Because

the bers are arranged radially, contraction of the dilator muscle

pulls

stroma

cells

cular

the

the

pupillar y

pupil

causing

sympathetic

e

gin

as

portion

toward

mydriasis.

e

the

root,

dilator

is

continues

to

thereby

enlarging

inner vated

by

the

system.

anterior

cuboidal

iris

epithelium

epithelial

cells.

e

anterior

the

iris

pupillar y

epithelium

mar-

con-

4

e

stroma

sphincter

and

retains

muscle

its

is

function

tinues

body

posteriorly

(Fig.

as

the

pigmented

5.14).

Trabecular

Scleral

Iris

Iris

5.7

Gonioscopy

image

showing

iris

processes.

meshwork

spur

process

Ciliary

Fig.

epithelium

body

of

the

ciliar y

CHAPTER

Anterior

Iris

border

Clump

Lens

Light

Posterior

e

Iris

second

posterior

iris

columnar

In

to

pigment

inner,

thin

the

which

a

as

it

the

single

the

ciliar y

by

transver se

covers

into

of

the

are

section

evident

iris

the

of

bet ween

basal

is

and

epithelium

ciliar y

(see

aspect

body

Fig.

of

the

pigmented,

junctions

epithelium

the

stroma

heavily

tight

posterior

body

posterior

to

layer

joined

continues

membrane

lines

posterior

cells

peripher y,

nonpigmented

basement

layer,

of

cells

pupillary

the

des-

begins

as

the

5.14).

this

A

cellular

apex

portion

muscle

e

layer

epithelium,

mosomes.

its

Clump

Epithelium

epithelial

approximately

lose

micrograph

muscle.

anterior

to

ment.

and

apex,

Apical

and

a

of

the

muscle

iris

Posterior

5.8

iris

posterior

microvilli

epithelium

capsule

the

of

epithelium

iris

anterior

result

layer

cell

Anterior

sphincter

65

Uvea

stroma

Sphincter

Fig.

5

showing

the

epithelium.

iris

events

extend

epithelial

during

from

layers

are

positioned

embr yological

both

surfaces,

develop-

and

desmo-

somes join the two apical surfaces. e epithelial cells curl around

from

the

margin,

encircles

Fig.

posterior

forming

the

iris

the

pupil;

to

the

anterior

pigmented

this

surface

pupillar y

normally

has

a

at

ru

the

(or

serrated

pupillar y

frill),

which

appearance

(see

5.10).

chamber.

CLINICAL

COMMENT: Iris

Iris

is

synechia

structure.

anterior

is

can

mor

If

a

and

can

ous

causes

a

will

the

the

is

iris

dramatic

epithelial

from

uveal

a

to

layers,

of

if

a

It

lens

usually

is

in

a

a

are

surface

is

the

head

another

to

anterior

meshwork.

or

a

together.

circulating

and

adherent

the

trabecular

forcefully

that

in

the

iris

Syn-

whiplash-type

Alternatively,

the

aqueous

hu-

synechiae.

portion

of

chamber.

the

trabecular

pressure.

of

The

the

pupillary

Continual

chamber

synechia.

to

increase,

called

iris

meshwork,

A

margin,

production

of

which

bombé.

setting

usually

posterior

iris

aque-

in

the

occurs

turn

This

medication-induced

break

aque-

can

stage

dilation

between

epithelium

on

the

5.15B).

at

the

peripheral

anterior

adhesion

or

to

iris

surface

synechia,

conguration

the

occurs

called

peripheral

the

large

remnants

(Fig.

blow

causing

intraocular

posterior

anterior

posterior

against

of

sharp

a

the

leaving

the

synechia

by

a

in

an

the

iris

endothelium

posterior

forward

increase

In

structures

sticky

the

iris

a

between

posterior

infection

involves

in

bow

break

of

two

surfaces

meshwork.

pressure

result

pressure

surface

corneal

the

peripheral

impeded

lar

a

the

5.15A).

brings

the

the

anterior

the

synechia

generally

becular

as

Synechiae

attachment

synechia,

(Fig.

to

accumulate

the

anterior

An

occur

that

make

will

for

surface

posterior

push

posterior

debris

ous

causes

abnormal

adherent

movement

cells

a

lens

surface

echiae

In

an

iris

synechia,

occupies

a

periphery

anterior

and

synechia.

causing

considerable

an

involves

Aqueous

increase

amount

of

in

the

the

tra-

outow

intraocu-

trabecular

meshwork.

Anterior

in, Fig.

5.9

Optical

coherence

tomography

angiography

radial

iris

blood

(Courtesy Thomas

ter,

Forest

Grove,

vessels.

Nguyen,

Ore.)

The

Pacic

pupil

margin

Universit y

is

on

radial,

Surface

collagenous

columns

or

trabeculae

are

evident

in

show-

lightly ing

Iris

the

Family Vision

pigmented

irises.

icker,

radially

oriented,

branching

left.

Cen-

trabeculae

crypts

encircle

(see

Fig.

depressions

5.1).

Crypts

or

are

openings

located

in

on

the

surface

both

sides

called

of

the

CHAPTER

66

5

Uvea

a

j

j

Fig.

5.10

pigment

cle

of

Pupillary

ruff

the

iris

(b)

in

portion

the

extend

of

pupillary

toward

the

iris. The

margin. The

the

pupil

and

dense

cellular

sphincter

through

anterior

muscle

the

is

border

at c. The

sphincter

layer

arcades

muscle. The

(a)

(d)

terminates

from

sphincter

the

at

the

minor

muscle

and

cir -

iris

epithelium are close to each other at the pupillar y margin. Capillaries, ner ves, melanocytes, and clump

cells (e) are found within and around the muscles. The three to ve layers of dilator muscle (f) gradually

diminish in number until they terminate behind the midportion of the sphincter muscle (arrow), leaving

cuboidal

from

the

the

Its

Alvarado

(Fuchs

dilator

sphincter

nuclei.

collarette

epithelial

cr ypts)

cells

apical

surface

near

is

JE.

the

to

form

form

muscle. The

JA, Weddell

and

(g)

muscle

the

Michel

posterior

root

(h)

of

with

the

(peripheral

epithelium

and

epithelium

contiguous

Histology

anterior

spur

the

Fuchs

(j)

is

formed

apical

Human

crypts).

of

the

spur

(i),

by

surface

Eye.

iris stroma as the volume of the iris changes with iris dilation and

viewed

contraction.

near

of

the

root

ciliar y

during

zone,

folds,

result

pupillar y

evident

from

dilation

tissue

(Fig.

on

the

moving

5.16).

anterior

toward

of

columnar

Iris

with

Spurlike

anteriorly

cells

with

epithelium.

Saunders;

posterior

the

margin.

extend

anterior

Posterior

e

contraction

tall

Philadelphia:

ey allow the aqueous quick exit and entrance into spaces in the

Circular

pupillar y

which

extensions

blend

basally

(From

with

located

Hogan

MJ,

1971 .)

Surface

surface

of

the

magnication,

pupil.

to

Radial

iris

small

is

fairly

circular

contraction

smooth,

furrows

furrows

(of

but

are

when

evident

Schwalbe)

are

surface

located

the

(of Schwalbe) run throughout the ciliar y zone and continue into

iris

in

the

pupillar y

zone,

and

the

deeper structural furrows

the ciliar y body as the valleys between the ciliar y processes. Also

CHAPTER

Fig.

found

5.11

on

similar

to

the

CLINICAL

of

causing

the

seen

the

on

surface

the

anterior

COMMENT:

pigmentary

opening

posterior

those

topography

In

Iridotomy

dispersion

posterior

seen

are

anterior

and

iris

to

rub

the

posterior

circular

the

along

iris

the

iris

bowed

zonules.

5.17

to

be

shed

from

iris

surface

Syndrome

posteriorly

This

and

toward

causes

the

pigment

lens

gran-

dispersed

into

the

The

pigment

can

be

deposited

on

the

iris,

lens,

or

corneal

5.13

at

5.18A)

outow.

or

in

the

Signicant

trabecular

pigment

meshwork,

loss

will

be

where

evident

it

might

on

the

micrograph

midpoint

of

the

showing

sphincter

muscle.

muscle

Small

end-

projections

endothelium

insert

(Fig.

Light

anterior

ing

chamber.

dilator

the

Fig.

ules

the

folds

shows

surfaces.

Dispersion

is

Uvea

(arrow).

contraction

surface. Fig.

posterior

Pigmentary

syndrome,

superiorly

67

5

compromise

transillumination

into

the

stroma

and

sphincter

muscle

(red

arrow).

aqueous

of

the

iris

8

9

melanocytes and the area they occupy.

when the red fundus reex shows through in the depigmented areas ( Fig. 5.18B).

e type of melanin pres-

ent and the arrangement of the connective tissue components can

also

Iris

ere

are

aect

to

a

number

arrangement

and

of

density

factors

of

that

determine

connective

tissue

eye

color:

components

in

iris

the

sky

the

by

anterior border layer and stroma, the number of melanocytes, and

8

is

the

nents.

tion,

Studies

and

irises

of

which

various

melanocyte

colors

and

counts

from

have

dierent

been

races

10

the

be

number

of

determined

melanocytes

by

the

is

fairly

number

of

have

between

shown

An

the

iris

wavelength

arrangement

Other

and

appears

reection

iris

and

colors

blue

seen

density

are

for

the

of

results

of

caused

the

by

from

connective

the

amount

that

which

depends

anterior

border

on

the

layer

pigment

density

melanocytes.

If

the

Color

granules

seems

within

to

the

vety,

and

whereas

the

color

in

a

lighter

ranges

iris,

from

the

grays

collagen

to

blues

Ciliar y

body

Posterior

chamber

A

B

of

the

ciliar y

portion

of

the

iris. The

dilator

muscle

is

evident

as

a

pink

band (arrow) anterior to pigmented epithelium. B, Light micrograph of the epithelial iris layers. Strands

of

the

dilator

muscle

(arrow)

iris

greens

Sclera

micrograph

light

is

the

compo-

absorp-

stromal

heavily

trabeculae

to

Anterior

Light

tissue

of

the

caused

pig-

mented, the anterior surface appears brown and smooth, even vel-

chamber

A,

that

scatter

within

epithelium

5.12

contributing

reason

light

Conjunctival

Fig.

light

same

11

constant.

melanin

done

blue;

transmission

12

color.

9

the size and density of melanin granules within the melanocytes.

in

the

9

Color

are

evident

above

the

pigmented

portion

of

anterior

iris

epithelium.

are

evident

depending

on

CHAPTER

68

5

Uvea

Anterior

iris

Posterior

Inner,

body

body

5.14

The

epithelium.

ciliar y

the

density

area

of

of

pigment

body

and

hyperpigmentation,

anterior

The

epithelium

pigmented

transitions

iris

epithelium

into

the

outer

transitions

epithelium

nonpigmented

pigmented

the

the

Iris

ciliary

epithelium

pigmented

into

ciliary

inner,

ciliary

body

nonpigmented

epithelium.

collagen.

an

iris

posterior

iris

epithelium

Outer,

Fig.

epithelium

A

freckle

accumulation

of

or

a

nevus

is

melanocytes,

an

Functions

of

and e iris acts as a diaphragm to regulate the amount of light entering

frequently is seen in the anterior border layer (Fig. 5.19). In all colthe eye. e two iris muscles are innervated separately: the sphincored irises, the two epithelial layers are heavily pigmented. Only in ter muscle, innervated by the parasympathetic system, is responsithe albino iris do the epithelial layers lack pigment. ble for constriction of the pupil, and the dilator muscle, innervated

by the sympathetic system causes pupillary enlargement.

CLINICAL

COMMENT: Heterochromia

Heterochromia

of

the

iris

is

a

condition

in

which

one

iris

differs

in

color

from

CILIARY the

be

other

or

portions

congenital

or

a

of

sign

one

of

iris

differ

uveal

in

color

from

inammation.

If

the

rest

of

congenital,

a

the

iris.

This

disruption

of

the

If sympathetic

innervation

may

be

suspected.

A

history

regarding

iris

the

be

iris

were

removed,

and

the

ciliar y

body

viewed

from

the

coloration

front should

BODY

can

of

the

eye,

it

would

be

seen

as

a

ring-shaped

structure.

Its

elicited.

width

A

is

approximately

5.9

mm

on

the

nasal

B

Fig.

5.15

residual

Synechiae.

iris

pigment

A,

on

Posterior

the

synechiae

anterior

surface

associated

of

the

lens

with

after

uveitis.

breaking

B,

a

A

different

posterior

patient

synechiae.

with

side

and

6.7

mm

CHAPTER

Fig.

5.16

Brittany

Grove,

Contraction

Hertz,

folds

Pacic

in

the

University

peripheral

Family

iris.

Vision

5

69

Uvea

(Courtesy

Center,

Forest

Ore.)

4

on

the

which

the

temporal

anterior

that

extend

ciliar y

has

One

extends

tions

of

the

at

ciliar y

into

body

anteriorly.

root

side.

terminates

serrata,

contains

posterior

triangular

corner

from

base

posterior

ora

body

the

a

e

the

the

of

base

the

lies

approximate

border

both

the

of

In

at

the

at,

folds

of

or

the

and

body,

whereas

processes

section,

which

scleral

of

anterior

ciliar y

sagittal

base

center

the

fairly

numerous

chamber.

shape,

the

area

appears

is

spur,

base,

the

located

the

and

posterior

iris

por-

cham-

bers. e outer side of the triangle lies against the sclera, and the

inner side lines the posterior chamber and a small portion of the

vitreous

cavity

Partitions

e

ciliary

(Fig.

of

the

body

5.20).

e

Ciliary

can

be

apex

is

located

at

the

ora

serrata.

Body

divided

into

two

parts:

the

pars

plicata

(corona ciliaris) and the pars plana (orbicularis ciliaris). e pars

plicata

is

the

wider,

anterior

portion

containing

the

ciliar y

proFig. 5.17

cesses

(see

Fig.

5.20).

Approximately

70

to

80

ciliary

Surfaces

and

layers

of

the

iris.

Beginning

at

the

upper

processes left

and

proceeding

clockwise,

the

iris

cross-section

shows

the

extend into the posterior chamber, and the regions between them

are

called

valleys

of

Kuhnt.

A

ciliary

process

measures

approxi-

mately 2 mm in length, 0.5 mm in width, and 1 mm in height, but

pupillar y

(A)

a

iris

brown

and

ciliar y

with

contraction

its

portions

dense,

furrows

are

(B),

matted

shown

and

the

anterior

(arrows)

in

surface

border

the

view

layer.

ciliar y

shows

Circular

portion

of

13

there

are

e

signicant

pars

variations

plana

is

the

in

all

atter

measurements.

region

of

the

the

ciliar y

body.

It

extends from the posterior pars plicata to the ora serrata, which

iris.

in the

the

transition

between

ciliar y

body

and

retina.

e

ora

cr ypts

pupillar y

root. The

surface

is

Fuchs

and

pigment

shows

a

(c)

are

ciliar y

ruff

less

is

seen

at

portion

seen

dense

at

either

and

the

side

the

peripherally

pupillar y

anterior

of

border

edge

layer

collarette

near

(d). The

and

the

iris

blue

iris

more

promi-

ser-

nent

trabeculae. The

iris

vessels

are

shown

beginning

at

the

major

rata has a serrated pattern, the for ward-pointing apices of which arterial

are

called

teeth

or

dentate

processes.

e

dentate

processes

and

elongations

of

retinal

tissue

into

the

region

of

the

pars

rounded

portions

that

lie

between

the

dentate

oral

processes

bays

Some

of

zonule

(Fig.

of

the

between

ing

these

pars

bers

the

membrane

of

course

insert

region

ciliar y

veins

body

is

extend

toward

from

into

and

valleys

the

travel

processes.

the

the

the

body

to

internal

limiting

for ward

through

Some

of

ciliar y

attach

pars

to

the

plicata

the

membrane

the

valleys

internal

(Fig.

lens.

toward

the

(e).

Radial

pupillar y

minor

arterial

pupil,

forming

the

limit-

5.21B).

e

extends

for-

demonstrates

(g)

and

the

surface

attached

to

the

vitreous

base,

which

of

structural

present

at

k.

radial

the

in

the

the

shows

of

circle

(f),

branches

region.

from

capillar y

of

The

the

arteries

arteries

which

form

branches

arcades. The

arrangement

of

the

Schwalbe

ciliar y

Hogan

Eye.

circular

processes

iris

folds

(From

Human

ciliar y

body

sector

ex-

below

5.21A).

bers

plana

ciliar y

are

it

e

the

incomplete

tend

called

in

plana. the

e

circle

are

the

radial

(j).

Alvarado

Philadelphia:

of

the

pars

JA,

Saunders;

sphincter

muscle

contraction

Circular

portion. The

MJ,

dilator

(h). The

furrows

contraction

plicata

Weddell

of

the

JE.

muscle

posterior

(i)

folds

and

the

also

are

ciliar y

body

Histology

of

is

the

1971 .)

13

ward

approximately

2

mm

over

the

posterior

pars

plana.

Supraciliaris

Histological

Features

of

the

Ciliary

Body

e

(Supraciliary

supraciliaris

is

the

Lamina)

outermost

layer

of

the

ciliary

body,

adja-

e layers of the ciliary body, from outer to inner are: supraciliaris,

cent

ciliary muscle, ciliary stroma, and two layers of ciliary epithelium.

bonlike layers containing pigmented melanocytes, broblasts, and

to

the

sclera.

Its

loose

connective

tissue

is

arranged

in

rib-

CHAPTER

70

5

Uvea

A

B

Fig. 5.18

Pigment dispersion syndrome. A, Pigment deposited on the posterior cornea (Krukenberg

spindle).

layers

of

B,

Retroillumination

the

of

the

midperipheral

iris

showing

defects

in

the

pigmented

epithelial

iris.

collagen bands (Fig. 5.22). e arrangement of these bands allows

terminations

or

“muscle

stars. ”

e

length

of

the

longitudinal

15

the

ciliary

body

to

slide

against

the

sclera

without

detaching

from

muscle

the

accumulation

displacement

of

the

of

uid

ciliary

within

body

its

from

spaces,

the

which

sclera.

may

cause

Damage

to

a

the

3.4

mm

and

is

longer

with

increased

axial

length.

Inner to the longitudinal muscle bers, the radial bers form

or stretching the tissue. e arrangement of the supraciliaris allows

for

is

wider, shorter interdigitating Vs that originate at the scleral spur

and

insert

into

the

muscular

elastic

connective

tissue

near

the

from

the

14

base

layer caused by trauma may result in a ciliary body detachment.

of

the

ciliar y

longitudinally

Ciliary

e

ciliar y

ented

in

muscle

such

among

is

longitudinal,

Inter weaving

layer,

e

Muscle

occurs

that

the

composed

radial,

between

various

muscle

and

smooth

circular

ber

amounts

bundles.

of

directions

bundles

of

e

muscle

and

connective

bers

(Fig.

from

tissue

longitudinal

ori-

5.23).

layer

are

muscle

to

found

bers

muscle,

sphincter

of

regions

the

oriented

innermost

annular

circle

processes.

type

the

of

radial

of

iris.

the

action.

Fig.

of

the

bers

the

and

muscles

is

a

transition

circular

bers.

muscle,

circular

shows

muscle

layer

ciliar y

ese

5.23

circular

to

of

formed

ciliar y

and

bers

region

is

is

the

muscle

are

located

are

near

relationship

surrounding

anchored

circular

bundles

the

between

the

a

major

these

structures.

in

or

with

same

Both

mus-

7

lie

adjacent

muscle

at

the

to

the

bundle

scleral

supraciliaris

resembles

spur,

a

whereas

and

long

the

parallel

narrow

apex

is

V ,

in

to

the

the

the

sclera.

base

elastic

of

Each

which

network

of

to

choroid.

the

scleral

Tendons

e

spur

from

the

tendon

and

to

of

origin

adjacent

longitudinal

attaches

the

trabecular

ciliar y

muscle

meshwork

muscle

insert

in

bers

sheets.

the

elastic

vous

for

system.

one-third

of

the

choroid

in

the

form

of

to

which

the

Parasympathetic

contraction,

inhibitor y

iris

dilator

muscle

is

attached.

whereas

stimulation

sympathetic

activates

inner vation

the

muscle

likely

has

an

eect.

ante-

Ciliary rior

tissue

e ciliar y muscle is dually inner vated by the autonomic ner-

is

14

the

cular

Stroma

stellate-shaped

e

highly

ciliar y

and

forms

tinuous

ciliar y

is

by

as

It

core

the

the

in

the

ciliar y

iris

root

of

the

plana,

in

is

processes.

it

to

It

is

arteries

are

processes,

con-

and

the

of

iris

posteri-

circular

capillaries

the

layers

is

of

arter y

ciliar y

of

bundles

with

circle

the

circular

posterior

ciliar y

the

continues

arterial

is

stroma

epithelial

continuous

where

stromal

the

the

separates

anterior

5.24).

long

e

ciliar y

major

tissue

and

that

stroma

stroma

the

particularly

of

e

(Fig.

arteries.

connective

muscle

tissue

the

pars

stroma.

the

ciliar y

fenestrated,

each

Anteriorly,

anastomosis

anterior

of

the

connective

thins

in

loose

between

choroidal

near

the

the

muscle.

located

and

lies

with

stroma.

orly

vascularized,

body

the

iris

muscle

formed

and

large

the

and

most

are

13

located

Ciliary

near

the

pigmented

epithelium.

Epithelium

Two layers of epithelium, positioned apex to apex, cover the cili-

Fig.

5.19

Family

Iris

Vision

nevi.

(Courtesy

Center,

Forest

Jade

Grove,

Brunsvold,

Ore.)

Pacic

Universit y

ar y body and line the posterior chamber and part of the vitreous

chamber.

e

two

epithelial

layers

are

positioned

apex

to

apex

CHAPTER

5

71

Uvea

Ciliar y

stroma

Ciliar y

muscle

Supraciliaris

Pigmented

epithelium

Nonpigmented

epithelium

Pars

Pars

Fig. 5.20

plicata

plana

Partitions

and

layer s

of

the

ciliary

body.

21

because

optic

tight

the

of

cup

invagination

(see

Ch.

junctions

apical

between

9).

connect

surfaces

the

layers

of

the

neural

Intercellular

the

provide

and

are

two

a

ectoderm

junctions,

layers.

means

of

important

Gap

the

forming

junctions

cellular

in

in

desmosomes,

the

and

between

communication

formation

of

aque-

ser ve

as

a

diusion

nonpigmented

than

the

activity,

humor

barrier

cells

have

pigmented

with

a

cells

between

a

and

signicant

blood

greater

thus

role

in

a

higher

the

and

number

active

aqueous.

of

e

mitochondria

degree

of

secretion

metabolic

of

aqueous

components.

16–18

ous.

Both epithelial layers contain cellular components char-

e

basal

and

basolateral

aspects

of

the

nonpigmented

19

acteristic

e

is

of

cells

outer

epithelial

pigmented

mosomes

ciliar y

lium

and

and

gap

Fig.

epithelium

is

(Fig.

mented

is

5.14).

A

in

(i.e.,

cuboidal,

5.25).

is

layer

and

with

the

continuous

the

the

retinal

anteriorly

stroma)

joined

outer

by

pigment

iris

epithe-

ciliar y

epithelium

attaches

the

des-

pigmente d

pigmented

stroma.

with

the

anterior

outer

ciliar y

to

are

the

membrane

the

cells

next

cells

with

the

basement

to

one

Anteriorly,

continuous

epithelium

secretion.

the

Posteriorly,

continuous

ciliar y

membrane

involved

junctions.

epithelium

(see

(RPE)

actively

is

the

pig-

have

surface

numerous

area

membrane

nal

covering

limiting

chamber,

with

the

limiting

site

for

extends

of

the

anterior

iris

epithelium

and

basement

membrane

portion

of

basement

posteriorly

Br uch

the

into

zonular

in

providing

posterior

chamber.

nonpigmented

of

the

the

epithelium,

body,

lines

invaginations,

membrane

the

bers

ciliar y

pars

and

of

plana

the

the

and

of

is

the

extensive

basement

the

the

is

retina.

region

bers

an

e

inter-

posterior

continuous

e

the

internal

attachment

vitreous

base.

basement

mem-

with

membrane

of

the

Ciliary

Body

the

e inner

the

limiting

membrane

the

to

membrane

internal

Functions brane

adjacent

invaginations,

of

ciliar y

body

has

various

functions,

including

generation

of

the

accommodation,

production

of

the

aqueous

and

vitreous

com-

choroid.

ponents, and regulation of material allowed in the aqueous, thus e

inner

epithelial

layer

(i.e.,

the

layer

lining

the

posterior

contributing chamber)

in

the

eral

is

pars

walls

joined,

nonpigmented

plana

of

the

near

zonula

and

cells

their

13

16

17

cuboidal

contain

apices,

occludens,

and

which

by

is

composed

cells

in

the

extensive

pars

one

columnar

plicata.

interdigitations

desmosomes,

form

of

site

of

gap

the

e

junctions,

are

and

nicant

e

nonpigmented

with

the

posterior

posteriorly

at

transformation,

metabolically

involved

in

aqueous

barrier.

blood-aqueous

e ability of the eye to change power and bring near objects into

focus

on

the

retina

is

called

accommodation.

It

is

accomplished

19–21

inner

continues

blood

Accommodation

by

anteriorly

the

lat-

and

barrier.

e

to

cells

active

the

ciliar y

iris

ora

epithelium

serrata,

becoming

active

secretion

epithelium

of

neural

aqueous

(see

where

nonpigmented

is

it

retina

continuous

Fig.

(see

epithelial

humor

5.14).

undergoes

Fig.

It

sig-

5.25).

cells

components

are

and

increasing

tudinal

and

bers

of

contraction

closer

by

the

the

to

the

power

the

of

lens,

ciliar y

of

ciliar y

the

the

muscle

circular

decreasing

body.

lens.

is

Contraction

pulls

bers

the

releases

the

draws

diameter

tension

of

on

of

the

choroid

the

the

the

longi-

for ward,

ciliar y

ring

body

formed

zonule

bers

and allows the lens capsule to adopt a more spherical shape. e

lens

thickens,

and

the

anterior

surface

cur ve

increases.

ese

CHAPTER

72

5

Uvea

i

h

a

g

f

e

b e

d

c

B

A

Fig.

ora

5.21

at

inner

(c),

processes

dentate

processes

from

arise

sides

Zonules

ment

the

from

of

the

Radial

ciliar y

the

two

the

columns

lens.

The

Hogan

an

The

of

in

(h)

its

size

and

processes

form

of

a

the

lens

1

and

side

mm

and

are

furrows

(i)

zonules

meet

which

(e)

on

site

on

as

by

attachments

of

radial

the

ciliar y

When

the

ciliar y

muscle

is

relaxed,

the

eye

rest

and

is

used

for

distance

vision.

During

Human

iris

sphincter

also

contracts,

restricting

said

to

decreasing

Ciliar y

spherical

muscle

can

incoming

light

the

shown.

and

form

attach

the

attached

1 .5

apex

to

att ach-

B,

the

lesser

Anterior

columns

(a)

lens. These

of

which

lens

The

iris

furrows

Philadelphia:

by

from

to

to

the

zonules.

circular

of

mm

another

zonules

they

point

to

for ward

capsule.

appearance

one

are

lens

the

Zonular

is

on

capsule.

is

pulled

(g).

Saunders;

(From

1971 .)

COMMENT: Presbyopia

is

and

the

the

loss

of

subject

the

of

ability

to

accommodate.

continuing

research.

In

It

is

a

normal

rhesus

age-related

monkeys,

the

ten-

rays that

related

change

up

and

accommodation,

aberration.

contraction

iris

as

and

Eye.

and

cur ve

the

common

from

the

(f)

to

(e)

from

processes.

crenated

body

for ward

bers

(b). The

Bays

be

don

and

a

plana

(d).

accommo-

is

change

the

(c)

of

folds

Presbyopia

at

a

become

CLINICAL

dation.

have

lens. The

is

they

ciliar y

valleys

peripheral

single

the

the

give

the

pars

project

posteriorly

(d)

cont aining

Histology

a

to

(g)

separated

the

and

serrat a. These

from

process

often

(a)

degeneration

between

equator

of

plicat a

striae

ora

then

att aching

structure

crenated

the

ciliar y

the

att aching

which

of

from

a

or

valleys

valleys,

of

pars

cystoid

ridges

the

from

zonules

(b),

or

mm

shape

surface

power,

1 .5

circular

JE.

Linear

ciliar y

the

exhibits

enter

border,

base

is

Weddell

refractive

to

tentlike

posterior

JA,

the

showing

triangle,

surface

Alvarado

increase

in

to

either

up

equatorial

furrows

a

into

shows

retina

shown.

plana

on

body

the

beginning

att ach

var y

it,

are

ridges

valleys

At

ciliar y

to

pars

plana

processes

zonules

revealing

MJ,

the

ciliar y

the

ora

the

Zonules

form

equatorial

upward,

in

side

the

pars

processes

view

either

of

across

from

of

posterior

dentate

lens.

processes.

on

(f)

anteriorly.

Ciliar y

of

aspect

and

the

the

coming

on

equator

lens.

result

is

dentate

bers

changes

A, The

serrata

conguration

of

attaches

structural

the

ciliary

changes:

muscle

it

to

thickens

the

scleral

with

age

spur

and

shows

becomes

extensive

surrounded

age-

by

a

dense layer of collagen, thus losing its elasticity. This loss of elasticity restricts

23

the trabecular meshwork because some of the longitudinal bers

are

attached

to

trabecular

meshwork

sheets.

is

altered

cong-

muscle

movement

be

component

one

involved,

uration

can

facilitate

aqueous

movement

through

the

angle

structures.

Accommodation

has

been

including

of

hampers

human

changes

accommodation.

presbyopia;

involving

the

A

however,

lens

itself

similar

other

mechanism

changes

(see Ch.

7).

are

The

may

likely

area

and

anterior

width

chamber

and

found

of

the

ciliary

muscle

increase

with

accommodative

demand,

and

these

to 24–26

do

22

cause

a

decrease

in

intraocular

pressure.

Accommodation

not

change

muscle

discussed

further

in

Chapter

7

with

the

onset

of

presbyopia.

This

suggests

is does

not

lose

its

ability

to

contract

in

presbyopia.

that

the

ciliary

CHAPTER

5

73

Uvea

Conjunctiva

Sclera

Supraciliaris

Ciliar y

muscle

Ciliar y

stroma

3

Outer

pigmented

ciliar y

Inner

epithelium

nonpigmented

ciliar y

Fig.

epithelium

5.22

Light

micrograph

of

a

transverse

section

of

the

1 3

ciliary

body

showing

detachment

from

the

sclera

in

region 2

of

the

ciliar y

supraciliaris.

body. The

Zonular

the

remnants

ciliar y

Aqueous

e

body

body

into

the

network

shape

of

the

and

evident

lens

muscle

located

in

in

the

the

occupies

center

posterior

of

most

each

chamber

of

the

2

process.

bet ween

equator.

capillaries

factors

addition,

dense

are

ciliar y

is

Production

ciliar y

signicant

In

The

stroma

the

in

the

stroma

of

within

fenestrated

processes

posterior

and

the

ciliar y

production

the

and

ciliar y

capillaries,

provide

a

large

epithelial

secretion

processes

and

surface

the

layers

of

contains

number

area

are

aqueous.

for

f

a

1

and

secretion

Fig.

chamber.

5.23

Ciliary

body,

components. The

ree

mechanisms

contribute

to

production

and

secretion

but

the

when

an

uneven

distribution

of

molecules

trabecular

exists

collectors

membrane

and

the

molecules

move

from

the

higher

to

the

lower

concentration.

Ultraltration

occurs

as

across

a

semipermeable

membrane

is

augmented

by

an

the

membrane

energy-utilizing

80%

to

90%

of

process.

aqueous

against

Active

a

concentration

secretion

production,

with

the

likely

the

nonpigmented

ciliary

epithelial

cell

gradient

accounts

majority

16

in

in

for

occurring

28

radial

ar y

1

and

diusion

allow

which

between

capillaries

body,

as

and

occurs

stroma.

with

Decreased

medications

blood

that

ow

cause

to

the

result

in

decreased

aqueous

humor

exit

they

the

move

blood

through

through

the

the

walls

stroma

of

the

the

of

ion

movement

through

these

cells

is

have

(b),

two

been

ex-

left

un-

of

the

outside

ciliar y

and

muscle

sectioned

are

shown

meridionally.

In

includes

cells

has

ciliar y

section

Ciliar y

the

muscle.

as

long ,

stars

(f).

3,

dissected

only

muscle

scleral

originate

forms

been

In

section

spur

2,

the

show

the

circular

cili-

of

and

in

the

adjacent

V-shaped

V-shaped

to

innermost

originates

(d)

paired

Arms

the

away

trellises

V-shaped

ciliar y

connective

bundles.

(e)

ten-

that

bundles

Longitu-

terminate

meet

at

wide

angles

(g)

and

formed

terminate

in

the

by

cili-

processes.

distant

V-shaped

ciliar y

in

bundles

the

ciliar y

of

circular

tendon

that

muscle

their

originate

arms

meet

at

ver y

wide

angle

(h).

The

iridic

portion

is

shown

(i),

joining

at

the

cap-

epithelia.

still

points

As

muscle

cells.

(From

Hogan

MJ,

Alvarado

JA,

Weddell

e JE.

model

canal

(d)

30

production.

and

the

longitudinal

shown.

muscle

circular

illaries,

spur

cili-

a

molecules

Schlemm

vasoconstric-

29

can

The

is

epichoroidal

such

tion,

(a),

scleral

the

ar y

ar y

the

muscle

muscle.

muscle

radial

ciliar y

from

the

ciliar y

ciliar y

tissue.

dinal

layer.

movement

and

components

viewed

shows

muscle

don,

in

Ultraltration

its

away,

hydro-

static pressure. Active secretion occurs when molecules are trans-

across

meshwork

(c),

Three

longitudinal

ported

and

dissected

bulk Section

ow

muscle

been

concenseparately,

tration

ciliary

have

across disturbed.

a

the

sclera

Diusion ternal

occurs

and

of

27

aqueous: diusion, ultraltration, and active secretion.

including

cornea

Histology

of

the

Human

Eye.

Philadelphia:

Saunders;

1971 .)

theoretical;

transport mechanisms have been identied but the regulation of

27

those

mechanisms

is

not

31–33

clear.

anterior

e two layers of epithelium are thought to function together as

chamber.

Carbonic

anhydrase,

found

within

the

epithe-

lial layers, regulates bicarbonate transport which, in turn, regulates

a syncytium because of the extensive gap junctions joining the cells

uid

within each layer, as well as the gap junctions between the two lay-

mented ciliary epithelium through ionic pumps, ion channels, and

transport.

ers. Ions enter the basolateral pigmented ciliary epithelium, diuse

cotransporters

through the apical membrane into the extracellular uid, and enter

tion

of

ion

Ions

and

pumps,

exit

the

enter

basolateral

the

channels,

membrane

posterior

and

chamber.

cotransporters

of

the

e

in

nonpig-

coordina-

the

two

epi-

31 34

the

nonpigmented

Active

transport

ciliary

uses

epithelium

metabolic

through

energy

to

gap

transport

junctions.

sodium

ions

thelial

layers,

epithelium

as

that

well

as

facilitate

aquaporins

water

in

the

movement,

nonpigmented

produce

the

ciliary

substance

31 35

into

is

the

anterior

creates

sodium

and

a

chamber

through

concentration

moves

across

the

gradient,

the

nonpigmented

in

which

nonpigmented

uid

epithelium.

follows

epithelium

into

the

the

secreted into the posterior chamber as aqueous humor.

e

lens.

aqueous

e

provides

primary

nutrients

dierence

to

between

the

avascular

blood

plasma

cornea

and

and

aqueous

CHAPTER

74

5

Uvea

Because

active

secretion

is

the

primary

mechanism

for

aqueous

formation, moderate changes in blood pressure have little eect on

27

the rate of formation.

Autonomic nerves located within the ciliary

body can inuence aqueous production by acting on the blood ves-

sels,

dilating

ume

by

them

and

constricting

increasing

the

vessels.

blood

volume

Further

or

decreasing

information

on

the

vol-

eect

of aqueous production on intraocular pressure and drug treatments

that reduce aqueous production will be found in Chapter 6

Blood-Aqueous

e

Barrier

blood-aqueous barrier selectively

stance—aqueous

humor.

e

controls

fenestrated

the

ciliary

secreted

body

sub-

capillaries

permit large molecules to exit the blood. However, the tight zonu-

lar

junctions

of

the

nonpigmented

epithelium

prevent

the

mole-

cules from passing between the cells, forcing them instead to pass

through

the

cell

to

enter

the

posterior

chamber.

One

of

the

sub-

stances thus controlled is protein. e protein content of aqueous

39

humor

easily

not Fig.

5.24

The

major

circle

of

the

iris

is

very

out

pass

of

small

the

into

compared

ciliary

the

with

vessels

posterior

that

of

through

chamber

the

because

16

of

e in

the

concentration

of

ascorbate

and

of

protein.

is

approximately

20

times

higher

in

blood

plasma

Ascorbate

and

is

must

thus

be

actively

supplied

to

transported

both

the

the

tight

aqueous

cornea

into

and

nonpigmented

is

freely

40–42

epithelium.

permeated

by

the

aqueous

the

enters

the

stroma

through

the

surface

humor,

out

of

cr ypts.

which

To

large

molecules

from

leaking

the

iris

blood

aque-

lens

and

altering

the

content

of

the

aqueous

uid,

the

iris

capillaries

is no

fenestrations,

and

their

endothelial

cells

maintain

oxidative

damage.

than

in

e

aqueous,

protein

a

content

consequence

in

of

plasma

the

is

tight

function

barrier.

e

low

concentration

of

protein

in

the

minimal

light

scatter

and

thus

maximum

light

their

zonula

occludens

junctions.

200

COMMENT: Tyndall

Phenomenon

aqueous Clinical

causes

through

juncCLINICAL

tional

the

41–44

barrier

greater

pre-

vessels

important as a free radical scavenger helping to guard these tissues

times

do

junction

than

have

against

pass

but

3

and ous.

of

Ascorbate

vent in

the

iris

readily concentration

Proteins

fenestrations

(arrow).

barrier

is

blood.

examination

of

the

aqueous

with

the

biomicroscope

is

accomplished

by

transmisfocusing a conical beam within the anterior chamber with high magnication in a

sion. e aqueous also carries waste products from the cornea and

lens

and

therefore

has

a

high

concentration

of

lactate,

a

darkened

metabolic

ous,

2.3

μL

of

aqueous

is

produced

per

particles

min-

ducing

36

ute.

Aqueous

higher

rate

31

during

the

day,

follows

the

decreasing

circadian

by

about

rhythm

50%

with

during

the

Cells

amount

and

may

rise

at

night,

particularly

or

in

the

the

for

invisible.

pathway

Tyndall

and

are

position.

is

increase

is

intraocular

pressure

infection.

ciliary

in

36–38

supine

can

is

in

thought

to

occur

because

of

changes

in

episcleral

venous

A

movement

The

of

the

within

out-of-focus

beam,

phenomenon,

the

anterior

in

into

uveoscleral

cells

of

light

making

chamber

the

eye

the

causes

inammatory

the

cornea

beam.

and

In

lens

normal

will

be

aque-

visible

will

the

be

beam

reected

visible

and

within

scattered

the

pro-

aqueous.

can

to

a

zonula

be

indicative

breakdown

conditions

ght

occludens

of

uveal

invading

of

the

which

between

inammation

nonpigmented

blood-aqueous

allow

microbes,

the

immune

causing

barrier.

factors

cells

and

leu-

are.

This

of

material

usually

appears

whitish

(Fig.

5.26),

and

if

there

amount

it

may

settle

in

the

inferior

anterior

chamber,

forming

Although the ultraltration process can be inuenced by changes hypopyon. 16

in intraocular pressure, the eect on the rate of formation is slight.

Inner

nonpigmented

ciliary

epithelium

retina Outer

Retinal

is

a

outow. signicant

Neural

This

and

pres-

accumulation

and

disruption

epithelial

occur

cocytes

sure

watching

be

a

Despite this, intraocular pressure does not decrease by

corresponding

the

while

will

36

night.

a

production

room

beam

in the reected light, but the aqueous will be dark or optically empty. If there are

waste product of the anaerobic glycolysis of the lens and cornea.

Approximately

the

pigmented

ciliary

epithelium

pigment

epithelium Ciliary

muscle

Choroid

Sclera

Fig.

the

5.25

ora

mented

ciliar y

Light

serrata

ciliar y

micrograph

region. The

epithelium

epithelium

of

the

ciliar y

ciliary

body

transitions

transitions

to

neural

to

is

epithelial

at

the

the

retinal

retina.

layer s

right,

and

pigment

in

the

the

par s

retina

is

epithelium.

plana

at

the

The

transitioning

left. The

inner

outer

to

pig-

nonpigmented

an

CHAPTER

5

75

Uvea

Retina

Choroid

Sclera

A

Rod

and

cone

segments

Pigment

Fig.

5.26

Cells

in

the

anterior

chamber.

Melanin epithelium pigment

Bruch

granules

membrane

Trauma

a

tear

involving

or

break

branches

cause

a

at

blow

the

entering

blood

to

iris

from

enter

to

the

root

the

the

head

and

major

anterior

or

an

injury,

result

circle

in

of

chamber

such

damage

the

and

iris.

as

to

whiplash,

the

Such

because

a

of

iris

can

blood

cause

hemorrhage

gravity

Choriocapillaris

vessel

will

will

B

settle

Fig.

inferiorly.

This

accumulation

of

blood

forms

a

hyphema

(Fig.

5.28

A,

Light

the

eye

showing

the

thelium.(×1000).

Histology.

CHOROID

e

choroid

extends

from

the

ora

serrata

to

the

micrograph

of

a

full

thickness

section

through

5.27).

optic

ner ve

and

potential

(B

retina,

from

Baltimore:

space

(the

choroid,

Krause

Williams

&

and

WJ,

Cutts

W ilkins;

suprachoroidal

sclera.

B,

JH.

Pigment

Concise

epi-

T ext

of

1981 .)

space)

between

the

sclera

48

is

to

located

outer

vessels.

of

the

between

retinal

layers

However,

stromal

the

a

sclera

(Fig.

thin

vessel

and

the

5.28).

It

connective

layer.

retina,

providing

consists

tissue

Although

primarily

layer

choroidal

lies

on

nutrients

of

blood

each

thickness

side

varies

and

the

from

both

stroma

the

choroidal

sclera

vessels.

(collagen

(melanocytes)

sclera,

part

of

the

is

bands

(Fig.

layer

and

5.29).

If

suprachoroid

contains

broblasts)

the

will

choroid

adhere

components

and

choroidal

separates

to

the

from

sclera

and

4

greatly

with

age,

gender,

45

var ying

ages,

length,

location

measurement,

when considering a healthy population

subfoveal

choroidal

thickness

46

µm.

of

part

will

is

around

300

tissue

choroid

is

thickest

subfoveally.

ment.

choroid

are:

laris,

allows

e

aqueous

ciliar y

they

and

is

Features

of

composed

of

suprachoroid

Bruch

the

vascular

suprachoroidal

the

to

the

choroid.

e

looseness

of

net

to

space

swell

is

a

without

causing

the

drainage

detach-

layers.

choroidal

From

outer

stroma,

to

inner

choriocapil-

membrane.

arteries

Choroidal

and

and

ner ves

the

space

from

the

carries

pathway

the

posterior

to

long

for

the

posterior

anterior

globe.

Stroma

e choroidal stroma is a pigmented, vascularized, loose connec-

larly

ribbonlike

suprachoroid

6),

tive tissue layer containing melanocytes, broblasts, macrophages,

Lamina

pigmented,

sue—the

Ch.

Choroid

four

lamina,

(see

lymphocytes,

Suprachoroid

in,

attached

47

e

Histological

e

remain

46

and method of study,

of

axial

branching

lamina

or

bands

lamina

of

connective

fusca—lies

outer

tis-

to

rior

around

ciliary

and

the

and

mast

cells.

vessels,

short

Collagen

which

posterior

are

brils

branches

ciliary

are

of

arteries.

arranged

the

long

ese

circu-

poste-

vessels

are

a

Bruch Retinal

membrane pigment

Choriocapillaris

epithelium

Medium

vessels

Stroma Large

vessels

Suprachoroid

Sclera

Fig.

5.27

Hyphema

following

trauma

to

the

eye.

Fig.

5.29

Histology

of

choroidal

layer s.

CHAPTER

76

5

Uvea

Neural

Retinal

retina

pigment

epithelium

Sattler

layer

Haller

layer

Suprachoroid

Fig.

5.30

Optical

coherence

tomography

showing

the

choroidal

vessels.

organized into tiers, those with larger lumina occupying the outer

and decreased choroidal blood ow. Parasympathetic stimulation

layer

causes

(Haller

layer).

medium-sized

to

form

a

ey

vessels

capillary

branch

(Sattler

bed

as

they

layer),

(Figs.

5.30

pass

inward,

which

and

forming

continue

5.31).

e

the

medium

and

49

large

choroidal

vessels

are

not

present

in

the

vasodilation,

resulting

in

increased

choroidal

blood

ow.

branching

peripapillary

area.

CLINICAL

A

choroidal

tation

(Fig.

COMMENT: Choroidal

nevus

5.33).

is

It

a

well

does

Nevus

circumscribed

not

cause

vision

area

of

loss

increased

unless

choroidal

located

near

pigmen-

the

fovea.

V enules join to become veins that gather in a characteristic vortex

Larger

pattern

or

in

more

each

large

quadrant

vortex

of

the

veins

eye

(Fig.

and

5.32).

exit

the

choroid

Choroidal

veins

as

valves.

external

Some

to

the

studies

have

found

choriocapillaris,

lymphatic

which

may

capillary

aid

in

uid

have

a

higher

risk

of

malignant

transformation.

contain

4

no

nevi

four

sacs

just

recircula-

Choriocapillaris

e

specialized

capillary

bed

within

the

choroid

is

called

the cho-

50

tion and immune surveillance;

however, others have been unable

riocapillaris

(lamina

choroidocapillaris).

It

forms

a

single

layer

51

to detect evidence of lymphatic vessels in the choroid.

of

anastomosing,

fenestrated

capillaries

having

wide

lumina

(see

52

e

vous

choroidal

system.

vessels

are

Sympathetic

innervated

stimulation

by

the

causes

autonomic

ner-

vasoconstriction

Fig.

5.31)

with

most

of

the

fenestrations

facing

toward

the

retina.

In each vessel, the lumen is approximately 3 to 4 times that of ordi-

nary

capillaries,

through

the

such

capillary

that

two

abreast,

or

three

whereas

red

in

blood

ordinary

cells

can

pass

capillaries

the

53

cells

usually

course

single

le.

e

cell

membrane

is

reduced

to

a

single layer at the fenestrations, facilitating the movement of mate-

54

rial

through

the

vessel

walls.

Occasional

pericytes,

which

may

5,53

have

a

contractile

function,

are

found

around

the

capillary

wall.

55

Pericytes have the ability to alter local blood ow.

e choriocap-

illaris is densest in the macular area, where it is the sole blood sup-

ply for this small region of the retina. e capillaries are arranged in

lobules, with each lobe being supplied by vessels from Sattler layer.

Fig.

5.31

Drawing

of

choroidal

blood

supply

and

innervation.

The pigment epithelium of the retina (a) is in close contact with Bruch

membrane

collagen

along

(b). The

brils.

the

inner

elastica

The

of

Bruch

choriocapillaris

choroid.

V enules

(d)

membrane

(c)

forms

leave

the

is

an

blue

and

intricate

contains

network

choriocapillaris

to

join

the vortex system (e). The short ciliary artery is shown at (f), before its

branching

(g)

the

choroid

ma

(i). The

to

(h)

form

and

of

choriocapillaris.

suprachoroidea

melanocytes, is at (j).

tology

the

sends

the

Human

ramifying

A

short

branches

(suprachoroid

ciliary

into

lamina),

the

with

nerve

enters

choroidal

its

stro-

star -shaped

(From Hogan MJ, Alvarado JA, Weddell JE. His-

Eye.

Philadelphia:

Saunders;

1971 .)

Fig.

5.32

Vortex

vein

(arrow).

CHAPTER

5

77

Uvea

1

2

3

4

5

Fig.

5.33

Choroidal

nevus. Fig.

5.34

Layers

of

Bruch

membrane,

delineated

on

the

basis

of

electron microscope studies: 1, Interrupted basement membrane

is arrangement allows for lling of the entire choroid simultane-

ously

but

also

creates

watershed

zones

that

make

the

choroid

vul-

of

4,

the

choriocapillaris;

inner

collagenous

2,

outer

zone;

5,

collagenous

basement

zone;

3,

membrane

elastic

of

the

layer;

retinal

56

nerable

and

to

does

growth

hypoxia.

not

e

continue

factor

(VEGF)

choriocapillaris

into

the

ciliary

receptors

are

is

unique

body.

found

to

the

V ascular

in

the

choroid

endothelial

pigment

they

respond

to

the

VEGF

produced

in

the

cells.

(From

Hogan

MJ, Alvarado

JA, Weddell

JE.

choriocapillaris, e

and

epithelial

Histology of the Human Eye. Philadelphia: Saunders; 1971 .)

retinal

suprachoroidal

space

provides

a

pathway

for

the

posterior

pigmented

48

vessels

and

ner ves

that

supply

the

anterior

segment.

epithelium, aiding in blood vessel development and maintenance. With aging, material is deposited between the RPE basement

membrane

Bruch

and

the

inner

collagenous

zone

of

Bruch

mem-

Membrane 57

58

brane.

ese

deposits,

called

drusen,

can

be

seen

as

small,

(Fig.

5.35).

e innermost layer of the choroid, Bruch membrane, fuses with pinhead-sized, the

retina.

It

runs

from

the

optic

nerve

to

the

ora

serrata,

undergoes

some

modication

before

continuing

into

spots

in

the

fundus

where ey

it

yellow-white

the

are

made

up

of

lipids,

cholesterol,

and

proteins.

cili-

53

ary

body.

Bruch

multilaminated

As

seen

from

membrane

brane

ment

of

layer,

of

the

choroid

and

the

tinuous

epithelium

are

the

(2)

the

ciliary

layer

to

(1)

Fine

basement

of

e

acellular,

elastic

(5)

the

from

brils

of

of

com-

zone,

basement

adhesion

the

bers.

basement

collagenous

(3)

mem-

the

base-

the

inner

between

the

retina.

membrane

membrane

body.

of

an

membrane

laments

tight

layer

is

interrupted

and

with

the

the

outer

zone,

merge

pigmented

basement

lamina)

center

the:

5.34).

RPE

contributing

outer,

the

(Fig.

the

serrata,

of

inner,

collagenous

cells

of

zone,

ora

to

a

basal

microscope,

choriocapillaris,

RPE

with

the

containing

inner

the

(or

electron

outer

(4)

the

an

membrane

collagenous

At

sheet

through

ponents,

elastic

membrane

of

the

the

RPE

outer

collagenous

and

is

con-

pigmented

elastic

layers

disappear into the ciliary stroma, and the basement membrane of

the

choriocapillaris

ciliary

body

Functions

of

e

primar y

gen

and

lites

to

the

from

choriocapillaris.

moregulation

pigmented

as

the

basement

membrane

of

the

Choroid

function

nutrients

pass

continues

capillaries.

to

the

e

and

choroid

of

the

the

vascular

outer

retina

through

choroid

also

intraocular

absorbs

retina

choroid

and

Bruch

plays

pressure

excess

an

light,

a

is

to

provide

egress

membrane

role

in

drainage.

as

for

does

into

retinal

e

the

oxy-

catabo-

the

ther-

darkly

RPE

layer.

Fig.

old

5.35

with

Pacic

Fundus

photo

scattered

University

showing

retinal

the

drusen.

Family Vision

right

eye

(Courtesy

Center,

Forest

of

Fraser

Grove,

a

49-year-

Horn,

Ore.)

OD,

CHAPTER

78

5

Uvea

A

B

C

Fig. 5.36

CLINICAL

Choroidal neovascularization in the right eye. A, Fundus image. B, Fluorescein angiography .

C,

Optical

B.

(Courtesy

coherence

Dina

tomography

Erickson,

COMMENT: Age-Related

O.D.,

Macular

taken

of

Pacic

the

same

University

person

but

at

Family Vision

a

later

Center,

date

compared

Forest

Grove,

with

A

and

Ore.)

Degeneration 61

stress Degenerative

processes

involving

the

choroid-retina

interface

in

the

have

been

implicated

in

these

cellular

metabolic

changes.

These

pro-

macular cesses cause exuded material to build up forming hydrophobic drusen between

area

often

are

manifested

as

age-related

macular

degeneration

(AMD).

AMD the

RPE

basement

membrane

and

the

inner

collagenous

zone

Bruch

mem-

basement

of

mem-

59

is the most common cause of blindness in Western countries.

Risk factors asbrane,

sociated

with

AMD

include

age,

genetics,

smoking,

a

diet

low

in

basal

56

ethnicity,

and

oxidative

deposits

between

the

RPE

and

the

RPE

antioxidants, 58

60

brane, 57

Caucasian

laminar

and

reticular

pseudodrusen

in

the

RPE

within

the

perifoveal

area

58

damage. 56

or

choroidal

watershed

zones.

The

accumulation

of

lipids

with

increasing

60

Early

AMD

is

characterized

by

drusen

and

RPE

abnormalities.

Advanced

AMD,

age

tends

to

be

greater

in

the

central

fundus

which can result in severe vision loss, involves either subretinal neovascularization

membrane

(Fig. 5.36) or geographic atrophy of the choroid, RPE, and photoreceptors ( Fig. 5.37).

thereby inhibiting the passage of metabolites.

becomes

hydrophobic

and

than

presents

a

in

the

barrier

to

periphery.

water

Bruch

movement,

62

If water accumulates between

63

the Metabolites

from

the

choriocapillaris

and

waste

products

from

the

RPE

pass

pigment

through

that

accumulates

Bruch

builds

at

the

up

membrane.

after

base

of

With

portions

the

RPE

of

age,

lipofuscin,

photoreceptors

causing

RPE

an

Bruch

membrane,

displacement

and

detachment

may

occur.

This

retina process

must

and

is

represented

diagrammatically

in Fig.

5.38

autouorescent

are

dysfunction

phagocytosed,

and

changes

in

Loss of nutrients to the highly metabolic retina can cause: (1) atrophy of the RPE,

followed

by

loss

of

photoreceptors,

or

(2)

development

of

a

neovascular

mem-

60

the

permeability

of

Bruch

membrane.

Free

radicals

resulting

from

oxidative

brane

in

an

attempt

to

compensate

for

the

loss

of

nutrients

(see Fig.

5.36).

The

CHAPTER

5

79

Uvea

presence of drusen can impair the ability of VEGF to travel between the RPE and

VEGF

receptors

ischemia.

The

new

RPE

or

choriocapillaris

branch

fragile,

denitive

xanthin)

the

penetrate

are

oxidants

in

production

vessels

can

vessels

No

VEGF

or

treatment

may

for

the

AMD

to

choriocapillaris

causing

choriocapillaris

tend

high

some

leading

increased

membrane

and

(e.g.,

provide

then

from

Bruch

leak,

minerals

is

to

and

exists

doses

protective

as

of

yet,

but

or

damage

vessel

remain

retina.

retinal

and

the

E,

and

growth.

beneath

However,

the

these

tissue.

supplementation

C

slow

blood

can

the

into

vitamins

effect

and

enter

hemorrhage

new

zinc,

with

lutein,

progression

to

anti-

and

zea-

advanced

58 64–66

disease

in

patients

with

high-risk

characteristics.

Although

there

is

no

cure

for AMD, intravitreal anti-VEGF injections have been shown to prevent vision loss

by targeting choroidal neovascular membranes. There is currently no treatment for

atrophy

of

the

RPE

and

photoreceptors;

however,

clinical

trials

using

humanized

monoclonal antibodies and various antiinammatory agents have shown promise.

BLOOD

SUPPLY

TO

THE

UVEAL

TRACT

e short posterior ciliary arteries enter the globe in a circle around

the

in

Fig.

5.37

Fundus

photo

showing

the

left

eye

of

a

patient

with

optic

the

nerve,

posterior

ies

supply

lar

zones

the

of

and

their

pole.

anterior

the

nasal

branches

Branches

of

choroid,

and

supply

the

as

long

well

temporal

as

the

choroidal

posterior

wedge-shaped,

choroid

between

vessels

ciliary

the

arter-

triangu-

posterior

48 67 68

age-related

macular

degeneration.

Conuent

drusen,

disci-

pole

and

peripheral

retina.

e

watershed

regions,

the

area

68 69

form

scarring,

and

dent.(Courtesy

Center,

Forest

pigment

Fraser

Grove,

mottling

Horn,

O.D.,

in

the

Pacic

macular

University

area

are

evi-

between two vessel distributions, is prone to choroidal ischemia.

Family Vision

Ore.)

e

long

arteries

join

posterior

to

form

ciliar y

the

arteries

major

circle

and

of

the

the

anterior

iris,

which

ciliar y

supplies

vessels to the iris and ciliar y body. e venous return for most of

the

uvea

is

through

information

4

3

2

5

on

the

the

vortex

blood

veins

(see Chapter

12

for

further

supply).

7

INNERVATION

Sensor y

ciliar y

TO

inner vation

ner ve,

a

THE

of

the

branch

of

UVEAL

uvea

the

is

TRACT

provided

ophthalmic

through

division

the

of

naso-

the

tri-

RPE

geminal

ner ve.

ganglion

the

via

Sympathetic

the

choroidal

bers

ophthalmic

blood

and

vessels,

from

short

and

the

superior

ciliar y

ner ves

sympathetic

cer vical

inner vate

bers

from

the

Bruch’s

superior

membrane

1

cer vical

the

iris

the

ciliar y

dilator

ganglion

and

ciliar y

ganglion

via

the

long

muscles.

inner vate

the

ciliar y

ner ves

Parasympathetic

ciliar y

muscle,

the

inner vate

bers

iris

from

sphinc-

6

ter

Choroid

Fig.

5.38

Summary

Bruch

membrane

retinal

pigment

1,

metabolites

across

the

nantly

from

catabolism

are

the

implications

transport

epithelium

pass

RPE

of

for

to

from

the

neural

results

predominantly

in

(RPE).

the

retina

the

cleared

In

choroid

neural

retina;

to

of

the

the

the

accumulation

operating

youngest

through

2,

of

choroid.

and

3,

waste

In

the

predomi-

progress

products

older

age

AGING

with

of

that

With

the

increasing

within

age,

the

catabolism

RPE;

5,

waste

results

in

products

in

lipid

age,

tion

may

within

Bruch

membrane;

6,

accumulation

IN

THE

UVEA

be

of

pigment

margin

seen

on

from

with

the

the

iris

epithelium

transillumination.

iris

surface,

anterior

is

evident

Pigment

lens

at

deposi-

and

trabecular

meshwork.

e

surface,

dilator

pos-

muscle

(lipo-

begin

of

loss

cornea,

atrophic,

and

the

sphincter

muscle

becomes

sclerotic,

to

making accumulate

vessels.

group:

accumulations

rich

CHANGES

pupillar y

becomes fuscin)

choroidal

Iris

terior

4,

the

group:

membrane

moves

and

in

across

age

Bruch

water

choroid;

accumulation

via

lipid

systems

muscle,

it

more

dicult

to

dilate

the

older

pupil

pharmacologi-

lipid-rich 70

debris

within

Bruch

membrane

may

inhibit

metabolic

input

to

cally.

With

more

convex

age,

the

pupil

size

decreases,

and

the

2

neural

Bruch

retina;

and

membrane

7,

the

presence

impedes

the

of

a

hydrophobic

passage

of

water

barrier

and

may

detachment

shall

J,

etal.

of

the

Aging

RPE.

(From

changes

in

Pauleikhoff

Bruch’s

D,

Harper

membrane:

a

shape,

bowing

toward

the

develops

a

71

cornea.

within

result

Ciliary in

iris

the

CA,

Body

Mar -

histochemi-

Although

the

amount

of

connective

tissue

within

the

layer

72

cal

and

morphological

study.

Ophthalmology.

1990;97(2):171 .)

of

ciliar y

muscle

increases

with

age,

there

is

no

signicant

CHAPTER

80

correlation

between

5

loss

Uvea

of

ciliar y

muscle

contractile

ability

15.

72,73

and

age.

Ciliar y

muscle

contraction

does

not

diminish

coma. Graefe’ s Arch Clin Exp Ophthalmol. 2018;256:2165–2172.

74

age.

e

formation

of

aqueous

decreases

with

age,

and

by

age

16.

80

Mao Y , Bai HX, Li B, etal. Dimensions of the ciliary muscles of Brücke,

Müller, and Iwano and their associations with axial length and glau-

with

years

it

is

approximately

25%

of

what

it

was;

however,

Gabelt BT , Kaufman PL. Aqueous humor dynamics. In: Kaufman

the PL, Alm A, eds. Adler’ s Physiology of the Eye. 10th ed. St Louis:

75

volume

of

the

anterior

chamber

decreases

by

about

40%. Mosby; 2003:237.

17.

Raviola

G.

e

structural

basis

of

the

blood-ocular

barriers.

Exp

Choroid Eye

e

changes

that

occur

in

AMD

occur

throughout

the

18.

membrane

aect

visual

increases

in

acuity

and

thickness

the

and

patient’ s

becomes

daily

life.

hyalinized

the

V arious

substances

membrane’ s

and

permeability

particles

to

accumulate,

serum

proteins,

its

mol

19.

Vis

Kasahara

20.

of

in

Sci.

Eichhorn

organ

capac-

76–79

K,

(GLUT1)

with

decreasing

and

Takats

localization

Bruch

60

age.

1997;25(suppl):27.

choroid

with advancing age. However, only those occurring in the macula

signicantly

Res.

the

the

T ,

Kasahara

M,

etal.

Ultracytochemical

er ythrocyte/HepG2-type

ciliar y

body

and

iris

of

the

glucose

rat

eye.

transporter

Invest

Ophthal-

1991;32(5):1659.

M,

Inada

culture.

K,

Curr

Noske

W ,

ciliar y

epithelium:

Stamm

Lütjen-Drecoll

Eye

CC,

Res.

E.

Human

ciliar y

body

in

1991;19(4):277.

Hirsch

M.

Tight

junctions

of

the

human

ity to facilitate metabolite exchange with the retina decreases.

Calcication

and

deposits

in

the

innermost

part

of

Bruch

are

responsible

for

the

clinical

appearance

of

hard

morpholog y

and

implications

on

tran-

memsepithelial

brane

regional

resistance.

Exp

Eye

Res.

1994;59:141.

drusen, 21.

Shiose

Y .

Electron

microscopic

studies

on

blood-retinal

and

60,62

which

increase

in

number

with

age. blood-aqueous

e

choriocapillaris

decreases

in

density

and

barriers.

Japan

J

Ophthalmol.

1970;

diameter, 14:73(Abstract).

resulting

in

a

decrease

in

choroidal

blood

ow,

and

choroidal 22.

Mauger

RR,

Likens

CP ,

Applebaum

M.

Eects

of

accommodation

46,49,61,80

thickness

decreases

in

the

normal-aging

macula.

and

J

23.

repeated

Optom

Tamm

ment

REFERENCES

Physiol

E,

of

Sidhartha

features

2.

E,

and

Hogan

He

relationship

ed.

Fine

M,

among

the

R.

JA,

Human

Eyeball.

Assessment

with

iris

Y ano

M.

Wol ’s

iris

Asian

24.

eyes.

structural

Chinese

anterior

Saunders;

Anatomy

mea-

and

of

the

chamber.

In:

Eye

and

plications.

Md:

Harper

alterations

eyes

CM,

Anatomy,

Physiolog y,

Butter worth-Heinemann;

Tektas

within

with

Pupil:

the

OY ,

Kaufman

peripheral

pigmentar y

PL,

xation

glaucoma.

&

Clinical

the

29.

iris

dilator

Ophthalmol

Vis

Imesch PD, Bindley CD, Khademian Z, etal. Melanocytes and iris

Rennie

and

IG.

other

Don’t

it

make

abnormalities

my

of

blue

the

eyes

iris.

brown:

Eye

31.

heterochromia

(London,

England).

32.

Wilkerson CL, Syed NA, Fisher MR, etal. Melanocytes and iris color,

Albert

bers

Am

12.

DM,

in

Asian,

W akamatsu

various

Hogan

in

K,

Soc.

Hu

human

colored

MJ,

chamber.

WR,

African

Ophthalmol

melanin

13.

Green

33.

ML,

American,

etal.

and

McCormick

iridal

irides.

Alvarado

In:

Zimbri

Iris

melanocyte

Caucasian

irides.

num-

Transact

and

choroidal

Pigment

JA,

Histolog y

of

Cell

Weddell

the

SA,

Characterization

melanocytes

Melanoma

JE.

Human

Ciliar y

Eye.

Res.

body

from

eye

34.

of

with

and

posterior

35.

Flügel-Koch

indication

C,

for

Ophthalmol

Am

W ,

etal.

Optom.

H,

Sci.

old,

attach-

presbyopic

1991;32:1678.

muscle

D,

Esteve-Taboada

during

JJ,

accommodation:

2019;12(1):14–21.

etal.

during

Posterior

accommodating,

Age-related

changes

accommodation.

Invest

in

the

anterior

Ophthalmol

Vis

LN.

e

eect

and

of

ageing

contractility.

on

in

Invest

vivo

human

Ophthalmol

ciliar y

Exp

RG,

blood

Eye

Lee

Ophthalmol

Hollingswor t h

humor

Re.

RK,

J.

ow

and

ultraltration

in

aqueous

1973;16:287–298.

etal.

Aqueous

humor

dynamics:

a

2010;(4):52–59.

M,

R ao

pro duc tion.

R,

Prog

eta l.

Retin

Ci liar y

Eye

blo o d

Res.

ow

and

2011;30(1):

36.

Saunders;

HA,

agonist

Exp

e

Candia

Posey

on

Eye

NA.

Res.

of

Prog

Macri

Cevario

FJ,

body

the

Alvarez

epithelia.

Retin

LJ.

Eye:

Res.

e

A

and

Do

Civan

MH,

uid

AJ,

ous

of

a

topical

aqueous

α2

adren-

production

in

MM.

Species

epithelium:

ciliar y

epithelium.

In:

Fischbarg

2006:127–148.

transport

phenomena

in

ocular

and

inhibition

mechanism

variation

similarities

in

of

biolog y

and

of

action.

and

dierences.

aqueous

Arch

Oph-

physiolog y

E xp

Eye

2009;88:631–640.

Levin

Sit

ciliar y

and

formation

1978;96:1664–1667.

CW ,

Eects

2008;27:197–212.

proposed

thalmol.

the

JW .

ow

Elsevier ;

Fluid

Eye

SJ.

production.

Kiel

blood

2006;82(3):405–415.

Ciliar y

Biolog y

OA,

M,

ciliar y

Verkman

transport.

Nau

CB,

dynamics

J

AS.

Mclaren

in

Aquaporins

Membrane

young

JW ,

Biol.

etal.

healthy

and

CFTR

in

ocular

epithe-

2006:205–215.

Circadian

adults.

variation

Invest

of

aque-

Ophthalmol

Vis

Sci.

2008;49(4):1473–1479.

Neuhuber

WL,

proprioception

Vis

of

Picciani

JW ,

ed.

lial

1971:260–319.

14.

Vis

ciliar y

morpholog y

role

Open

Delamere

Res.

2007;21:97–105.

Philadelphia:

Jungkunz

young,

Monsálvez-Romín

the

Davies

formation.

Reitsamer

of

etal.

pressure.

2011;52(3):1809–1816.

M,

humor

2003;101:217–222.

DN,

Kiel

J,

light microscopic ndings. Arch Ophthalmol. 1996;114:437–442.

11.

Goel

AL,

e

rabbits.

2012;26(1):29–50.

10.

A.

ergic

color. Electron microscopic ndings. Arch Ophthalmol. 1996;114:443.

9.

J

Jiang

intraocular

1–17.

30.

2014;55(7):4541–4551.

8.

Sci.

Bill

aqueous

muscle

Sci.

A,

in

biometr y

muscle

review.

Morphological

analysis.

A,

E,

in

Ophthalmol

age

on

2015;56(6):3522–3530.

humor

Ap-

of

Tao

Sheppard

Vis

1999.

etal.

of

Invest

and

Y ,

ciliar y

28.

e

Boston:

Flügel-Koch

26.

27.

Hagerstown,

Shao

Sci.

Orbit.

1979:195.

IE.

Eect

segment

1971:202–259.

1976:30–180.

Histolog y.

25.

Invest

tonometr y

1984;61(1):28.

muscle

Domínguez-Vicent

etal.

2012;40(2):162–169.

and

Philadelphia:

Saunders;

Ocular

Iris

in

surface

American

Ophthalmol.

JE.

iris

sectorial

in

Caucasians,

W eddell

Eye.

of

thickness

Dierences

E xp

In:

Philadelphia:

BS,

etal.

Clin

Alvarado

of

Loewenfeld

in

L,

American

Chinese.

MJ,

War wick

Row ;

7.

etal.

Wu

7th

6.

J,

2014;121(5):1007–1012.

D,

Histology

5.

Liao

Wang

mainland

4.

their

P ,

Ophthalmolog y.

surements

3.

Gupta

Optic.

Lütjen-Drecoll

ciliar y

monkeys.

1.

applanation

Sci.

Kaufman

in

the

PL,

human

2009;50(12):5529–5536.

etal.

ciliar y

Morphologic

muscle.

Invest

37.

Gautam

tions

in

N,

Kaur

S,

intraocular

(Report).

Br

J

Kaushik

pressure

Ophthalmol.

S,

etal.

across

Postural

the

and

spectrum

2016;100(4):537–541.

diurnal

of

uctua-

glaucoma.

CHAPTER

38.

Moon

Y ,

Lee

intraocular

level

Sci.

39.

in

Smith

of

U,

Raunio

RS.

the

of

J,

ZO-1

45.

Am

and

diurnal

between

intraocular

patients.

Invest

nocturnal

J

Wu

on

the

Ophthalmol

of

e

aqueous

the

Eye

the

iris

and

barrier.

ciliar y

63.

64.

junction-

barrier :

humor

of

past,

present,

Park

to

ethnicity

coherence

JY ,

Kim

of

measured

L,

Exp

BG,

Hwang

vascular

coherence

JH,

arcade

in

etal.

using

tomography.

Laviers

H,

choroid:

etal.

tomography.

Zambarakj

a

review

Ophthalmol.

Borrelli

E,

ation

the

Eye

of

Res.

Adhi

dal

65.

Eye

Res.

enhanced

thickness

depth

in

66.

imaging

eyes

thickness

using

in

in

M,

Schrödl

in

D,

current

Freund

and

D,

Ophthalmol

depth

Vis

67.

K,

etal.

Baxter

F ,

the

aging

tomography.

in

L,

the

Graefe’s

Arch

of

the

Clin

eyes

PloS

OCT

angiography

disorders.

and

Prog

Adamson

Characterization

using

S,

enface

evalu-

Spitzmas

Kaser-Eichberger

53.

Sci.

A,

of

choroi-

swept-source

Compelling

adult

Trost

Reale

Hogan

E.

70.

human

A,

Invest

cells

in

human

faces

MJ,

Alvarado

evidence

choroid.

Eye.

etal.

Lymphatic

Ophthalmol

of

Vis

fenestrations

choroidal

Weddell

Philadelphia:

JE.

Saunders;

Exp

71.

KR,

in

Sohn

the

degeneration.

57.

Al-Zamil

ular

58.

Mitchell

P ,

H,

(London,

Y assin

Liew

Lancet.

Stone

SA.

a

G,

vessels.

Choroid.

and

Invest

Ophthalmol

In:

Histolog y

of

73.

monograph:

of

cataract,

and

1973–1975.

Gupta

T,

Surv

rioretinal

an

acuity

74.

Arora

an

Sng

Disease

C

B,

Int

Aging.

etal.

for

diabetic

a

and

molecular

age-related

in

J,

76.

and

LR,

NF ,

macular

e

and

mac-

77.

J

2

J,

etal.

and

me m-

Retin

Eye

Aging

Res.

changes

morphologic

Research

acids

Eye

Am

for

Group.

in

study.

Lutein

age-related

Disease

Med

Study

Study

Assoc.

Research

trial

beta

and

Phillips

+

macular

2

(AREDS2)

2013;309(19):2005–

of

carotene,

vision

Group.

high-dose

and

loss:

A

randomized,

supplementation

zinc

AREDS

for

age-related

report

no.

8.

Arch

DI,

etal.

macular

Lutein

and

degeneration.

zeaxanthin

Invest

status

Ophthalmol

ciliar y

arter y

lecture.

circulation

Invest

in

health

Ophthalmol

Vis

and

Sci.

748.

population

Strenk

N,

choroidal

2631

Vaclavik

V ,

infarction.

etal.

Retin

e

Case

spectrum

Brief

Rep.

immunohistochemical

study.

in

J

D.

Amalric

layer

triangular

infarction.

syndrome

Ophthalmic

Surg

asso-

Lasers

2017;48(8):668–670.

CD.

b o dy.

Practice

of

Aging

In:

changes

Alb er t

DM,

in

trab ec ular

Jakobie c

O phthalmolog y.

JC,

Nongpiur

measurements

degen-

Mc

Study.

cho-

Histochem

Sivak

Optom

in

Invest

JG.

Vis

ME,

a

FA,

meshwork,

e ds.

Philadelphia:

etal.

Chinese

Ophthalmol

Age-related

Sci.

Semmlow

ciliar y

Invest

Pr in-

Saunders;

Associations

population:

Vis

Sci.

of

the

iris

Singapore

2013;54(4):2829–

SA,

JL,

muscle

LM,

J

Cataract

JW .

Strenk

and

Ophthalmol

Strenk

changes

in

human

ciliar y

2000;77(4):204.

Vis

Guo

accommodating,

Laren

Moore

Sci.

S.

Refract

a

etal.

changes

resonance

imaging

1999;40(6):1162.

and

Surg.

of

Age-related

magnetic

Magnetic

phakic,

Measurement

LM,

lens:

resonance

pseudophakic

imaging

ciliar y

of

muscle

2006;32:1792–1798.

aqueous

humor

ow.

Exp

Eye

Res.

DJ,

Clover

Moore

DJ,

Sci.

Hussain

JW ,

Curcio

visualization

Huang

JD,

eect

Bruch’s

AA,

of

age

on

membrane.

Marshall

of

Exp

Presley

Eye

J.

Bruch’s

analysis

choroid

in

of

Ophthalmol

JB,

the

macromolecular

Invest

Ophthalmol

Vis

Age-related

membrane.

variation

Invest

in

the

Ophthalmol

CL.

lipid

Vis

Chimento

etal:

Sci.

MF ,

membrane

Quick-freeze/deep-

accumulation

etal.

as

in

Bruch’s

2003;44:1753.

Age-related

seen

by

changes

in

quick-freeze-deep-

2007;85:202–218.

van

der

Bruch’s

aging.

Millican

age-related

Bruch’s

Res.

RS,

CA,

of

Invest

macular

Ramrattan

ric

e

1995;36(7):1290.

Ruberti

human

80.

GM.

human

conductivity

membrane.

79.

of

2001;42:2970.

etch

adults,

the

MT,

SA,

Strenk

etch.

changes

Sarraf

nuclear

B elcher

Eye

human

Vis

degen-

Framingham

macular

of

EJ,

outer

Allen

hydraulic

epidemiological

retinopathy,

Holz

ciliar y

and

Pardue

Sci.

78.

etal.

Age-related

2017;65(10):567–577.

E,

Weisenfeld

permeability

1980;24:335.

etal.

Br uch’s

2009;88:641–647.

macular

age-related

Age-related

general

fatty

clinical

triangular

diameters.

75.

2017;12:1313–1330.

ophthalmological

in

in

Prog

2001;119(10):1417.

Retina.

CC,

aging,

2017;31(1):10–25.

Maunder

Ophthalmol.

N,

junction:

Cytochem.

DE,

glaucoma,

visual

Saini

Structural

developments

Clin

Gopinath

Eye

eration,

etal.

implications

Recent

Marshall

Phasukkijwatana

D C,

and

study.

the

2018;392(10153):1147–1159.

Krueger

J,

ST,

muscle.

junctions

1971:320–392.

England).

review.

HM,

Study

EM,

choroid:

Leibowitz

study

60.

Eye

degeneration:

eration.

59.

W ,

E

aging

age.

2835.

Chakravarthy U, Gardiner TA. Endothelium-derived agents

Chirco

C hange s

w it h

Study

trial.

Posterior

with

Chinese

mark-

Sci.

Bernstein MH, Hollenberg MJ. Fine structure of the choriocapillaris

changes

Surv

1994:697.

for

Clin

in pericyte function/dysfunction. Prog Retin Eye Res. 1999;18(4):511.

56.

O ates

ciples

and retinal capillaries. Invest Ophthalmol Vis Sci. 1965;4(6):1016.

55.

Eye

the

Garrity

in

JA,

A.

Age-Related

age-related

SS.

amalric

ir is,

optical

72.

Fracture

degen-

2003;44:2461.

structural

choroid.

CA,

Disease

the

Hall

of

Nemiro

ciated

1975;14:98–107.

Human

54.

M,

endothelial

Vis

69.

Retin

2015;10(7):e0133080.

etal.

and

macular

strategies.

2017;11(1):S113–S120.

vascular

etal.

One.

developing

human

Sci.

Hayreh

of

Exp

2015;56(12):7406–7416.

of

68.

2012;40(1):128.

adult

CR,

Imaging

RF ,

Age-related

therapeutic

histochemical

degeneration

risk

disease:

Sci.

imaging-OCT

literature.

choroidal

Mullins

normal

Ophthalmol.

ers

the

choroid

Ferrara

layers

Koina

of

Enhanced

Bi rd

omega-3

2004;45(3):749–757

H.

and

1990;97(2):171.

clinical

vitamins

Gale

Vis

and

spectral-domain

2018;67:30–55.

M,

lymphatics

52.

Age-related

and

2016;36(1):82–90.

Choroidal

Invest

A

placebo-controlled,

1965;4:135.

2014;252(12):1871–1883.

Sarraf

coherence

51.

and

randomized

administered

Choroidal

Retina.

healthy

etal.

2015.

topically

dynamics.

Tang

P ,

Harper

Eye

degeneration:

and

2017;58(13):5827–5837.

50.

Age-Related

Ophthalmol.

optical

49.

D,

Karapetyan

P ,

SH,

st r uc ture s

membrane.

macular

outside

48.

Pauleikho

with

Ouyang

Y oo

2003;48(3):257.

Lut her t

Schlingemann RO, Hofman P , Klooster J, etal. Ciliary muscle capillar-

A,

BK,

pathogenesis,

rel ate d

ies have blood-tissue barrier characteristics. Exp Eye Res. 1998;66:747.

optical

47.

R,

and

zeaxanthin

occlud-

2002;71:123(Abstract).

barriers:

Eects

Guy mer

Bruch’s

body

1997;93:149.

RT.

Ambati

Ophthalmolog y.

of

blood-aqueous

Res.

etiolog y,

81

Uvea

1999;18(1):59.

blood-aqueous

in

J,

brane

aqueous

1971;71:1066.

blood-ocular

Jackson

human

Co-locolaization

human

Exp

of

tracer

etal.

the

normal

Ambati

eration:

Ophthalmol.

Vis

1969;159:178.

studies

P ,

Ophthalmol.

MB,

of

Ophthalmol.

H,

61.

pressure

62.

Proteins

F-actin.

JG.

Doc

relation

46.

Relationship

and

electron-dense

proteins

Waitzman

ouabain

44.

an

Gong

Cunha-Vaz

future.

V .

Ultrastructural

mouse.

Sonsino

ing,

43.

etal.

glaucoma

Ophthalmologica.

associated

42.

DW ,

elevation

2015;56(9):5271–5279.

Krause

Transport

41.

Jeong

normal-tension

humour.

40.

JY ,

pressure

5

Scha

TL,

membrane,

Invest

Mooy

the

Ophthalmol

CM,

etal.

Morphomet-

choriocapillaris,

Vis

Sci.

and

the

1994;35(6):2857.

6

Aqueous

e

aqueous

within

the

aqueous

ous

gel.

and

eye.

vitreous

e

humor,

A

and

are

anterior

and

the

description

Vitreous

contained

and

vitreous

of

each

in

posterior

chamber

chamber

Humors

three

chambers

chambers

contains

will

contain

the

be

followed

and

function

many

vitre-

ous

by

with

an

of

aspect

the

of

with

the

trabecular

the

spur,

that

of

scleral

meshwork

such

the

spur

that

the

trabeculae

aid

in

sheets

collagen

(Fig.

widening

attach

of

the

6.2).

the

to

the

spur

ese

is

anterior

continu-

connections

intertrabecular

spaces

1

explanation

aqueous

of

and

the

the

formation,

composition,

of

the

and

maintaining

e

anterior

tion

of

the

anterior

(Fig.

6.1).

er y

of

tissue

the

body,

surface

e

peripher y.

is

bounded

peripherally

ciliar y

iris

and

and

center

of

by

the

the

the

the

anteriorly

trabecular

iris

root;

pupillar y

anterior

anterior

e

chamber,

aqueous

where

humor

the

the

is

deeper

formed

the

a

por-

by

anterior

at

the

periph-

and

anterior

the

lens

than

the

corneoscleral

exits

corneal

posteriorly

of

chamber

the

by

meshwork,

and

area

e anterior chamber angle is

meet.

Schlemm

canal.

trabecular

meshwork

encircles

the

circum-

CHAMBER

chamber

endothelium;

of

Meshwork

avascular

ference

e

patency

vitreous.

Trabecular

ANTERIOR

the

uveal

chamber

aspect

of

of

the

the

triangular

anterior

internal

shape,

membrane

scleral

with

(termed

chamber,

its

occupying

sulcus.

apex

Schwalbe

at

In

the

line)

most

of

the

cross-section,

termination

and

its

of

base

at

inner

it

has

a

Descemet

the

scleral

spur (Fig. 6.3). e inner face borders the anterior chamber, and

the

outer

side

canal.

e

sheets,

with

into

15

to

lies

against

meshwork

three

20

to

ve

sheets

corneal

is

as

stroma,

composed

sheets

they

at

the

extend

sclera,

of

and

attened

apex.

ese

posteriorly

Schlemm

perforated

sheets

from

branch

Schwalbe

2

through

the

structures

located

in

this

angle.

line

to

the

scleral

latticework,

Anterior

e

the

ltration

Schlemm

the

Chamber

structures

as

the

ese

area

aqueous

consist

of

the

structures

located

internal

Structures

which

apparatus,

canal.

excavated

known

Angle

through

at

the

scleral

lar

exits,

collectively

trabecular

and

the

internal

called

meshwork

scleral

spur

corneoscleral

and

spaces

openings

and

join

the

junction

tion

of

of

the

e

Spur

scleral

lters

spur

lies

at

the

posterior

edge

of

the

internal

scleral

smaller

aqueous

area

sulcus (see Ch. 4). e posterior portion of the scleral spur is the

similar

attachment

endothelial

to

the

near

stem

a

e

connected

openings

canal.

canal.

is

No

e

adjacent

to

canal.

ese

cells

cells

ere

may

be

is

pores,

portion

directly

for

the

tendon

of

ciliar y

muscle

bers,

whereas

e

cells

of

meshwork

the

can

trabecular

capable

be

meshwork

of

separated

into

two

aer

in

which

that

this

properties

replacing

3

site

por-

tissue

diers

evidence

have

or

sizes

anterior

meshwork

that

open

var ying

connective

is

reside

an

apertures

trabecular

canal.

of

most

posterior

where

is

intertrabecu-

through

are

Schlemm

Schlemm

niche

meshwork

interlace.

Schlemm

meshwork

than

cells.

are

e

Schlemm

more

into

is

trabecular

which

sheets

with

rather

from

of

sheets.

trabecular

limbus

anterior

the

the

meshwork

structure

Scleral

between

the

e

branches

within

become

occupy

sulcus.

the

spur.

the

4

injur y.

anatomic

divisions.

e corneoscleral meshwork is the outer region; its sheets attach

to

Canal

the

scleral

spur.

e

inner

sheets,

which

lie

inner

to

the

spur

of

and

attach

to

the

ciliar y

stroma

and

longitudinal

muscle

bers,

Schlemm

make

e m

b ra T

e

c

u

s

ro

the

uveal

5

to

the

e

is Ir

up

rk o w h

la

iris

meshwork;

some

of

these

sheets

may

attach

6

root.

e

corneoscleral

two

portions

meshwork

is

dier

sheetlike,

slightly

and

in

the

structure.

uveal

mesh-

t o 2

work

the

is

cordlike

largest,

and

(Fig.

pore

6.4).

size

e

pores

in

diminishes

the

in

the

uveal

meshwork

sheets

closer

to

are

the

canal. Projections from the surface layer of the iris, known as iris

processes

jecting

e

of

6.1

anterior

82

Periphery

chamber

of

the

angle

anterior

are

labeled.

chamber.

Structures

of

the

(see

and

covered

e

by

5.7),

a

than

meshwork

elastic

cells

connect

for ward

trabecular

endothelial

lium.

Fig.

farther

collagen

and

Fig.

no

bers

basement

are

a

endothelial

to

the

the

beams

consist

embedded

membrane

continuation

cells

trabeculae,

midpoint

contain

of

the

in

and

the

of

the

of

usually

pro-

meshwork.

an

inner

ground

core

substance

endothelium.

corneal

cellular

e

endothe-

organelles

for

CHAPTER

6

Aqueous

and Vitreous

T rabecular

Canal

b

of

83

Humor s

meshwork

Schlemm

Scleral

spur

c

1

a

A

d

2

Ciliar y

muscle

B

C

d

e

j

D

h

i

f

g

Fig.

6.3

Light

micrograph

of

transverse

section

through

the

k

j

anterior

scleral

chamber

spur,

trabecular

allowing

and

angle

Schlemm

meshwork

them

to

showing

have

relax

the

meshwork,

canal.

properties

and

trabecular

contract.

similar

to

T endons

smooth

of

the

muscle,

ciliary

mus-

cle are connected to the elastic bers within the trabecular lamel-

9

lae Fig.

6.2

Drawing

of

the

limbus.

The

limbal

conjunctiva

(A)

and

juxtacanalicular

muscle formed

by

epithelium

(1)

and

loose

connective

tissue

will

T enon

tissue

capsule

layer

over

(B)

the

forms

a

episclera

thin,

(C).

poorly

Limbal

dened

stroma

enlarge

(D)

merge

(a).

and

in

They

teriorly

this

trascleral

limbal

(d)

cut

and

stroma.

in

of

scleral

scleral

and

stromal

occupies

planes.

plexus

spur

has

corneal

vessels

arcades

Bowman

different

deep

The

scleral

corneal

termination

are

of

Conjunctival

peripheral

the

(c)

composed

region.

form

to

vessels

is

(b),

layer

(e)

are

also

canal

seen

an-

the

within

dense

in-

the

e

region

causing

(f).

The

anterior

part

of

the

longitudinal

thelial

cells

becular

(g)

merges

with

the

scleral

spur

and

of

The

lumen

of

Schlemm

canal

(h)

and

trabecular

loose

and

body

enlarge

outow

resistance.

lining

layer.

the

Tissue

basement

Schlemm

is

It

called

canal

the

consists

of

membrane

from

the

of

sheets

juxtacanalicular

endothelial

cells

the

of

endo-

the

tissue

and

tra-

or

the

broblasts

10–13

e

cells

of

the

juxtacanalicular

tissue

have

pro-

ciliar y

occasionally

joined

by

adhering

and

gap

junctions.

e

mesh-

cells work.

ciliary

embedded in a matrix of collagen, elastic-like bers, and ground

collagen

portion

Connective

meshwork

cribriform

cesses muscle

reduced

separating

substance.

bers

the

spaces

that

Episcleral

forming

shown

and

of

meshwork

the

extend

(arrow).

are

coarse

tissues

which

Vessels

Contraction

trabecular

connective

Juxtacanalicular area

the

stroma

Schlemm (2).

tissue.

is

tissues

of

also

form

similar

connections

with

the

endothelium

of

the

its 14

inner wall

are

seen.

Sheets

of

the

corneal

trabecular

meshwork

(i)

to

cords

of

uveal

meshwork

(j).

An

iris

process

(k)

is

of

Schlemm

canal.

ere

are

micron-sized,

spaces

within

the

juxtacanalicular

tissue

and

inner

9

arise

from

meshwork

Descemet

or

border

JE.

the

at

iris

the

surface

level

membrane

of

the

Histology

the

the

(From

Human

travel

anterior

terminates

limbus.

of

of

and

portion

(double

Hogan

Eye.

toward

MJ,

the

of

at

Alvarado

Philadelphia:

canal

that

appear

to

lack

extracellular

15

of

16

matrix

and

trabecular

scleral

arrows)

wall

seen

Schlemm to

pore-

are

like outer

wall

JA,

spur.

may

anteri-

of

Weddell

to

the

Saunders;

1971 .)

provide

the

the

brils

a

canal.

pathway

e

juxtacanalicular

that

also

for

uid

endothelium

tissue

connect

to

by

the

to

of

a

move

toward

Schlemm

network

scleral

spur

of

the

canal

inner

is

wall

anchored

elastic-containing

and

the

tendon

of

the

12

ciliar y

muscle.

is

connective

14

lating

protein

tissue

synthesis

and

components.

are

capable

ese

cells

of

also

replacing

contain

the

them

eroding

and

the

capacity

abnormal

short

areas

of

for

phagocytosis,

extracellular

tight

matrix

junctions

join

removing

buildup.

occludens

are

found.

the

6

cells

of

At

lial

neighboring

the

scleral

covering,

but

Cytoplasmic

the

the

Gap

junctions

endothelial

cells;

projections

no

connective

tissue

collagenous

of

the

spur

e

sheets

lose

their

and

elastic

bers

and

ciliary

body.

endothe-

continue

into

6

Cells

of

modu-

17

outow.

Schlemm

be

canal

a

of

the

the

lies

of

channel,

rather

anterior

canal

(see

than

to

lies

against

spur

Schlemm

venous

humor

and

2

the

connect

8

trabecular

in

and

sheets.

spur,

help

which

debris

7

zonula

might

connective

lysosomes,

Canal give

aqueous

network

blood.

the

a

circular

It

scleral

against

the

Fig.

is

although

the

is

it

outer

spur

Within

limbal

the

to

(Fig.

juxtacanalicular

6.3).

vessel

and

normally

the

e

and

connective

lumen

of

considered

trabecular

6.5).

sclera,

is

contains

meshwork

external

the

wall

internal

tissue

Schlemm

to

aqueous

and

of

wall

scleral

canal,

septa

CHAPTER

84

6

Aqueous

and Vitreous

Humor s

1

2

3

Fig.

6.5

Optical

chamber

canal

angle.

(cur ved

work

(double

canal.

e

of

cells,

the

Pores

an

5

arrow),

which

and

10

21

wall

of

the

Drawing

of

aqueous

outow

apparatus

and

of

(2),

(arrow),

contributes

of

to

resistance

vesicles

passage

the

iris

anterior

(3),

Schlemm

trabecular

mesh-

in

the

aqueous

increased

to

aqueous

cell

sti ness

outow.

membrane

humor

into

are

Schlemm

24

basal

Schlemm

side

that

of

canal.

membranes

vacuoles 6.4

body

spur

increase

Transcellular

on

apical

Fig.

nature

can

the

canal.

sure

tomography

ciliar y

scleral

pinocytic

for

15

(1),

arrow).

contractile

avenue

2

coherence

Cornea

to

empty

pores

the

e

cells

come

into

occur

as

endothelial

deform

together

Schlemm

uid

cells

causing

and

canal.

exerts

along

fuse

pres-

the

the

inner

basal

forming

Paracellular

and

giant

pores

are

adjacent

areas of dilation within the intercellular space. is dilation may tissues.

Schlemm

ternal

collector

terior

part

extend

(d)

(f)

of

from

channel

the

the

posteriorly.

occupy

canal

(a)

(of

canal.

divided

corneolimbus

inner

into

Sondermann)

Sheets

Ropelike

the

is

of

of

(b)

portions.

opens

corneoscleral

(e)

anteriorly

components

portion

two

the

of

to

the

into

the

the

in-

pos-

meshwork

scleral

uveal

trabecular

An

(c)

spur

meshwork

meshwork;

increase

in

the

ciliar y

body

(CB)

near

the

angle

recess

and

the

lar

as

pores

act

cell

to

the

(h)

termination

extends

from

of

the

Descemet

iris

root

to

membrane

merge

(g).

with

become

internal

at

approximately

the

level

of

the

anterior

part

spur. The

of

spur,

longitudinal

but

a

portion

ciliar y

of

muscle

muscle

(i)

joins

is

attached

the

the

deep

tinuous

(arrows).

Descemet

corneolimbus. The

with

the

trabecular

membrane

corneal

at

(j).

A

(double-headed

to

membrane

arrows)

and

ends

begins

where

near

uveal

(From

Hogan

MJ,

becomes

broad

JA,

6.6).

of

the

Human

Eye.

Philadelphia:

of

Des-

joins

deep

and

inner

and

outer

wall

and

Weddell

Saunders;

are

JE.

e

of

and

lumen

shape

of

contractile

S chlemm

endothelial

2

zonula

when

7

intraocular

canal

cells,

is

lined

many

of

with

contains

extend

into

a

number

the

of

juxtacana-

the

trabecular

meshwork.

Sondermann)

can

be

ese

fairly

internal

long

to

increase

the

surface

area

of

the

and

canal

endothelium

to

a

sheet

of

is

always

connective

separated

from

the

tra-

tissue.

the

structures

because

this

within

angle

is

the

the

anterior

location

of

chamber

exit

for

angle

is

aqueous

clinically

humor.

must

be

able

to

ow

freely

and

unimpeded

out

of

the

anterior

The

cham-

If

its

exit

a

single

are

is

damage

blocked,

will

occur.

pressure

The

within

width

of

the

the

eye

angle

will

can

be

increase,

and

estimated

ocular

using

bio-

maintain to

determine

whether

the

angle

appears

wide

enough

to

provide

19

increases.

which

by

1971 .)

thought

pressure

canal

that

His-

18

patency

endo-

COMMENT : Gonioscopy

of

microscopy

its

Schlemm

pouches,

(of

ser ve

eir

state

tissue

the

the

con-

ber.

connect

toward

space

aqueous

tology

as

eyes.

transition

termination

meshwork

Alvarado

decreased

glaucomatous

within

important

corneolimbus.

in

the

The

cemet

of

blind

channels

CLINICAL

zone

sti

corneoscleral

terminates

endothelium

endothelium

more

wall

or

tissue

becular meshwork

are

of

paracellu-

the

(Fig. scleral

and

process

iris

branching scleral

the

and

uveal

collector meshwork

valves

during

transcellular

just

An

the

one-way

deform

B oth

they

end

licular process

cells

formation.

21

thelial

evaginations,

posterior

endothelial

pore

e

arise

as

transcellular

easy

layer

joined

by

access

wide

the

to

enough

anterior

the

or

if

trabecular

there

chamber

is

meshwork.

concern

angle

that

structures

If

the

aqueous

is

angle

exit

does

is

not

appear

inadequate,

a

to

view

be

of

necessary.

20–22

occludens.

e

endothelial

cells

have

an

incomA

direct

view

of

the

anterior

chamber

angle

cannot

be

achieved

because

plete basement membrane b etween the canal and the juxtacanthe 2

alicular

5

limbus

sels,

it

by

tight

whereas

similar

lateral

to

walls

e

continuous

junctions

the

makes

endothelial

the

discontinuous

lymph

of

opaque.

Light

directed

obliquely

through

the

cornea

into

the

23

tissue.

lining

with

cells angle

joined

is

the

channels.

cells

of

similar

basement

e

the

canal

tight

inner

blood

membrane

junctions

wall

to

restrict

ves-

makes

between

ow

into

the

the

does

performed

The

exit

using

gonioscopy

anterior

or

not

she

a

facing

special

lens

chamber

is

because

lens

contains

angle

the

of

(Fig.

angle

total

that

internal

overcomes

mirrors

6.7).

and

reection.

The

that

allow

image

sighting

the

the

along

total

the

Gonioscopy

internal

examiner

examiner

the

anterior

be

reection.

to

sees

can

view

is

as

surface

if

of

the

he

the

CHAPTER

Fig.

6.6

lumen

Drawing

of

irregular,

along

with

the

between

arises

(Fig.

6.8A).

If

inner

the

near

the

men

from

all

structures

and

outpouchings.

external

JE.

can

be

and

canal

the

trabecular

cells

often

Histology

seen,

they

wall

the

spaces.

the

appear

bet ween

Eye.

beginning

at

the

posterior

aspect:

iris

root,

ciliary

body,

channel,

(gv)

(ew)

is

(ts).

are

and

trabecular

trabecular

adjacent

Philadelphia:

seen

and Vitreous

adjacent

of

the

in

shown. The

An

surrounded

internal

a

wall

sheets

sheets.

(a)

(cst)

ver y

cells

internal

wall

wall

(iw)

channel

where

that

it

is

its

frequently,

Hogan

MJ,

lies

(icc)

lost.

separates

branch

(From

Saunders;

is

endothelial

collector

meshwork,

by

tissues. The

inner

the

85

Humor s

As

lu-

and

Alvarado

1971 .)

following

anterior

order,

Aqueous

Endothelium

space

the

is

Corneoscleral

bridges

the

canal

into

channel

(e).

vacuoles

trabecular

extends

Human

in

Giant

Schlemm

collector

form

of

of

and

collector

endothelium

nearest

wall

internal

by

internal

folds

posterior

lined

an

is

canal,

endothelial

canal,

(sc)

wall. The

adjacent

Weddell

Schlemm

canal

endothelium

Schlemm

JA,

iris

many

with

their

of

Schlemm

6

scleral

chamber

through

the

pupil

(Fig.

6.10).

In

the

anterior

spur,

chamber, the aqueous circulates in convection currents, moving trabecular

meshwork,

and

Schwalbe

line

(Fig.

6.8B).

Schlemm

canal

lies

down behind

the

trabecular

meshwork

in

this

view

and

is

generally

not

along

exiting If

blood

of

the

is

examiner

exerts

episcleral

ocular

In

a

backed

trabecular

veins

into

the

pressure

and

on

causing

canal

(Fig.

the

the

a

thin

6.9).

red

Such

gonioscopy

episcleral

line

can

pooling

lens,

venous

be

of

seen

blood

thereby

in

the

occurs

to

cooler

exceed

the

cornea

peripher y

and

of

up

the

along

the

warmer

iris

and

chamber.

area

if

the

compressing

pressure

through

the

intra-

pressure.

wide-open

seen.

up

meshwork

the

visible.

As

becomes

certain

anterior

peripheral

narrower,

conditions,

interfering

with

iris

and

chamber

tissue

access

cellular

aqueous

angle,

the

approaches

to

debris

the

or

drainage;

entire

the

trabecular

pigment

such

an

trabecular

trabecular

openings

accumulates

occurrence

meshwork

meshwork,

may

be

within

would

can

the

diminished.

the

be

be

angle

In

meshwork,

evident

with

gonioscopy.

AQUEOUS

e

aqueous

oxygen

duced

the

and

in

DYNAMICS

humor

glucose,

the

posterior

pars

provides

to

the

plicata

chamber

of

necessar y

avascular

the

through

ciliar y

the

metabolites,

cornea

body

and

and

epithelium

primarily

lens.

is

It

is

secreted

covering

the

pro-

into

ciliFig.

ar y

processes.

It

passes

between

the

iris

and

lens,

entering

the

6.7

anterior

The gonioscopy lens uses mirrors to direct light into the

chamber

angle.

CHAPTER

86

6

Aqueous

and Vitreous

Humor s

E

D

C

E D

I

C B

A B

A

B

A

Fig.

6.8

The

view

seen

in

gonioscopy

is

the iris to the anterior chamber angle. A,

chamber

majority

angle

of

trabecular

anatomy

aqueous

is

meshwork

as

seen

ltered,

(D),

with

has

if

you

are

pigment ation.

line

COMMENT : Krukenberg

on

the

chamber

posterior

Iris

root

lens

angle

trabecular

(A),

ciliar y

and

looking

anatomy.

B,

meshwork,

body

(B),

across

Anterior

where

scleral

spur

the

(C),

(E).

the CLINICAL

standing

anterior

gonioscopy. The

mild

Schwalbe

as

Histological

ciliar y

muscle

bundles,

and

then

into

the

supraciliar y

and

Spindle

suprachoroidal spaces. From there, the uid exits by three methKrukenberg

spindle

is

a

characteristic

vertical

pattern

of

pigment

on

the

pos-

ods: terior

cornea

associated

with

pigmentary

dispersion

syndrome.

In

it

moves

vasculature; dispersion

friction

syndrome,

causes

the

pigment

iris

bows

liberated

posteriorly

from

the

rubbing

posterior

iris

on

to

the

zonules.

enter

through

the

sclera

to

be

absorbed

into

the

orbital

pigmentary

the

it

is

absorbed

into

the

choroid

where

it

drains

into

This

the

aqueous

anterior

ciliar y

veins

and

vortex

veins;

and

it

drains

through

26,30

in

the

posterior

chamber

and

chamber.

forms

the

The

pigment

characteristic

follows

vertical

the

aqueous

pattern

along

into

the

the

lymphatic

anterior

corneal

e

endo-

channels

second

within

avenue

the

ciliar y

through

stroma.

which

aqueous

exits

the

ante-

25

thelium because of the convection currents in the anterior chamber (Fig. 6.11).

Pigmentary

dispersion

syndrome

can

result

in

glaucoma

as

the

pigment

rior chamber, the conventional outow pathway, uses a pressure

accu-

driven

system

to

maintain

steady

intraocular

pressure.

Here,

mulates in the trabecular meshwork causing loss of trabecular meshwork endo-

aqueous

thelial

cells

and

decreased

outow

moves

through

narrower

pores

juxtacanalicular

ere

are

two

e

accounts

for

avenues

by

which

unconventional

5%

to

60%

uveal

trabecular

meshwork,

into

channels.

the

chamber.

the

of

or

the

aqueous

uveoscleral

total

exits

the

outow

outow,

and

anterior

pathway

decreases

canal,

In

the

and

into

the

tissue

wall

corneoscleral

and

Schlemm

histological

inner

of

endothelial

lining

through

of

the

Schlemm

canal.

sections,

of

the

meshwork,

many

Schlemm

of

canal

the

have

endothelial

been

cells

found

to

lining

contain

3,26–29

with

lar

age.

Here

meshwork,

aqueous

into

the

passes

through

connective

tissue

the

uveal

spaces

trabecu-

surrounding

E D

I

C B

A

Fig.

6.10

ciliar y

Fig.

6.9

When

Schlemm

pinkish

ular

blood

canal,

hue.

Iris

meshwork

the

root

(D),

backs

up

posterior

(A),

ciliar y

Schwalbe

from

the

trabecular

body

line

(B),

(E),

episcleral

veins

meshwork

scleral

Schlemm

spur

takes

(C),

canal

into

on

a

trabec-

(arrow).

through

the

Flow

of

processes,

the

pupil,

trabecular

episcleral

and

(From

ed

2.

humor.

out

ows

meshwork

veins.

Pharmacology,

aqueous

moves

out

into

of

the

the

JD,

is

formed

cr yst alline

anterior

Schlemm

Bartlett

Boston:

Aqueous

around

chamber

canal

Jaanus

and

SD.

the

and

through

then

Clinical

Butter worth-Heinemann;

in

lens

to

the

Ocular

1989.)

CHAPTER

Factors

e

pressure

tissue

the

must

and

is

small

be

kept

e

way.

are

at

a

level

the

in

that

a

can

that

in

and

within

is

of

the

not

Most

impeded

at

range

to

by

and

preser ve

ocular

the

the

this

or

helps

com-

rate

of

balance,

the

exit

can

pressure.

Production

increased

intraocular

outow.

various

the

carries

Intraocular

detrimental

aqueous

through

eye.

production

of

and

aqueous

production

cases

be

of

the

small

intraocular

decreased

cornea

volume

normally

by

exits

lens

fairly

rate

either

changes

the

pressure

within

constant.

outow

to

87

Humor s

Pressure

constant

mechanisms

caused

Aqueous

a

between

variations

fairly

pressure

and

maintained

signicant

remains

nutrients

intraocular

Homeostatic

cause

and Vitreous

Intraocular

away,

equilibrium

exit.

but

carries

products

maintain

plex

Aqueous

Affecting

aqueous

waste

to

6

sites

ciliar y

along

body

the

(the

path-

uncon-

ventional outow) passes into the ciliar y body from the anterior

chamber

into

the

either

ciliar y

covering

Fig.

6.11

Krukenberg

spindle

in

a

patient

with

pigment

disper -

and

the

thus

sion syndrome showing the vertical orientation of the pigment

e

on

aected

through

body.

ciliar y

the

tissue

uveoscleral

the

ere

body

oers

outow

uveoscleral

is

no

as

it

borders

little

is

meshwork

continuous

the

resistance

believed

to

layer

be

or

of

anterior

to

directly

epithelium

chamber

aqueous

fairly

passage.

constant

and

not

29,45

the

posterior

corneal

endothelium.

by

ere

the

is

intraocular

greater

anterior

pressure.

variability

chamber

via

in

the

the

amount

conventional

of

aqueous

pathway

exiting

compared

22–24,31–33

giant

vacuoles,

some

of

which

exhibit

openings

into

the

with

the

unconventional

pathway.

Resistance

in

this

outow

8,34,35

lumen.

e

transient,

means

the

the

vacuoles

transcellular,

for

endothelial

An

and

large

gradually

intermittently,

channels

molecules,

indentation

cell,

close

unidirectional

transporting

endothelium.

open

such

forms

in

enlarges,

as

the

and

that

creating

provide

proteins,

basal

a

across

surface

eventually

of

opens

pathway

increase

to

is

major

passage

unless

pores,

factor

intraocular

aqueous

work

a

there

the

pressure.

through

pigment

are

in

or

ere

the

is

of

has

aqueous

normally

sheets

debris

decreased

rate

of

the

exit

little

and

trabecular

accumulated

can

resistance

mesh-

within

trabecular

meshwork

cells,

or

trabecular

meshwork

bers.

the

there

3

onto

the

apical

surface.

en

the

cytoplasm

in

the

basal

aspect

are

adhesions

between

the

When

36

of

the

cell

moves

throughout

the

to

occlude

the

endothelium

opening.

is

e

uncertain

number

because

of

some

pores

may

be

Schlemm

tance

to

canal

is

wide

outow ;

open,

however,

it

as

also

provides

intraocular

little

to

pressure

no

resis-

increases,

37

artifacts

caused

by

tissue

preparation.

Smaller

pinocytic

ves-

Schlemm

canal

narrows

and

focal

areas

of

the

canal

can

col-

1,3,46

icles

the

also

provide

greatest

Schlemm

a

transport

volume

canal.

of

system

aqueous

Tight

for

humor

intercellular

substances.

diuses

junctions

However,

passively

may

into

respond

lapse.

in

e

those

to

spur

pharmacological

with

collapse

with

which

of

glaucoma,

is

unable

Schlemm

perhaps

to

canal

because

maintain

canal

is

of

more

a

prevalent

shorter

patenc y

in

scleral

the

eye

1

changing

physiologic

conditions

(i.e.,

eects

of

glaucoma.

e

external

collector

channels

and

aqueous

16

agents)

by

modifying

their

permeability

and

increasing

the

ease

veins

normally

provide

negligible

resistance.

e

location

of

7,22

by

of

which

the

aqueous

trabecular

ows

into

meshwork

the

may

canal.

e

actually

endothelial

release

cellular

cells

factors

the

highest

region

of

resistance

the

to

aqueous

juxtacanalicular

movement

tissue

and

the

seems

to

be

endothelium

in

the

of

the

14,16,47,48

that

can

increase

the

permeability

of

the

inner

wall

of

Schlemm

inner

wall

of

Schlemm

canal.

Plaque-like

material

that

38

canal.

accumulates

e

endothelial

cells

lining

the

external

wall

of

Schlemm

area

vacuoles.

ow

either

in

the

directly

extracellular

or

indirectly

matrix

of

increases

the

juxtacanalicular

resistance

in

the

out-

47

canal

are

joined

Approximately

tributed

by

25

around

zonula

to

the

37

occludens

external

outer

wall

of

and

contain

collector

no

channels

Schlemm

canal

are

and

dis-

branch

pathway.

meshwork

speculated

In

and

to

the

the

have

normal

cells

eye,

within

some

the

the

cells

of

the

juxtacanalicular

self-regulating

ability

that

trabecular

tissue

can

are

inu-

14,49,50

from

it

to

empty

into

the

deep

scleral

plexus

and

then

intra-

ence

changes

veins.

Sustained

in

resistance

and

thus

intraocular

pressure.

6,39,40

scleral

plexus,

Occasionally,

which

aqueous

in

turn

veins

drain

(of

into

Ascher)

the

episcleral

which

pass

aqueous

directly from the collector channel lumen to episcleral veins, are

visible

with

biomicroscopy

as

a

pulse

of

aqueous

followed

by

a

ocular

resistance

to

outow

usually

results

in

elevated

intra-

pressure.

Because

muscle

tendons

connect

of

with

the

the

longitudinal

contractile

portion

bers

of

of

the

the

ciliar y

trabecular

41,42

bolus

there

of

blood

are

along

more

the

vessel.

external

Schlemm

collector

channels

canal

is

larger

nasally

and

compared

meshwork

tion

can

and

alter

juxtacanalicular

the

geometr y

of

tissue,

the

ciliar y

trabeculum

muscle

by

contrac-

widening

the

43

with

temporally.

In

addition,

the

number

of

open

external

col-

spaces between the sheets, resulting in a decrease in outow resis-

17

lector

channels

increases

with

an

increase

in

intraocular

44

sure

in

normal

eyes

but

not

in

those

with

glaucoma.

pres-

tance.

Schlemm

canal

diameter

increases

with

accommoda-

51

tion.

Pharmacologically,

increasing

ciliar y

muscle

contraction

CHAPTER

88

decreases

6

Aqueous

unconventional

outow

and Vitreous

whereas

Humor s

cycloplegic

agents probe can contact the cornea. The force required to cause applanation of a given

26

increase

unconventional

outow.

Parasympatholytic

medicaarea

tions

are

associated

with

a

reduction

in

the

area

of

of

the

corneal

surface

gives

an

estimate

of

the

pressure

within

the

eye.

Schlemm Intraocular pressure is only one of the clinical ndings that aids in the diagnosis

52

canal

It

[F

and

is

])

this

may

important

is

equal

to

be

a

that

the

cause

the

of

reduced

amount

amount

that

of

outow.

aqueous

exits

the

of glaucoma. The appearance of the optic nerve head and the retinal nerve ber

formed

eye

(ow

(ow

out

[F

in

layer

is

assessed,

and

the

visual

eld

is

examined

for

defects.

])

out

and

can

be

represented

as

F

=

F

in

between

in

in

exit.

the

As

factors

discussed

in

.

is

represents

a

balance

out

aecting

production

Chapter

5,

and

aqueous

those

involved

production

(F

)

CLINICAL

is

Glaucoma

COMMENT : Glaucoma

is

a

complex

disease

process

that

is

not

completely

understood.

in

Many

dependent on molecules moving out of the ciliar y body capillar-

ies

and

out

through

of

the

the

blood

ciliar y

vessels

stroma

occurs

and

epithelium.

because

the

Increased

Movement

pressure

ber

within

ing

the

ciliar y

body

capillaries

(P

)

CB

is

greater

than

the

patients

the

eye,

the

intraocular

glaucoma

intraocular

layer,

blood

either

pressure

directly

perfusion.

have

In

by

can

higher

than

contribute

mechanical

normotensive

normal

to

damage

pressure

glaucoma,

intraocular

or

of

the

indirectly

retinal

nerve

pressure.

retinal

through

bers

nerve

imped-

are

dam-

pressure

caps

aged,

within

with

pressure

(IOP),

and

can

be

but

intraocular

pressure

measurements

are

normal

or

even

low.

In

these

repcases,

the

likely

cause

is

a

decrease

of

perfusion

pressure

in

the

retinal

tissue

45

resented

as

(P

−

CB

IOP).

e

ease

with

which

the

molecules

caps

resulting

pass

through

tissue

is

called

facility

and

will

be

(C

).

Facility

is

the

reciprocal

of

resistance,

as

the

facility

decreases.

e

nal

factor

in

evident

aqueous

is

the

rate

at

which

energ y-utilizing

pumps

metabolites

and

cell

death.

Retinal

nerve

ber

layer

loss

at

the

optic

disc

and

can

cause

enlargement

and

deepening

is

of

physiological

cup.

produc-

Increased

tion

of

resistance

in

increases,

loss

represented most

as

in

actively

intraocular

pressure

associated

with

glaucoma

generally

occurs

move

because

of

increased

resistance

within

the

conventional

outow

pathway,

material toward secretion into the posterior chamber and is des17

often

involving

the

juxtacanalicular

tissue

or

inner

wall

of

Schlemm

canal.

45

ignated

as

(S).

us

F

=

(P

in

−

CB

IOP)

C

caps

+

S.

S

is

generally

in

Proliferation

considered

to

be

a

constant.

e

other

factors

might

of

the

juxtacanalicular

tissue

increases

with

age

and

has

been

uctuate. 6

Flow

out

outow.

includes

Flow

from

both

conventional

Schlemm

canal

into

and

the

found

to

cause

ocular

tissue

a

decrease

in

outow.

Some

histological

preparations

of

unconventional

episcleral

veins

from

glaucomatous

eyes

give

evidence

for

a

decrease

in

outow.

is A reduction in the cross-sectional diameter of Schlemm canal and fewer pores

45

represented

as

(IOP

−

P

),

and

the

ease

with

which

the

aque-

in

the

endothelial

lining

of

the

canal

were

found

in

glaucomatous

eyes

when

ev

44

ous

moves

canal

is

through

the

facility,

the

trabecular

represented

meshwork

by

(C

).

e

and

into

small

Schlemm

amount

compared

lar

that

with

normal

component

of

the

53

54

eyes.

Other

matrix

in

the

studies

show

an

juxtacanalicular

increase

tissue

in

in

the

bril-

glaucomatous

out

48

exits

and

through

is

the

generally

F

=

F

in

=

(

out

uveoscleral

fairly

is

represented

by

eyes.

(U)

− IOP caps

)

Deposits

restrict

constant.

P CB

meshwork

C

+ S =

in

(

IOP − P ev

)C

+

this

equation

is

an

oversimplication,

it

pigment

ow

or

through

debris

the

on

the

trabecular

trabecular

sheets

and

cords

can

spaces.

U

out

Drugs

Although

of

aqueous

does

give

an

that

Glaucoma

indication of the factors to be considered and their interdependence.

lar

It represents the steady state of homeostasis, and in the normal eye,

tion

pressure

or

Reduce

treatment

using

increase

Intraocular

consists

drugs

of

that

aqueous

Pressure

attempts

either

outow.

to

decrease

One

of

the

reduce

intraocu-

aqueous

earliest

produc-

treatment

45

only

small

uctuations

occur

throughout

the

day.

e

amount

of

plans

involved

aqueous produced usually does not change appreciably, so when the

causes

steady

changing

mised

state

and

is

an

disrupted,

elevation

it

of

is

usually

the

intraocular

outow

pressure

that

is

follows.

compro-

If

aqueous

tate

sheets.

(thus

was

a

decrease

is

in

likely

facility).

to

be

the

e

major

location

juxtacanalicular

tissue

of

the

increased

between

the

last

trabecular sheet and the inner wall of Schlemm canal.

Small

small

uctuations

eect

on

the

in

intraocular

egress

of

aqueous

pressure

from

the

might

the

use

and

of

pilocarpine,

sphincter

and

conguration

perhaps

Pilocarpine

oen

miosis

the

iris

outow,

exit is compromised, it is usually because of an increase in resistance

resistance

the

poor

by

was

of

the

allowing

of

the

cholinergic

muscle

to

trabecular

more

commonly

because

ciliar y

a

ciliar y

sheets

separation

used;

agonist,

contract,

however,

uncomfortable

to

that

thus

facili-

between

the

compliance

side

eects—

spasm.

Most drugs that inhibit aqueous production act on the ciliar y

have

ciliar y

some

processes,

epithelia,

iting

either

by

intracellular

interfering

enzymes

with

that

neural

pathways

maintain

the

or

ionic

by

inhib-

transport

55

but

this

is

usually

negligible.

mechanisms

important

the

sympathetic

is CLINICAL

COMMENT : Measurement

of

Intraocular

role

unclear,

pressure

can

be

estimated

clinically

with

a

tonometer.

eter and the Goldmann applanation tonometer. Intraocular pressure is measured

millimeters

of

mercury

(mm

Hg)

and

a

reading

between

10

formation

inner vation

beta-blockers

and

of

in

aqueous.

aqueous

alpha2-adrenergic

Although

production

and

21

aqueous

production,

perhaps

by

agonists

interfering

with

do

cili-

Common

instruments used to measure the intraocular pressure are the noncontact tonom-

in

the

Pressure

decrease Intraocular

of

in

mm

Hg

is

ar y

epithelial

such

as

function.

brimonidine,

aqueous

production

by

Drugs

an

that

have

vasoconstrictive

alpha2-adrenergic

decreasing

blood

ow

agonist,

in

the

action,

decrease

ciliar y

ves-

55,56

considered normal. Readings in the low to mid 20s may be suspect, and intraoc-

ular pressure measurements in the upper 20s or higher require close monitoring.

The

noncontact

tonometer

(also

called

the

air-puff

tonometer)

detects

the

sels,

causing

Brimonidine

to

applanate

the

cornea

by

a

rapid

pulse

of

air.

When

reduction

also

in

increases

oxygen

availability

uveoscleral

outow.

to

the

tissue.

Carbonic

anhy-

force

drase

necessary

a

inhibitors

are

also

common

in

glaucoma

treatment.

ey

performing

decrease

aqueous

production

by

inhibiting

key

enzymes

Goldmann applanation tonometry a topical anesthetic must be instilled so that a

sar y

for

ionic

transport

across

the

epithelial

layers.

neces-

CHAPTER

Currently,

ment

ance

are

is

the

most

eective

prostaglandins.

good

because

Prostaglandins

drugs

ey

are

instillation

enhance

is

outow

used

well

in

glaucoma

tolerated

necessar y

through

and

only

the

once

treat-

density

compli-

lular

per

in

uveoscleral

day.

path-

and

6

size

matrix

lumen

Aqueous

of

giant

plaques

diameter

outow

resistance

the

in

of

in

and Vitreous

vacuoles,

the

accumulation

juxtacanalicular

Schlemm

the

an

canal,

vicinity

of

and

the

which

sue

and

causes remodeling of the extracellular matrix within the connec-

by

inducing

the

synthesis

of

matrix

metalloproteases

the

amount

inner

of

tive

the

cause

the

wall

of

Schlemm

connective

tissue

an

the

extracel-

a

decrease

increase

in

the

tis-

67–69

canal.

in

of

tissue,

juxtacanalicular

16

way

89

Humor s

An

ciliar y

increase

muscle

may

in

be

29

tissue

between

muscle

bundles.

is

remodeling

increases

the spacing between muscle bundles, which increases tissue per-

17

meability

and

aqueous

28

29

50

pressure

of

reduction

increases

about

57–59

in

1

uveoscleral

mm

Hg

per

analogues

meshwork

may

also

Certain

pathway,

increase

possibly

by

outow

Intraocular

of

age

in

those

70

outow.

prostaglan-

of

African

descent

but

does

not

63

din

outow.

decade

through

expanding

the

the

size

trabecular

of

Schlemm

decreases

of

in

the

Caucasians

Asian

have

change

no

paradoxically

71

population.

found

or

Although

change

or

even

some

lowered

studies

intraocu-

72

canal,

degrading

the

trabecular

meshwork

extracellular

matrix

60

by

matrix

metalloproteases,

or

modulating

cytokine

lar

pressure

levels.

cant,

but

not

73

Rho

ing

kinase

resistance

through

inhibitors

through

multiple

increase

the

aqueous

conventional

mechanisms,

outow

by

pathway.

including

decreas-

is

aecting

with

likely

the

along

Schlemm

extracellular

matrix,

17

becular

ness

20

the

cells

of

decreasing

widening

ese

trabecular

endothelial

thus

and

the

a

statistically

increase

in

signi-

intraocular

74

occurs

production

spaces

in

the

CHAMBER

of

medications

meshwork,

Schlemm

decrease

juxtacanalicular

canal

by

the

tra-

sti-

e posterior chamber is an annular area located behind the iris

tissue,

reducing

and

contractile

and

bounded

ciliar y

processes

posterior

COMMENT : Increased

Intraocular

Pressure

by

the

posterior

iris

surface,

the

equatorial

zone

of

the lens, the anterior face of the vitreous, and the ciliar y body. e

limiting

Steroid

found

intercellular

properties.

CLINICAL

have

signicant,

62

meshwork.

of

canal

others

clinically

pressure.

POSTERIOR junctions

age,

61

that

chamber.

membrane

ar y

body,

the

lens

pass

secrete

e

of

the

through

the

aqueous

zonule

bers

humor

arise

nonpigmented

the

posterior

project

from

the

epithelium

chamber,

and

of

into

the

internal

the

insert

cili-

into

With

capsule.

e

posterior

chamber

contains

two

regions:

Use

the area occupied by the zonules is the canal of Hannover, and the Use

of

corticosteroids

can

increase

intraocular

pressure.

This

is

thought

to

retrozonular occur

by

activating

the

Rho

kinase

pathway,

causing

resistance

to

space,

the

area

from

the

most

posterior

zonules

to

aqueous

the vitreal face, is the canal of Petit (Fig. 6.12). e canal of Petit outow

by

increasing

the

stiffness

of

the

endothelial

cells

surrounding

21

Schlemm

CLINICAL

Surgical

might

20

canal

and

increasing

production

COMMENT : Surgical

procedures

may

be

used

as

of

the

extracellular

Treatment

the

initial

of

be

better

Glaucoma

glaucoma

described

as

a

potential

Canal

treatment,

but

of

Petit

they

Canal

are

particularly

ment,

the

tions,

or

logical

if

nerve

surgeries

more

ber

include

efcient

the

patient

layer

to

damage

stents

or

access

to

shunt

compliant

side

even

the

which

opening

channels,

the

topical

vigorous

small

laser

the

or

dilate

Hannover

pharmaco-

in

the

glaucoma

aqueous

Schlemm

of

treat-

medica-

holes

Microinvasive

allow

of

recommended

from

with

making

movement.

devices

collector

with

effects

continues

uid

enlarge

the

not

involves

increase

meshwork,

is

signicant

Trabeculoplasty

meshwork

trabecular

if

experiences

treatment.

trabecular

the

useful

patient

space.

matrix.

to

canal

collector

bypass

allowing

channel

openings. In trabeculectomy, a wedge of trabecular meshwork is removed, and

a

scleral

ap

is

formed

so

that

aqueous

can

percolate

through

the

trabecular

opening and accumulate beneath the ap to be absorbed into episcleral tissue.

Endoscopic

laser

to

AGING

With

cyclophotocoagulation

damage

of

the

CHANGES

age,

anterior

tissue

the

anterior

chamber

reduces

ciliary

IN

THE

chamber

volume

aqueous

production

by

applying

a

processes.

ANTERIOR

angle

decreases,

width

probably

CHAMBER

narrows

and

secondar y

to

the

lens

63,64

growth.

is

Asians

may

and

narrowing

be

related

is

to

more

the

signicant

higher

in

incidence

women

of

and

angle-clo-

65,66

sure

glaucoma

in

these

patients.

Other age-related changes include a decrease in aqueous pro-

duction,

a

reduction

in

uveoscleral

outow,

a

decrease

in

the

Fig.

6.12

Regions

of

the

posterior

chamber.

90

CHAPTER

6

Aqueous

VITREOUS

CHAMBER

and Vitreous

Humor s

embedded

mented

rmly

in

epithelium

the

of

basement

the

ciliar y

membrane

body

and

the

of

the

nonpig-

internal

limiting

75

e vitreous chamber is lled with the transparent gel-like vitreous

membrane

body and occupies the largest portion of the globe. It is bounded in

the

front

portion

by

of

the

the

posterior

posterior

surface

of

chamber.

the

lens

and

Peripherally

the

and

retrozonular

moving

poste-

e

tal

8

of

the

hyaloideocapsular

ligament,

to

9

peripheral

mm

in

forms

an

retina.

ligament

annular

diameter

(of

Weiger),

attachment

between

the

1

to

posterior

2

or

retrolen-

mm

surface

wide

of

and

the

lens

76

riorly, it is bounded by the pars plana of the ciliary body, the retina,

and

and

site

the

optic

disc.

All

surfaces

that

interface

with

the

vitreous

are

the

in

anterior

young

face

of

persons,

the

but

vitreous.

the

is

strength

of

is

a

the

rm

attachment

bond

diminishes

77

basement

the

membranes.

patellar

fossa,

an

e

center

indentation

of

in

the

anterior

which

the

surface

lens

sits.

contains

e

vitre-

ous makes up about 80% of the entire volume of the eye.

aer

a

age

35

years.

potential

present

space,

because

Within

the

the

the

ring

retrolental

lens

and

formed

space

vitreous

by

(of

are

this

ligament

Berger),

which

juxtaposed

but

is

is

not

78

joined.

Vitreous

e

Attachments

vitreous

tures.

e

forms

e

several

strongest

of

attachments

these

is

the

to

surrounding

vitreous

base,

struc-

located

at

also

peripapillar y

diminishes

macula

is

3

to

adhesion

with

4

age.

mm

in

e

around

the

annular

diameter

edge

ring

and

is

of

of

the

optic

attachment

most

adherent

disc

at

the

in

the

75

the

ora

serrata.

strength)

are

e

to

the

other

attachments

posterior

lens,

the

(in

order

optic

of

disc,

decreasing

the

macular

fovea.

e

attachment

of

the

vitreous

to

retinal

blood

vessels

consists of ne strands that extend through the internal limiting

79,80

area,

and

e

the

1

vessels.

vitreous

ora

rata,

retinal

serrata.

to

3

75

base,

It

mm

membrane

the

extends

posterior

most

1.5

to

to

it,

extensive

2

mm

and

adhesion,

anterior

several

to

straddles

the

millimeters

ora

ser-

into

the

base

are

ese

there

to

branch

strands

is

may

vitreal

e

nature

and

traction

of

surround

account

the

on

for

the

the

larger

retinal

hemorrhages

that

vessels.

occur

when

retina.

attachment

between

the

vitreous

and

the

76

vitreous

(Fig.

6.13).

e

vitreal

bers

that

form

the

retinal

internal

retina

remains

terior

vitreous

limiting

membrane

uncertain.

It

is

throughout

unlikely

that

the

brils

rest

from

of

the

the

pos-

81–83

insert

Rather

the

linking

the

of

internal

into

vitreoretinal

outer

part

of

the

internal

interface

the

limiting

contains

vitreous

a

cortex

membrane.

molecular

and

the

glue

inner

part

75,84,85

the

extracellular

tin,

heparan

limiting

membrane.

matrix—molecules,

sulphate,

and

is

including

opticin,

that

area

contains

laminin,

have

been

bronec-

identied

as

77,86,87

having

adhesive

During

properties.

early

childhood

(as

early

as

age

3

years),

a

liquied

88,89

pocket

is

develops

bounded

by

anterior

the

to

vitreous

the

macula

cortex

(Fig.

6.14).

posteriorly

and

is

area

vitreous

gel

88–90

anteriorly.

Vitreous

bers

arise

tangential

to

the

vitreous

91

cortex

cal

to

wrap

vitreous

associated

anatomic

cortical

around

pockets,

with

the

also

known

age-related

development.

vitreous

pocket

A

pocket.

ese

as

liquefaction

septum

with

posterior

premacular

but

connects

Cloquet

canal

are

part

the

(see

precorti-

bursa,

of

are

posterior

Fig.

not

normal

pre-

6.14),

but

bur sa

(B)

B

A

C

Fig. 6.13

Vitreous relationships in the anterior eye. The ora serrata

(1)

termination

is

the

for ward

approximately

gion

is

ciliary

to

the

of

approximately

4

mm

oriented

body,

inner

at

but

a

the

2

over

of

over

the

right

the

The

the

over

to

the

the

ciliar y

vitreous

ciliar y

peripheral

angle

anteriorly,

surface

retina.

mm

retina.

pars

(2)

and

plana,

of

it

the

is

extends

posteriorly

Collagen

surface

body. The

base

body

in

more

posterior

this

retina

re-

and

parallel

hyaloid

(4)

is

adjacent to the retina and the anterior hyaloid (3) is near the zonules

and

lens.

space

of

Histology

Also

depicted

Berger

of

the

(6).

are

(From

Human

the

hyaloideocapsular

Hogan

Eye.

MJ,

Alvarado

Philadelphia:

ligament

JA,

Saunders;

(5)

Weddell

1971 .)

and

JE.

Fig.

with

6.14

A

septum

Cloquet

canal

(A)

(C).

connects

the

premacular

CHAPTER

there are liquied channels connecting the two in 30% to 93% of

e

6

Aqueous

prepapillar y

hole

and Vitreous

can

sometimes

91

Humor s

be

seen

clinically

when

90,92

eyes.

Although

nections

between

the

the

function

of

posterior

the

lacuna

precortical

is

not

known,

vitreous

con-

pockets

and

the

posterior

canal

may

provide

a

pathway

for

inammator y

mate-

detaches

from

the

retina.

e

premacular

hole is a region of decreased cortex density rather than an actual

76

Cloquet

vitreous

88

92

94

95

hole.

e

prevascular

ssures

provide

the

avenue

by

79

rial

to

play

travel

a

role

in

between

the

the

aqueous

formation

of

and

cystoid

macular

macular

area

and

edema

may

several

e adjacent premacular cortex plays a role in

vitreomacular

ne

bers

enter

the

retina

and

encircle

retinal

vessels.

following

88

cataract surger y.

which

conditions.

Intermediate

e

Zone

intermediate

zone

contains

ne

bers

that

are

continu-

76

ous

and

ese

CLINICAL

At

the

posterior

strong

With

of

cause

wall

attachment

age,

the

connections

tion

COMMENT : Vitreomacular

occur.

all

of

of

posterior

the

cortex

the

which

between

macular

can

precortical

vitreous

starts

to

Vitreomacular

connections

distortion

membrane,

the

between

vitreous

can

these

of

internal

the

occurs

vitreous

a

into

vitreous

from

traction

the

in

and

detach

anatomy,

result

traction

limiting

retina

when

cortex

macular

decreased

pocket,

visual

or

acuity

is

an

or

a

cortex,

(Fig.

at

whereas

the

region

cortex.

the

more

run

of

e

the

93

96

anteroposteriorly.

vitreous

peripheral

central

Membrane-like

condensations,

dierentiated

areas

bers

base

bers

parallel

and

insert

parallel

Cloquet

the

canal.

called

vitreous

tracts,

may

be

94

as

that

have

diering

ber

densities.

contrac-

This

can

Cloquet

Canal

Cloquet

canal,

epiretinal

distortion

also

called

the

hyaloid

channel

or

the

retrolen-

of

tal vision

arise

posterior

that

persistent

macula.

hole,

is

bers

the

and

membrane.

but

there

and

there

unbranched

tract,

is

located

in

the

center

of

the

vitreous

body

(Fig.

6.16).

6.15).

It

has

an

S

shap e,

downward,

tem

Vitreous

Zones

and

formed

Clo quet

is

rotated

the

during

canal

90

former

degrees

site

of

embr yological

aris es

at

the

with

the

the

hyaloid

de velopment

retrolental

space.

Its

center

dip

ar ter y

(s ee

sys-

Ch.

anterior

9).

face

75

e vitreous can be divided into zones that dier in relative den-

is

sity.

are a

e

outermost

zone

is

the

vitreous

cortex,

the

center

zone

approximately

of

head

to

tinuous

solid

cortex

and

whereas

bers

running

surrounds

the

in

central

an

the

center

vitreous

anterior

to

is

canal.

more

posterior

e

uid

cortex

with

is

more

that

extends

with

the

5

a

mm

in

diameter.

funnel-shap ed

for ward

into

the

It

space

terminates

at

vitreous

the

to

at

optic

the

ner ve

b ecome

con-

canal.

collagen

Composition

direction.

e

Vitreous

to

Mar tegiani,

is occupied by Cloquet canal, and the intermediate zone is inner

the

4

Cortex

highly

soluble

e vitreous cortex, also called the hyaloid surface, is the outer

work

of

transparent

proteins,

of

Vitreous

the

and

vitreous

hyaluronic

insoluble

protein,

is

a

acid

dilute

solution

contained

collagen.

e

of

within

vitreous

salts,

a

mesh-

is

98.5%

75

zone

which

surrounds

the

vitreous

gel.

It

is

100

μm

wide,

and

to

99.7%

water

and

has

been

described

as

having

94

it

is

composed

of

tightly

packed

collagen

brils,

some

of

which

tissue

status

and

being

an

extracellular

connective

97

matrix.

B ecause

of

its

93,94

run

parallel

and

e

anterior

some

cortex

perpendicular

lies

anterior

to

to

the

the

base

retinal

and

is

surface.

adjacent

high

to

the ciliar y body, posterior chamber, and lens. e posterior cor-

tex

extends

ina.

It

posterior

contains

to

the

transvitreal

base

and

channels

is

in

that

contact

appear

with

as

the

at

water

tissue

content,

xation

study

oen

of

have

the

vitreous

dehydrating

is

dicult.

eects

that

Attempts

introduce

artifacts.

ret-

holes—the

prepapillar y hole, the premacular hole, and prevascular ssures.

Weiger

Berger

space

ligament

Premacular

brusa

Fovea

Area

(dip)

of

Martegiani

Cloquet

canal

Vitreous

Fig.

6.15

macular

Vitreomacular

hole.

traction

resulting

in

a

full

base

thickness

Fig.

6.16

Vitreous

chamber

anatomy.

CHAPTER

92

6

Aqueous

and Vitreous

Humor s

Physiology

Collagen

e

collagen

base,

next

content

highest

of

the

in

the

in

the

vitreous

posterior

is

highest

cortex,

in

the

vitreous

e

in

the

anterior

support

next

of

vitreous

the

was

Vitreous

thought

surrounding

to

tissues,

merely

but

a

passively

new

interact

understanding

and

of

the

76

cortex,

and

collagen

lowest

brils,

each

8

center.

to

16

nm

A

in

ne

meshwork

diameter,

is

of

uniform

evident

on

elec-

dynamic

largely

vitreous

quiescent

is

developing.

because

e

factors

cells

present

in

in

the

the

cortex

vitreous

remain

prevent

98–100

tron

microscopy

and

lls

the

vitreous

body.

e

individual

cell

migration

density

bril

and

regularity

network

diers

can

be

seen.

throughout

e

the

density

of

vitreous.

that

is,

Most

Hyaluronic

e

second

nan),

a

Acid

(Hyaluronan)

major

vitreal

is

a

long

hyaluronic

unbranched

acid

(hyaluro-

molecule

coiled

into a twisted network. is hydrophilic macromolecule is located

balance

the

network

component,

glycosaminoglycan,

the

of

of

be

in specic sites within the collagen bril network and is believed to

the

into

and

Although

there

and

is

and

is

liquid

hyal-

which

may

reported

little

by

a

become

activity

in

collagen

large

as

state.

widely-spaced

disruption

the

patient

metabolic

viscoelastic

vitreous

the

A

cause

the

the

in

acid.

can

to

of

bound

hyaluronic

complex

bundles,

clinically,

gel

vitreous

acid-collagen

aggregate

visible

between

in

collagen

hyaluronic

to

water

contributes

between

properties of the vitreous and inuences the physical properties,

their

brils

interaction

tions

in

collagen

e

uronic

collagen

and

proliferation.

brils cannot be seen with the slit lamp, but the pattern of varia-

this

acid

and

the

brils

enough

to

oaters.

within

the

vitre-

76

maintain

tein

the

opticin

wide

and

spacing

between

brils.

glycosaminoglycan

In

addition,

chondroitin

the

sulphate

pro-

may

aid

ous,

be

an

intact

quite

vitreous

important

gel,

to

as

occurs

ocular

in

health.

the

younger

With

age,

patient,

there

is

may

a

slow

87,101

in maintaining the spaces between the collagen brils.

e con-

centration of hyaluronic acid is highest in the posterior cortex and

degradation

uefaction

of

the

vitreous

accompany

gel,

several

and

this

degeneration

age-related

ocular

and

diseases,

liq-

such

85,102

decreases

centrally

and

anteriorly.

e

gel

structure

is

a

result

as

nuclear

sclerotic

cataract

and

neovascular

diabetic

retinopa-

of the interaction of collagen and hyaluronic acid. Hyaluronic acid

thy. Studies suggest a correlation between vitreous degeneration

stabilizes the network formed by the collagen strands.

and

an

Vitreous

Cells

Vitreous

cells,

spaced

layer

the

lens

or

in

hyaloc ytes,

the

cortex

are

near

located

and

in

parallel

a

to

single,

the

widely

vitreal

sur-

development

intact

of

may

nuclear

provide

sclerotic

some

cataract,

protection

vitreous

times

has

higher

a

high

than

concentration

blood

plasma)

and

of

that

nuclear

ascorbate

might

have

76,96

a

(up

to

role

in

108

face.

Various

Some

inferring

against

changes.

e

40

vitreous

functions

investigators

have

have

been

determined

attributed

that

these

to

these

cells

cells.

synthesize

the

regulation

diuses

into

of

the

intraocular

vitreous

molecular

from

the

oxygen.

retinal

As

vessels,

it

is

oxygen

likely

to

103–105

hyaluronic

acid.

Others

have

found

evidence

that

hya-

be

consumed

by

ascorbate

before

it

reaches

the

lens

and

ante-

76,106

locytes

Still

synthesize

others

glycoproteins

indicate

that

for

hyalocytes

the

collagen

have

brils.

phagocytic

rior

segment,

proper-

Vitreous

appear-

sumes

gel

providing

has

a

some

higher

protection

concentration

from

of

oxidative

ascorbate

96,105,107

stress.

and

con-

109

ties.

Apparently,

hyalocytes

can

have

dierent

oxygen

at

a

faster

rate

than

liquid

vitreous.

Vitreous

76

ances

in

depending

the

vitreous

on

base

their

are

activity

at

a

given

broblast-like

time.

when

Cells

anterior

to

located

the

ora

loss

caused

by

ease

processes

and

tissue

liquefaction

in

which

or

vitrectomy

excessive

oxygen

can

be

causes

linked

to

oxidative

dis-

stress

81

serrata

and

macrophage-like

Fibroblasts

ous

base

near

composing

blasts

may

believed

present

the

less

ciliar y

than

have

that

in

the

of

and

the

mistaken

broblasts

posterior

vitreous

body

10%

been

when

are

near

the

vitreous

for

synthesize

to

located

optic

cell

in

the

disc.

in

collagen

the

vitre-

Although

population,

hyalocytes

the

it.

bro-

past.

brils

It

that

greater

changes

nuclear

is

run

damage.

e

concentration

within

Another

benet

the

sclerotic

lens

of

lens

nucleus

therefore

aer

be

vitrectomy,

could

increase

exposed

and

the

to

a

oxidative

likelihood

of

cataract.

hypothesis

from

might

oxygen

vitreous

suggests

that

liquefaction

or

there

might

surgical

be

removal

some

of

the

76

anteroposteriorly

Other

cells

and

that

are

have

active

been

in

pathological

identied

as

conditions.

macrophages

vitreous.

likely

Vitreous

molecular

loss

oxygen

may

that

results

benet

in

increased

ischemic

retinal

intraocular

disease

by

low-

75,94

originate

in

the

nearby

retinal

blood

vessels.

ering vascular endothelial growth factor and thus reducing neo-

108

vascularization.

Vitreous

e

in

vitreous

place

only

body

next

to

connected

vitreous

and

Function

is

a

provides

the

to

an

physical

choroid,

each

storage

provides

understanding

as

other

area

avenue

for

for

the

at

support,

neural

the

disc

the

retina

and

metabolites

holding

for

movement

the

the

of

and

ora

the

retina

choroid

serrata.

retina

these

and

become

lens

substances

In

the

body.

acts

shock

absorber,

protecting

the

fragile

retinal

tissue

importance

relationship

evident

Age-Related

ume

a

its

as

studies

of

the

with

vitreous

and

neighboring

a

better

tissues

will

continue.

are

e

within the eye. e vitreous, because of its viscoelastic properties,

as

more

e

of

infant,

With

Vitreous

the

maturation,

decreases

and

the

dur-

vitreous

liquefaction

ing rapid eye movements and strenuous physical activity. e vit-

vitreous

is

reous

50%

80%

gel

Changes

vitreous

liquid

or

and

is

a

ver y

changes

volume

synchisis

20%

homogeneous,

occur

in

increases;

senilis.

liquid,

which

and

By

by

age

70

or

the

this

40

80

gel-like

gel

is

vol-

called

years,

years

the

it

is

93

transmits

and

refracts

light,

aiding

in

focusing

the

rays

on

liquid.

Most

of

the

liquefaction

occurs

in

the

central

vit-

94

the retina. Minimal light scattering occurs in the vitreous because

reous.

of

tally

its

lar

extremely

spacing

low

ensured

concentration

by

the

of

particles

hyaluronic

and

the

acid-collagen

interbril-

complex.

in

Both

aected

the

hyaluronic

by

free

hyaluronic

acid

radicals

acid

and

that

collagen

cause

molecule

and

may

be

detrimen-

conformational

breakdown

in

changes

collagen

CHAPTER

4.

Kelley

6

Aqueous

MJ,

Rose

meshwork:

AY ,

present

and Vitreous

Keller

and

KE,

future

etal.

93

Humor s

Stem

promises.

cells

Exp

in

the

Eye

trabecular

Res.

2009;88:

747–751.

5.

War wick

Orbit.

6.

R.

7th

Eyeball.

ed.

Lütjen-Drecoll

trabecular

Lippincott;

Bhatt

K,

G,

the

Fig.

6.17

Posterior

vitreous

detachment.

9.

of

Park

two

crosslinks.

Subsequent

displacement

of

collagen

from

the

acid-collagen

network

inuences

the

change

from

Anatomy

Functional

Tasman

W ,

of

the

Eye

and

1976:30–180.

morpholog y

Jaeger

Ophthalmolog y,

vol

EA,

1.

eds.

of

the

Duane’s

Philadelphia:

Freddo

Sci.

in

and

photon

monkey

JK,

canal

the

studies

human

Invest

MY ,

of

of

eye.

aqueous

Schlemm.

in

the

inter-

Invest

the

in

the

freeze-fracture

Vis

Revisiting

with

microscopic

A

sclerocorneal

Ophthalmol

etal.

connections

excitation

route

of

junctions

eye.

Kahook

their

of

Paracellular

endothelial

Lee

Freeze-fracture

angle

1995;36(7):1379.

E.

meshwork

and

TF .

the

Sci.

ciliar y

trabecular

imaging.

angle

of

1981;21:52.

muscle

meshwork

Invest

by

Ophthalmol

hyalVis

uronic

F ,

Vis

the

CY ,

Wol ’s

Saunders;

JW .

In:

Clinical

junctions

macaque

tendons

Rohen

R aviola

trabecular

study

of

Gong

Ophthalmol

R aviola

Eugene

1994:1.

endothelial

8.

E,

meshwork.

Foundations

7.

In:

Philadelphia:

gel

Sci.

2016;57:1096–1105.

to 10.

Epstein

DL,

Rohen

JW .

Morpholog y

of

the

trabecular

meshwork

110–112

liquid.

As

complex

occurs,

network,

112

the

causing

e

to

dissolution

of

the

macromolecule

the

brils

to

hyaluronic

moves

coalesce

into

out

acid-collagen

of

bers

the

and

and

collagen

then

into

the

11.

113

bands.

cent

the

these

redistribution

bundles,

of

allowing

collagen

pooling

of

leaves

liquid

spaces

adja-

vitreous;

monkey

Inomata

H,

through

the

in

these

inner-wall

the

endothelium

eye.

Bill

Invest

A,

cationized

Ophthalmol

Smelser

trabecular

cynomolgus

aer

GK.

Sci.

Aqueous

meshwork

monkey

Vis

and

(Macaca

ferritin

in

1991;32:160.

humor

into

irus).

perfusion

pathways

Schlemm’s

Am

J

canal

Ophthalmol.

1972;73:760.

pockets

are

called

lacunae.

12.

Rohen

JW ,

Futa

cribriform

tangential

CLINICAL

COMMENT : Peripheral

Retinal

aging,

the

vitreous

base

adhesion

extends

further

posteriorly,

and

114

Umihira

approaches

peripheral

the

retina

might

These

contribute

changes

to

the

can

increase

development

of

traction

retinal

e

ne

structure

glaucomatous

Ophthalmol

Vis

Sci.

eyes

of

as

the

seen

in

1981;21:574.

J,

Nagata

and

S,

Nohara

M,

glaucomatous

etal.

Localization

human

trabecular

of

elastin

in

meshwork.

on

Acott

Ophthalmol

TS,

Kelley

Vis

MJ.

Sci.

1994;35(2):486.

Extracellular

matrix

in

the

trabecular

mesh-

detachment.

work.

15.

16. CLINICAL

COMMENT : Posterior

acid

is

displaced

Vitreous

from

the

into

bundles,

the

bundles

can

DA,

O verby

Res.

Lei

DR ,

2008;86:543–561.

TC,

Gibson

meshwork.

St amer

EA,

Mol

W D,

etal.

Vis.

Two-photon

imaging

of

2010;16:935–944.

Joh ns on

M.

The

chang i ng

p ara-

Detachment

collagen

network

and

as

of

contract

and

apply

traction

out f low

resist ance

ge ne rat i on :

towards

sy ne rg ist i c

brils

mo dels coalesce

Eye

trabecular

dig m hyaluronic

Exp

Ammar

the

As

Invest

E.

and

tears

14.

and

normal

115

equator.

and

sections.

normal

Invest

the

in

the

the

border

Lütjen-Drecoll

Traction

13.

With

R,

network

to

of

t he

JCT

and

i n ner

wa l l

end ot heliu m .

E xp

Eye

Res.

the

2009;88:656–670. vitreous

and

thus

malities

that

occurs

to

the

posterior

retina.

One

of

the

most

common

abnor-

17. at

the

posterior

retinal-vitreous

interface

is

a

Braunger

outow vitreous

detachment

caused

by

this

traction.

When

the

vitreous

BM,

pathways

the

retinal

internal

limiting

membrane

at

the

peripapillary

region,

is

torn

away

with

the

vitreous

causing

a

circular

condensation

that

may

be

visible

within

the

vitreous.

If

liquid

vitreous

seeps

into

space

through

the

prepapillary

and

premacular

areas,

a

ER.

e

unifying

aqueous

concept

of

humor

disease

and

causative

treatment.

Europ

J

Pharmacol

Bio-

2015;95:173–181.

Bentley

MD,

Hann

CR,

Fautsch

MP .

Anatomical

variation

of

the

human retrocortical

Tamm

(Weiss

18. ring)

R,

glaucoma:

glial

pharm. tissue

in

detaches

mechanisms from

Fuchshofer

posterior

collector

channel

orices.

Invest

Ophthalmol

Vis

Sci.

syneresis,

2016;57:1153–1159. or

collapse,

of

the

vitreous

can

follow

because

of

the

volume

displacement

19. (Fig.

Carreon

T,

van

der

Mer we

E,

Fellman

RL,

etal.

Aqueous

6.17).

outow

20.

-

A

veins.

Prog

Inoue

T,

continuum

Retin

Eye

Tanihara

from

Res.

H.

trabecular

meshwork

to

episcleral

2017;57:108–133.

Rho-associated

kinase

inhibitors:

a

novel

REFERENCES glaucoma

21. 1.

Swain

DL,

Ho

J,

Lai

J,

etal.

Shorter

scleral

spur

in

eyes

Stamer

therapy.

WD,

open-angle

glaucoma.

Invest

Ophthalmol

Vis

Braakman

Retin

ST,

Eye

Zhou

Res.

2013;37:1–12.

EH,

etal.

Biomechanics

of

with

Schlemm’s primar y

Prog

canal

endothelium

and

intraocular

pressure

reduc-

Sci.

tion.

Prog

Retin

Eye

Res.

2015;44:86–98.

2015;56:1638–1648.

22. 2.

Hogan

MJ,

Alvarado

JA,

Weddell

JE.

Iris

and

anterior

Y e

W ,

Gong

human In:

Histolog y

of

the

Human

Eye.

Philadelphia:

H,

Sit

A,

etal.

Interendothelial

junctions

in

normal

chamber.

Saunders;

Schlemm’s

canal

respond

to

changes

in

pressure.

Invest

1971:

Ophthalmol

Vis

Sci.

1997;38(12):2460.

202–259.

23. 3.

Yun

H,

Zhou

Y ,

Wills

A,

etal.

Stem

cells

in

the

trabecular

Gong

H,

Ruberti

trabecular work

for

regulating

intraocular

pressure.

J

Ocul

Overby

Pharmacol

meshwork

using

D,

etal.

A

new

quick-freeze,

er.

microscopy. 2016;32:253–260.

J,

view

of

the

human

mesh-

Exp

Eye

Res.

2002;75:347.

deep-etch

electron

CHAPTER

94

24.

Ethier

wall

CR,

Coloma

endothelium

6

FM,

of

Aqueous

Sit

AJ,

etal.

Schlemm’s

and Vitreous

Two

canal.

pore

Invest

types

Humor s

in

the

Ophthalmol

inner-

Vis

46.

Sci.

1998;39(11):2041.

25.

Okafor

K,

Vinod

syndrome

and

Johnson

humor

K,

Gedde

pigmentar y

27.

Krohn

space

M,

SJ.

Update

glaucoma.

on

pigment

Curr

Opin

dispersion

copy.

Ophthalmol.

47.

J,

29.

Alm

A,

T.

SF .

Scand.

e

Overby

Exp

drainage

DR.

Unconventional

Res.

2017;158:94–111.

casts

of

routes

the

in

aqueous

human

eye.

49.

Acta

SF .

Gupt a

N,

phat ic

out f low

aque ous

Patel

Uveoscleral

routes.

Eye.

outow—a

1997;11:149.

review.

Exp

Eye

50.

Res.

erties

32.

33.

Ly

T,

et a l.

p at hway

and

in

Ev id enc e

human

g l auc oma.

e

Speakman

J.

Schlemm’s

canal.

Parc

CE,

ne

structure

Ophthalmol.

Drainage

Br

Johnson

preferentially

and

of

a

ne w

she ep;

Invest

uve oly m-

51.

i mpli c at i ons

O phthalmol

Vi s

for

Feeney

Am

35.

Acad

S c i.

J

of

the

inner

wall

of

in

the

Ophthalmol.

Brilakis

collector

studies

Ophthalmol

trabecular

wall

of

ERC.

trabecular

HS.

Giant

channels.

vacuoles

Invest

are

found

Ophthalmol

Vis

53.

Sci.

Sit

of

AJ,

using

Am

wall

an

electron

J

of

electron

of

the

microscopy

tracer.

Trans

54.

the

thalmol

38.

Vis

Alvarado

cellular

work

FM,

wall

Sci.

JA,

of

primate

tra-

of

Alvarado

of

CR,

RG,

canal.

etal.

of

Y eh

aqueous

cells

drive

Schlemm’s

Dvorak-eobold

tomic

40.

relations.

Ashton

veins

N.

by

Ophthalmol.

41.

Ascher

the

KW .

visible

G.

outow

Exp

Eye

Factors

Schlemm’s

across

Res.

55.

1971;

aecting

canal.

the

Invest

pores

56.

Oph-

Johnstone

a

canal

RF ,

etal.

A

new

how

mechanism

endothelial

insight

trabecular

that

into

regulates

cells.

Br

J

the

mesh-

veins:

Res.

43.

Li

P ,

vivo

of

Am

canal:

Ophthalmol

study

neoprene

of

its

of

veins,

Part

I

Soc.

the

per-

Hann

manifestations

in

normal

Chien

I

canal

and

Aqueous

uid.

and

mar y

CR,

Gabfelt

St

Keil

JW ,

J

A.

Pulsatile

and

ow

Louis:

etal.

and

Br

60.

J

canal

Invest

optical

into

and

channel

coherence

eyes

Ophthalmol

A,

PL.

Vis

MD,

using

Sci.

Aqueous

eds.

Adlers

2003:293.

etal.

channels

of

the

61.

low

eyes.

Exp

variations

tomography.

Anatomic

normal

and

struc-

etal.

Eerent

and

and

scleral

aerent

spur.

Jr,

etal.

Functional

meshwork.

Exp

Eye

prop-

Res.

humor

Eye

of

Br

62.

in

S,

high

the

in

Invest

eta l.

ang le

chi ldren

study.

w it h

D y namic

changes

mor pholog y

he a lt hy

O phthalmol

JL,

Sci.

Kater

angle

AT,

etal.

Schlemm’s

Vis

etal.

Eect

microarchitecture

Read

of

de

e yes:

Vi s

a

S ci.

e

canal

of

cyclopentolate

in

healthy

subjects.

pore

density

in

of

glaucomatous

the

on

J

inner

eyes.

2002;43(9):2950.

AW ,

Ethier

glaucoma:

dimensions

in

J

and

CR.

Schlemm’s

correlation

outow

of

J

pri-

canal

between

facility.

Exp

and

Sch-

Eye

Res.

10th

ed.

A,

brimonidine

par ticipants

does

between

it

play

a

ciliar y

role

in

blood

glaucoma

2006;15:172–181.

Gulati

V ,

on

with

A.

Uveoscleral

J

E,

etal.

IOP

Daytime

and

ocular

outow.

Gabelt

Glaucoma.

and

aqueous

nighttime

humor

hyp er tension.

KPB,

Grierson

Res.

2009;88:786–791.

Toris

their

CB,

of

J,

pressure

Gabelt

topical

Surv

Chen

travoprost

Eye.

J

dynam-

Glaucoma.

BT,

I.

in

Kaufman

etal.

action

PL.

Outow

of

aqueous

1):S42.

analogues

and

Update

for

side

on

the

intraocular

in

the

eects.

ante-

Exp

Eye

mechanism

pressure

of

reduc-

2008;53(Suppl1):S107–S120.

Zhang

healthy

coherence

B,

Prostaglandin

prostaglandins

H,

2000;14:488.

Tian

lowering

Ophthalmol.

Huang

AT,

2001;10(Suppl

eye:

Andrés-Guerrero

63.

Guo

T,

and

S,

etal.

subjects

tomography.

Expansion

of

determined

Invest

Schlemm’s

by

canal

Fourier-domain

Ophthalmol

Vis

Sci.

canal

and

V ,

in

future

García-Feijoo

the

medical

J,

Konstas

therapy

considerations.

Adv

of

AG.

Targeting

glaucoma:

er.

2017;34:

Sampathkumar

biometrics

in

S,

the

Fan

S,

ageing

etal.

Aqueous

Chinese

eye.

humour

Br

J

dynam-

Ophthalmol.

2017;101:1290–1296.

64.

Shimizu

anterior

Am

In:

Relationship

1049–1069.

perfusion

Eye.

HA.

production:

Glaucoma.

Agrawal

current

in

changes

and

hydrodynamics.

of

A,

2013;54:1127–1134.

2014;55:5834–5841.

Physiolog y

D,

aqueous

Cracknell

by

aqueous

microstructures

in

Q u ar t i l ho

Chien

rior

ics

B entley

collector

glaucoma

Alm

Mosby ;

AJ,

and

Kaufman

PL,

Fan

action

Ophthalmol.

glaucomatous

Characteristics

collector

A,

canal

Reithamer

and

Schlemm’s

imaging

Vercnocke

BT,

Kaufman

JL,

canal

open-angle

pressures.

45.

open

canal

humor.

ana-

aqueous

veins.

importance

Am

RR,

Lütjen-Drecoll

2017;101:808–813.

Schlemm’s

JM

trabecular

ir ido cor ne a l

cohor t

Ophthalmol

Alm

2011;92:318–327.

Ophthalmol.

in

S,

Allingham

optical

Jamil

A,

M,

pathways:

2009;88:648–655.

2000;41(8):2184.

the

and

Skaat

58.

1934;32:574.

physiologic

intraocular

E,

Butt

resistance?

2014;23:276–281.

Ophthalmol.

anastomosis

Schlemm’s

casts,

Martin

Schlemm’s

Res.

meshwork

Gonzalez

Chan

tion.

aqueous

elimination

enhanced-depth

44.

MS,

57.

1951;35:291.

M,

Sci.

AM,

cana l

endothelium

eects

2018;192:xxix–xliv.

42.

Wittmann

Johnson

ow

59.

Trans

e

an

biomicros-

outow

outow

Eye

trabecular

MK,

in

Exp

2017;26:133–137.

ics

outow :

Schlemm’s

Anatomical

means

24-hour

1996;62(1):101(Abstract).

2005;89:1500–1505.

39.

the

pressure:

ultrasound

humour

meshwork

Glaucoma.

lemm’s

1997;38(8):1517.

regulation

meability

Ethier

endothelium

endothelial

Vis

D ubis

Schlemm

therapy?

inner

J,

accommo dat ion

primar y

1971;71:90.

aqueous

Schlemm’s

dense

1966;70:791.

Ophthalmol.

Mechanism

Coloma

aqueous

aspects.

primate

Schwinn

MC,

vivo

wall

11:116.

37.

between

intraocular

highfrequency

trabecular

bronectin

Rosman

in

1960;44:513.

Otolaryngol.

Scanning

meshwork.

Tripathi

the

and

2018;59:3497–3502.

52.

Invest

DR.

relationship

2017;42:1389–1395.

Gottanka

of

S ch lemm

dur ing

Schlemm’s

1959;62:956.

channels

DH,

near

Outow

Anderson

becular

36.

L.

D aniel

in

2000;41:2984.

34.

e

JM,

of

using

functional

JA,

e

canal

controls

Ophthalmol

Faralli

etal.

2006;82:545–557.

cross-s e c t iona l

AS.

Arch

Selbach

Res.

What

Res.

ER.

X,

Schlemm’s

study

Eye

M.

and

Y an

in

2009;88:689–693.

M,

d rainage

Holmberg

canal.

Tamm

Invest

outow

2008;49:2879.

31.

Y ,

inner vation

2009;88:760–768.

30.

Curr

Eye

tural

suprachoroidal

the

48.

1997;75:32.

uveoscleral

Nilsson

Eye

Corrosion

uveoscleral

Ophthalmol

Nilsson

JW ,

review.

Bertelsen

and

28.

a

Zhao

Johnson

Exp

McLaren

outow :

M,

obser vational

2017;28:154–160.

26.

Li

uctuations

65.

He

Y ,

Assoc

N,

Wu

between

sound

Nakakura

chamber

Pediatr

L,

Qi

S,

angle

Nagasawa

structure

Ophthalmol

M,

American

etal.

Strab.

etal.

Curr

and

Eye

of

children

ciliar y

Ethnic

Res.

Comparison

and

of

the

adults.

J

2017;21:57–62.

Comparison

Caucasians

biomicroscopy.

T,

between

body

Chinese

anatomy

using

2016;41:485–491.

ultra-

CHAPTER

66.

Wr ig ht

C,

closure

g l aucoma:

Taw f i k

MA,

an

Wais b ourd

up d ate.

M,

Ac ta

et a l.

Pr i mar y

O phthalmol.

ang le -

87.

2016;94:217–

nosis,

Chen

the

Z,

Sun

human

with

J,

Li

M,

etal.

Schlemm’s

swept-source

Eect

canal

optical

of

and

age

on

the

trabecular

coherence

morphologies

meshwork

tomography.

Eye

of

88.

measured

(Lond).

89.

2018;32:1621–1628.

68.

Toris

CB,

namics

the

ME,

aging

Wang

human

YL,

eye.

etal.

Am

J

Aqueous

humor

Ophthalmol.

dy-

90.

1999;

Boldea

RC,

Roy

S,

70.

Leske

MC,

ocular

Mermoud

subjects.

Connell

pressure,

AM,

e

A.

Int

Wu

Ageing

of

Schlemm’s

Ophthalmol.

SY ,

Barbados

etal.

Eye

Distribution

Study.

canal

in

2001;24:67.

Arch

of

Zhao

of

D,

Kim

MH,

age-related

Samsung

intra-

Pastor-Barriuso

in

Study.

R,

intraocular

Ophthalmol.

Invest

etal.

A

longitudinal

pressure:

Ophthalmol

Vis

the

Sci.

Hoehn

R,

Mirshahi

Åström

S,

21

-

Acta

Jóhannesson

of

ocular

elderly

study

Kangbuk

Homann

and

risk

its

a

factors:

H,

Lindén

longitudinal

Ophthalmol.

G,

Hallberg

parameters:

healthy

EM,

etal.

association

2014;55:6244–

the

Distribution

with

ocular

Gutenberg

of

Hogan

the

76.

the

77.

78.

MJ,

a

93.

C.

Study.

age-cohort

pressure

study

in

Ambarki

K,

changes

J.

Eye.

sectional

Graefe’s

e

Eye.

9th

JA,

Arch

vitreous.

ed.

St

In:

Louis:

H,

study

Clin

In:

Fischbarg

Elsevier ;

2006:181–194.

histochemical

congenital

J,

Van

WM

Mosby ;

J,

J,

ed.

JE.

northern

of

Exp

young

and

96.

Ophthalmol.

Jr,

Histolog y

of

ed.

Adler’s

Physiolog y

of

e

B,

Biolog y

of

the

J,

etal.

Eye.

e

Mutlu

F ,

system.

80.

Wolter

man

81.

Timmermans

characteristics

of

the

JR.

posterior

Amsterdam:

J.

structure

of

and

in

JP ,

etal.

vitreolenticular

cataract.

Structure

J

Catarac

Immuno-

interface

Refract

in

the

the

B,

internal

electron

normal

and

Surv

Blanks

of

JC,

internal

the

human

retinal

membrane

microscopic

SJ.

F ,

of

the

C,

of

the

hu-

Russell

SR,

conjugates

85.

La

on

changed

the

ne

Topographic

A,

in

the

Go

MM,

Eye.

Ramesh

opticin

S,

in

JD,

etal.

juncture.

human

Vis

Bishop

Hageman

retinal

Sci.

PN.

vitreoretinal

103.

variations

Invest

in

rab-

104.

Ophthalmol

Bonshek

RE,

human

Bishop

eye.

Br

J

GS.

Some

ultrastruc-

105.

Ophthalmologica.

Distribution

internal

vitreous

PN.

1.

e t  a l.

O b s e r v at i on

u s i ng

of

in

chil-

p o ste r i or

s we pt - s ou rc e

O phthalmol

Dolz-Marco

of

the

bursa,

cisterns.

N.

Vi s

R,

S ci.

etal.

posterior

Cloquet’s

Graefe’s

Arch

opt i c a l

c oh e r-

2013;54:3102–

In

vivo

vitreous

canal,

Clin

G.

Itakura

Duane’s

imaging

and

its

of

relation-

prevascular

Exp

vitre-

Ophthalmol.

Lippincott;

S.

EA,

the

cortical

Bishop

LZ,

body

Eckl

vitreous

body :

study.

Am

J

body

in

the

Clinical

In:

Tasman

W ,

Ophthalmolog y,

of

vitreous.

Clinical

In:

Tasman

W ,

Ophthalmolog y,

Jaeger

vol

1.

EA,

M,

of

vitreomacular

interface.

2011;31:1400–1404.

Exp

the

vitreous.

of

1994.

the

etal.

Cytological

layer.

Takanosu

ciliar y

of

changes

Pa).

XII,

tissue

PN,

the

1994.

Aging

Balazs

Toth

of

Foundations

Lippincott;

Kishi

vitreous

of

tomography

Foundations

anatomy

(Philadelphia,

the

coherence

anatomy

Duane’s

Clinical

H,

Microarchitecture

optical

Philadelphia:

eds.

Schwarz

W .

Electron

body.

In:

Academic

Matoltsy

Eye

Le

Studies

and

Res.

Go

on

the

structure

histochemical

of

studies

on

1964;3:57.

M,

etal.

biosynthesis

AG.

A

J,

Bishop

J

PN.

of

e

role

vitreous

of

the

pos-

humour.

Eye.

on

Physiol.

Gen

AG,

the

the

Structure

structural

Cohen

of

on

the

the

Eye.

human

New

protein

Vitrosin:

Cytol.

the

vitreous

gel.

a

member

of

the

col-

1955;1:215.

macromolecules

vitreous

of

1952;36:29.

C.

Biochem

Structural

obser vations

ed.

1961:283.

J

Biophys

of

GK,

study

Matoltsy

class.

microscopic

Smelser

Press;

(vitrosin).

Gross

B embridge

Osterlin

Hultsch

and

BA,

limiting

of

glyco-

membrane.

and

e

postnatal

E,

Prog

and

Retin

supramolecular

Eye

Res.

2000;19:

Immunolocalisation

animal

CN,

Pirie

vitreous

A.

Phase-contrast

b o dy.

Br

J

Ophthalmol.

108.

of

2004;88:697–702.

109.

MI,

vitreous

Ayad

S,

owl

EA.

by

of

hyaluronic

monkey.

In

vitro

cells

J.

of

Exp

synthesis

the

acid

Eye

of

vitreous.

in

Res.

the

vitreous,

IV

1968;7:524.

glycosaminoglycans

Invest

Ophthalmol

Vis

B,

JB.

A

B,

Balazs

granules.

new

look

EA.

Exp

at

e

Eye

chemical

Res.

composition

1979;29:479.

vitreous-humor

collagen.

1984;218:835.

JA ,

C el ls

Holekamp

Shui

Jacobson

hyalocyte

Weiss

Szir mai

the

synthesis

the

1973;14(Suppl):43.

Biochem

107.

in

Balazs

B a l azs

in

t he

NM.

Ophthalmol.

Ophthalmol.

Crawford

the

glycoproteins

b o dy.

structure

of

SE.

Freeman

of

2008;22:1214–1222.

the

Q,

Functional

eds.

regeneration

1991;32(7):1986.

Adult

pocket

1952;36:131.

106.

Shepherd

Ophthalmol

change.

86.

102.

1992;9:219.

membrane.

Caratero

vitreoretinal

D,

Invest

Retina

Sci.

Caratero

aspects

vitreous

2016;168:24–30.

organisation

1984;25:71.

Malecaze

Invest

and

microscopy

studies

pathologically

Ryan

correlation.

323–344.

limiting

limiting

diag-

1):S1–S21.

vitreomacular

precortical

p o cke t

premacular

EA.

EA,

Eisner

lagen

vascular

1985;191:22.

84.

100.

Surg.

1964;42:971.

Ophthalmol.

Li

architecture

Y oshimura

Balazs

body

1964;71:93.

Ophthalmol.

membrane.

primate

Sci.

tural

Arch

Vitreous

Matsumato

Vis

A,

Y ork:

101.

IH.

Ophthalmol.

Pores

retina.

Gaertner

bit

83.

Leopold

Arch

limiting

82.

the

vitreous

99.

V ,

2013;27(Suppl

the

and

2002;16:454.

98.

Fischbarg

2016;42:1037–1045.

79.

to

terior

1992:268.

Sander

97.

1971:607–637.

Ger wen

unilateral

In:

S,

Ghadiali

Philadelphia:

Age-dependency

Vitreous.

Saunders;

Hart

Sebag

vitreous.

Looveren

Weddell

Philadelphia:

Lund-Andersen

Van

O,

ssures,

EA,

95.

etal.

traction

pathophysiolog y,

2015;40:1034–1039.

v it re ou s

high-resolution

vol

94.

Intraocular

and

Posterior

tomo g r aphy.

Jaeger

2014;92:417–420.

P ,

cross

subjects.

Alvarado

Human

Sebag

Uji

a

features

Health

(Lond).

of

2016;60:239–273.

Res.

Ki sh i

vitreomacular

review

95

Humor s

2019;257:709–714.

92.

2015;253:1979–1983.

75.

H,

Eye

anatomy

SY .

Eye

brillar

ship

2013;120:961–968.

Stenlund

years

Sweden.

74.

A,

pressure

cardiovascular

over

Oh

Ophthalmol.

Ophthalmolog y.

73.

treatment.

Curr

Gal-Or

ous

changes

Health

intraocular

and

K-A,

Idiopathic

comprehensive

Vitreous

It a ku r a

the

6250.

72.

Park

AJ.

and Vitreous

3107.

91.

1997;115:1051–1057.

71.

a

Ophthalmol.

e nc e

nonglaucomatous

and

S.

Loter y

hole:

pre c or t i c a l

127:407.

69.

J

dren.

Y ablonski

in

Kishi

Jpn

Aqueous

DHW ,

macular

225.

67.

Steel

6

Stu di e s

e

on

l aye r.

vitreous

gel:

t he

Arch

more

st r uc ture

of

O phthalmol.

than

meets

t he

v it re ous

1958;59:34.

the

eye.

Am

2010;149:32–36.

Holekamp

vitreous

EA.

cor t i c a l

and

NM,

Kramer

B C,

etal.

ascorbate-dependent

e

oxygen

gel

state

of

consumption:

J

CHAPTER

96

relationship

mol.

110.

to

the

6

Aqueous

etiolog y

of

nuclear

and Vitreous

cataracts.

Arch

Humor s

Ophthtal-

mol

Lund-Andersen H, Sander B. e vitreous. In: Kaufman PL, Alm

A, eds. Adler’ s

Physiology

of

the

Armand

Chakrabarti

112.

Ponsioen

matic

of

gel

dichroism

TL,

and

Conformational

liquid

studies.

Deemter

collagen

B.

M,

cross-links,

human

Curr

Bank

Eye

RA,

dierences

vitreous:

Res.

between

fractionation

1987;6:445.

etal.

Mature

enzy-

hydroxylysylpyridinoline

and

Vis

Sebag

face.

114.

G,

hyaluronates

circular

113.

Eye. 10th ed. St Louis: Mosby;

2003:293.

111.

lysylpyridinoline,

2009;127:475–482.

and

Teng

J.

Sci.

Age-related

Arch

CC,

Che

Wang

J,

in

basal

the

the

aging

human

dierences

Ophthalmol.

detachment.

115.

in

vitreous.

Invest

Ophthal-

2009;50:1041–1046.

H.

Am

McLeod

Vitreous

J

Henson

retinovitreous

2003;44(5):1793.

the

changes

Ophthalmol.

D,

in

human

vitreoretinal

inter-

1991;109(7):966.

and

the

mechanism

of

retinal

1957;44:335.

DB,

etal.

adhesion.

Age-dependent

Invest

changes

Ophthalmol

Vis

Sci.

7

Cr ystalline

e cr ystalline lens is an avascular, transparent elliptic structure

the

that

eter

aids

within

and

in

the

focusing

posterior

posterior

to

light

rays

on

chamber,

the

iris

the

retina.

anterior

(Fig.

7.1).

to

e

e

the

lens

lens

is

vitreous

is

located

chamber

suspended

from

anterior

and

posterior

nasal-to-temporal

reaches

cally

an

adult

during

size

the

por tions

in

of

the

9.0

teenage

of

infant

mm

the

is

lens.

6.5

and

then

e

mm.

horizontally

years

lens

e

and

does

Lens

9.7

not

diam-

diameter

mm

verti-

change

sig-

5–8

the

surrounding

ciliar y

body

by

zonular

bers.

It

is

malleable,

nicantly,

although

some

report

a

small

age-related

increase

9

and

ciliar y

muscle

contraction

increasing

the

causes

increase

dioptric

can

power

of

cause

the

a

eye.

change

e

in

lens

shape,

mechanism

in

diameter.

e

that

refractive

power

of

the

unaccommodated

lens

is

approxi-

10,11

allows

an

near

objects

in

to

lens

be

power

focused

is

on

accommodation,

the

which

mately

20

diopters

e posterior lens surface is attached to the anterior vitreous face

surrounding

Within

is,

this ring is a potential space, the retrolental space (of Berger), an area

of

of nonadhesion between the vitreous and the lens (see Fig. 6.13).

changes

hyaloid

capsular

ligament,

a

circular

ring

adhesion.

lens

the

environment,

thickness.

protein

optical

LENS

and

depends

on

the:

(1)

surface

curva-

tures, (2) refractive index, (3) change in index between the lens and

retina.

the

by

(D)

in

e

and

lens

has

concentration

optical

density

density

cause

the

(4)

a

length

gradient

within

the

throughout

index

of

of

the

optical

refractive

lens

the

bers

lens.

refraction

which

ese

to

path,

index

that

because

produces

variations

increase

from

in

the

periphery of the lens to the center of the lens. e refractive index of

DIMENSIONS

12

the cortex is 1.38 and the nucleus has an index of refraction of 1.41. e

lens

is

biconvex,

with

the

posterior

surface

having

the e

steeper

cur ve.

e

anterior

radius

of

cur vature

measures

8

ing 14

mm,

and

the

posterior

surface

radius

of

cur vature

power

of

the

lens

increases

in

a

maximum

accommodative

measures

to

8

called

the

e

centers

of

the

anterior

and

posterior

the p oles,

anterior

to

and

the

posterior

lens

pole.

thickness

e

is

the

thickness

3

mm

14

D,

result-

reached

Accommodative power decreases

surfaces

of

distance

14

the

each

year

throughout

age,

approaching

zero

aer

50

years.

f rom

unaccom-

modated lens is 3.6 to 4.5 mm (mean of 4 mm), and it increases

0.02

of

2

mm.

with are

accommodation,

amplitude

13

between ages 8 and 12 years. 1

5

with

to

EMBRYOLOGICAL

DEVELOPMENT

4

life.

e

e quator

is

the

large structure of the adult lens is determined during embr yolog-

est

circumference

of

the

lens,

located

at

the

junction

between ical

development.

obser vable

in

the

e

lens

vesicle,

developing

the

embr yo,

rst

is

lens-like

composed

structure

of

a

layer

of

Cornea

Anterior

epithelial

cells

tioned

that

that

forms

a

hollow

sphere.

e

cells

are

posi-

chamber

Lens

so

the

apical

surface

lines

the

lumen

of

this

sphere.

Iris Ciliary

muscle

e

posterior

cells

dierentiate

and

elongate,

forming

the

pri-

Zonule

Ciliary

body

mar y

Ora

serrata

lens

anterior

has

no

bers

cells,

(Fig.

the

posterior

7.2).

center

of

As

these

the

epithelium

bers

sphere

because

grow

lls.

it

and

us

was

the

used

to

reach

adult

form

the

lens

these

rst lens bers. During the rest of the life of the lens, cell division

occurs

the

bers

Vitreous

in

lens

the

germinative

equator,

that

are

and

laid

zone

these

down

of

cells

outer

the

epithelium

elongate

to

all

to

earlier

form

just

anterior

secondar y

bers.

With

to

lens

age,

the

Retina

lens

continues

to

grow

as

it

forms

new

bers

(see Ch.

9).

Choroid

Sclera Fovea

LENS Optic

HISTOLOGY

nerve

Lens

e

Capsule

lens

capsule

is

a

transparent

envelope

that

surrounds

the

entire lens. It provides a semipermeable barrier preventing large

molecules, Fig.

7 .1

Diagram

showing

the

relationship

of

the

lens

and

such

as

albumin

and

hemoglobin,

from

entering

the

zon6,15

lens ules

to

other

ocular

structures.

(From

Figure

3.4B;

but

allowing

nutrients

and

antioxidants

to

enter.

Paterson

e capsule is a basement membrane that, with time, becomes CA,

Delamere

NA. The

lens.

In:

Levine,

Nilsson, Ver

Hoeve, Wu, 16

the editors.

Edition

1 1 .

St

Louis:

Mosby;

thickest

in

the

body.

Its

thickness

varies

with

location.

e

201 1 .)

97

CHAPTER

98

7

Crystalline

Lens

Lens

capsule

A Presumptive

fibers

Anterior

epithelium

B

Lens

fibers

C

Elongating

posterior

epithelium

D

Primar y

lens

Fig.

fibers

to Fig.

the

7 .2

Development

lens

forming

placode,

the

lens

of

the

embryonic

precursor

vesicle.

C, The

nucleus.

of

the

hollow

A,

lens.

lens

7 .3

and

E

Formation

B,

Light

capsule.

the

micrograph

A

of

honeycomb

epithelium

is

the

anterior

appearance

of

lens

lens

epithelium

bers

of

Invagination

vesicle

is

lined

with

membranes

of

the

epithelial

cells

are

joined

by

desmosomes

19–23

epithelium.

bers.

E,

D,

Posterior

Primar y

nucleus. The

lens

cells

bers

anterior

elongate

ll

the

epithelium

becoming

lumen

primar y

forming

remains

in

the

lens

-

embr yonic

place.

lens

capsule

is

produced

by

the

anterior

e

band

anterior

epithelium

and

thickens with age. At the anterior pole, the capsule thickens from

24

gap junctions.

tion

anterior

adjacent

evident.

of

each

to

of

the

cell

cell

cells

in

equator

mitosis.

divides,

equator,

and

25

ere are few, if any, tight junctions.

a

the

is

Cell

the

division

daughter

withdraws

preequatorial

called

from

cell

the

region

germinative

continues

migrates

cell

cycle,

that

zone,

lies

the

throughout

posteriorly

and

just

loca-

life.

toward

dierentiates

As

the

into

17

approximately

the

anterior

11

pole

to

15

μm.

appears

to

e

be

the

annular

region

thickest.

It

too

surrounding

increases

with

a

lens

ber.

stretches

Each

toward

newly

the

formed

posterior

cell

pole

elongates;

and

the

the

apical

basal

aspect

aspect

toward

17

age from approximately 13.5 to 16 μm.

thinnest

(approximately

contribution

from

bers,

not

it

does

the

3.5

μm).

basal

e posterior pole is the

Although

membrane

appreciably

increase

it

of

with

may

the

age.

receive

some

posterior

e

lens

thickness

at

the

anterior

equator,

of

the

lular

pole

with

lens

(Fig.

bers

move

is

stretching

peripher y.

nuclei

7.4).

As

with

the

the

process

toward

cells

in

the

each

cytoplasm.

occurs

poles

layer

A

line

all

around

from

all

elongate,

drawn

to

the

aspects

the

cel-

connect

17

the

equator

e

increases

capsule

slightly

consists

with

primarily

age,

of

and

on

collagen;

average

it

is

contains

7

μm.

no

elas-

tic bers but is highly elastic because of the lamellar arrangement

6

of

the

the

shape

It

of

dots

the

encloses

lens.

shape,

but

all

e

this

lens

components

capsule

would

tendency

is

and

prefer

helps

to

to

take

counteracted

by

a

becomes

more

cal

the

pull

as

it

bers,

it

with

from

the

zone

of

the

equator

annular

the

area

capsule

to

an

area

mentioned

is

called

near

both

poles.

previously.

the

zonular

e

is

outer

lamella

and

lens

surface)

merging

with

a

underlying

older

supercial

these

Eventually,

mold

from the zonular bers. e zonular bers insert into the capsule,

coincides

of

nuclei

would

have

an

arcuate

shape

toward

the

anterior aspect, a conguration called the lens bow (see Fig. 7.4).

loses

all

cellular

organelles,

the

elongated

cell

18

bers.

spherical

the

and

tive

and

e

the

are

e

more

cells

bers

end

between

new

lie

lens

laid

are

directly

from

the

lens

ber

epithelial

are

bers

formed

called secondar y

of

the

bers

supercial

youngest

All

anterior

itself

bers.

capsule.

zone

e

insinuates

lens

bers.

the

ber.

layer

down

longer

below

mitosis

api-

and

outer

than

the

in

(the

the

to

the

deeper

epithelium

the

germina-

bers

6

consists

of

zonules

interconnected

with

matrix.

Lens

Lens

Epithelium

Adjacent

epithelial

cells

to

the

anterior

cells—the

secrete

the

Fibers

Lens ber production continues throughout life, with the new lens

lens

capsule

anterior

a

single

of

7.3).

to

form

the

primary

lens

during

bers.

e

the

being

laid

down

outer

to

the

older

bers.

Growth

results

in

concentric layers of secondary lens bers. e structure of the lens

A section through the equator of the lens shows that the bers cut

development

used

are

bers

onion, but each layer is made up of adjacent bers within the layer.

was

and

ese

epithelium

it

life

cuboidal

is similar to an onion; each layer of bers is similar to a layer of an

because

throughout

layer

(Fig.

site

present

capsule

is

epithelium

of metabolic transport mechanisms. As noted earlier, no posterior

is

anterior

lens

embryological

basal

aspect

of

in cross-section have the shape of a attened hexagon with dimen-

26

the

epithelial

cell

is

adjacent

to

the

capsule,

and

the

apical

por-

sions

of

3

by

9

μm

(Fig.

7.5).

In

the

adult

lens,

the

27

tion

is

oriented

inward

toward

the

center

of

the

lens.

e

lateral

outer ber can be up to 1 cm from suture to suture.

length

of

an

CHAPTER

C

Fig.

7 .4

Composite

attachments.

The

size

zone,

lens

at

the

equator.

equator

itself.

arrows);

capsule,

JE.

they

nuclei

The

are

of

not

the

cells

crystalline

lens

can

zone.

migrate

become

lens

At

and

Human

compared

equator,

cells

send

somewhat

(d)

and

is

thicker

attach

or

to

zonular

Eye.

with

anterior

lamella

of

a

of

the

are

ne

to

lens

in

B,

form

as

to

into

99

Lens

and

the

intermediate

(arrows)

the

to

equator

are

than

the

Alvarado

At

formed

at

the

(double

hexagons

to

the

bow.

inclusions

and

form

toward

lens

cells

attened

MJ,

zonular

cross-section.

the

new

capsule

Hogan

a

posteriorly

lamentous

posterior

(g).(From

Saunders;

and

posterior

elongate

and

cells

and

elongating

equator

the

capsule,

section

anteriorly

into

and

bers

at

cells

cont ains

lens

epithelium,

in

the

displaced

anterior

Philadelphia:

to

Crystalline

A

those

processes

Lens

the

seen

dividing

capsule

posteriorly.

(f)

cortex,

is

anterior

more

equatorial

present

bers

be

lens,

epithelium

the

more

capsule

pericapsular

the

of

central

elongate,

anterior

Zonular

forming

Histology

these

nuclei

The

these

cross-section.

of

As

their

time,

anterior

equatorial

cells.

and

same

the

shape

C,

cortical

sutures,

the

and

and

drawing

A, The

B

7

(e)

in

equatorial

JA, Weddell

1971 .)

6

Lens

teins,

40%

ber

cytoplasm

known

of

the

as

net

contains

cr ystallins,

weight

of

a

which

the

high

concentration

accounts

ber.

Alpha

for

of

pro-

approximately

cr ystallins

are

junctions,

e

bers

and

are

B ecause

tightly

allow

also

the

for

joined

lens

has

sliding

by

no

between

bers

(Fig.

19

25

7.6).

desmosomes.

vascular

supply

and

the

bers

lose

28

associated

or

distribution

and

thegradient

28

partially

embedded

concentration

refractive

index,

as

in

the

of

cell

membrane.

cr ystallins

well

as

the

e

contribute

transparency

of

to

the

their

cellular

organelles

as

they

age,

some

cell-to-ber

is

an

extensive

network

of

gap

junctions

throughout

e

cr ystallin

concentration

varies

from

approximately

along

the

lateral

ber

membranes

to

account

for

the

19

30

in

A

vides

the

cortex

cytoskeletal

structure

to

70%

in

network

and

also

the

of

with

nucleus.

microtubules

provides

stability

and

by

laments

being

pro-

anchored

to

gap

ent

which

nutrients

junctions

protein

plasma

and

membrane.

elaborate

have

a

and

ions

dierent

connexins

lens

move

within

packing

forming

the

the

channel

than

31

lens.

arrangement

do

facility

and

the

ese

dier-

typical

22

25

the

the

29

lens.

15%

and

ber-to-ber mechanism of communication is necessar y. ere

e

lateral

interdigitations

membranes

along

the

ber

have

numerous

length

that

take

gap

junctions.

throughout

the

e

lens,

gap

with

junctions

few

near

are

the

not

evenly

poles,

more

distributed

toward

16

various

shapes,

such

as

ball-and-socket

and

tongue-in-groove

equator,

and

seemingly

fewer

junctions

in

deeper

layers.

the

22

23

CHAPTER

100

7

Crystalline

Lens

and

bers

but

such

in

the

central

zone

(i.e.,

near

the

poles

and

sutures),

22

junctions

increase

toward

the

germinative

zone.

25

Pinocytosis

does

DIVISIONS

occur

OF

at

THE

this

interface,

facilitating

exchange.

LENS

e primary lens bers from the elongating posterior epithelium

form

the

sequent

then

cell

a

e Fig.

7 .5

Scanning

electron

micrograph

shows

the

in

lens

fetal

ber.

hexagonal

cross-sectional

proles

of

lens

of

are

the

migrates

the

lens,

laid

the embryonic

down

outer

preequatorial

toward

All

nucleus

such

the

region

equator

bers

includes

this

of

and

formed

the

to

are

nucleus.

core.

the

sub-

mitosis

epithelium.

then

elongates,

secondary

embryonic

All

Cell

nucleus

lens

and

e

form-

bers.

the

bers

charac-

surrounding teristic

center

bers

begins

new

ing

very

lens

ber

it

that

are

formed

before

birth.

e adult

nucleus

is

cells.

considered to include the embryonic and fetal nuclei, as well as the (From

Paterson

CA,

Delamere

NA. The

lens.

In:

Hart WM

Jr,

edi-

bers tor.

Adler ’s

Physiology

of

the

Eye,

ed

9.

St

Louis:

Mosby;

formed

tex

contains

Some

In

addition,

aspects

fusion

of

micropinoc ytic

ber

also

membranes

allow

vesicles

and

movement

of

at

the

signicant

material

apical

areas

from

ber

16

contribute

to

communication

between

21

and

of

23

basal

membrane

to

ber

and

e

border

thelium

known

are

and

as

the

the

but

that

apical

across

such

disagreement

20

23

31

the

of

exists

was

on

of

the

interface.

epithelium-ber

movement

now

and

sexual

the

bers

aer

maturation.

sexual

e lens cor-

formed

maturation

before

sexual

(Fig.

7.7C).

maturation

the

29

and

the

remaining

bers

the

cortex.

e

lens

cortex

has

the

low-

est and the embryonic nucleus has the highest index of refraction.

32

anterior

elongating

Nutrients

interface.

facilitated

whether

the

gap

by

It

gap

epi-

ber

is

and

ions

was

once

junctions,

junctions

are

pres-

the

their

lens

bers

layer,

suture

and

SUTURES

is

formed

the

reach

forming

by

posterior

a

the

poles

junction

the

joining

suture

is

they

meet

known

of

the

formed

as

a

apical

by

with

other

suture.

aspects

the

bers

e

of

joining

the

of

in

anterior

bers,

the

basal

aspects. e secondary bers formed during embryological devel-

opment

meet

in

three

branches,

forming Y

sutures.

e

anterior

suture is an upright-Y shape and the posterior suture an inverted-

32

ent.

Gap

membrane,

surfaces.

membrane

membrane

birth

formed

juvenile nucleus, those added before middle age the adult nucleus,

As

apical

epithelium-ber

exchanged

assumed

the

bers

bers.

Interface

between

the

consider

LENS

Epithelium-Fiber

between

1992.)

and

Few

preparations.

junctions

the

true

are

usually

epithelium-ber

gap

Minimal

junctions

coupling

have

found

on

interface

been

occurs

the

lateral

involves

visualized

between

the

in

cell

Y shape (see Fig. 7.7A). As growth continues and the lens becomes

apical

larger, the sutures become asymmetric and dissimilar. e limbs of

tissue

the anterior and posterior sutures are oset, and the complexity of

epithelium

the

sutures

aer

Ball-and-

birth

contributes

are

adulthood

more

have

6

to

lens

stellate

to

9

transparency.

shaped.

branches,

Sutures

and

e

sutures

formed

there

are

9

formed

through

to

15

early

complex

33

socket

branching stars formed in middle to old age (see Fig. 7.7B).

intercellular

process

CLINICAL

COMMENT: Slit-Lamp

An

optic

section

as

well

as

bright

the

line

through

anatomical

on

anterior

the

lens

the

lens

transition

anterior

capsule.

lens

Appearance

demonstrates

zones

surface

Posterior

to

the

within

is

the

convex

this

is

a

which

remodeling

contains

zone

transparency Fiber

or

newly

zone

because

of

of

synthesized

disjunction,

an

abrupt

the

change

in

lens

line,

of

(Fig.

the

structure,

7.8).

and

the

The

area

cell

Lens

The

thought

rst

to

subcapsular

be

clear

35

bers.

is

the

forward

dark

34

zone,

of

biconvexity

of

next

the

bright

cortex

that

differentiation.

line,

is

Then

the

losing

various

cells

gray

Ball-and-

socket

zones

fetal,

and

are

seen

indicative

embryologic

nuclei.

of

the

The

remaining

anterior

Y

cortex,

suture

of

as

the

well

fetal

as

the

adult,

nucleus

may

intercellular

be

evident.

The

center

of

the

lens

is

the

embryonic

nucleus.

The

posterior

processes

inverted-Y suture may be seen within the posterior portion of the fetal nucleus

Pyknotic

(Fig.

7.9).

with

the

Posterior

to

this,

the

zones

of

discontinuity

are

concave

forward,

nucleus

of

nal

zone

being

the

posterior

capsule.

The

zones

of

discontinuity

are

fiber

apparent

because

of

changes

in

light-scattering

properties.

A

diffuse

view

of

cell

the

Fig.

7 .6

Fiber

cells

of

the

lens

cortex.

(T ransmission

anterior

×6000.)

(From

Krause

WJ,

Cutts

JH.

Concise

Histology.

Baltimore:

Widilliams

&

W ilkins;

1991 .)

illustrates

lens

the

surface

of

an

orange,

shagreen,

likely

T ext capsule

of

surface

with

the

lens

surface

re-

electron sembling

microscope;

lens

to

the

epithelial

cell

undulations.

caused

by

the

conformation

of

the

CHAPTER

7

Crystalline

Lens

a

b

A

B

C

Fig.

7 .7

us. The

wide

Y

Fetal

bands.

suture

lens

at

lens.

the

reader

nucleus

is

or

the

In

MJ,

in

is

at

attach

to

pole.

into

drawing ,

for

a

the

of

the

adult

Alvarado

JA,

and

the

tips

B, The

Lens

fork

the

the

Y

that

the

the

sutures

lens. The

Weddell

the Y

that

the

of

Histology

the

is

one

the

the

of

(b). The

pole

tip

of

and

of

lens

lens

lens

C,

The

capsule

Human

the

to

in

A,

are

to

in

a

various

of

zones

Philadelphia:

fork

in

the

the

of

the

insert

single

zones,

nucle-

depicted

sutures

conser ves

lie

Fetal

the

branch

thickness

nuclear

Eye.

att ach

suture

appears

throughout

cells.

cells

posterior

a

arrangement

suture

lens

the

at

anterior

nucleus.

the

of

at

from

extends

fet al

arrangement

suture

pole. This

purposes,

thickness

JE.

of

arise

opposite

suture

in

and

suture

organization

cells

at

sutures

posterior Y

of

educational

remember

level

showing

(a),

complex.

posteriorly

the

lenses

opposite

should

to

that

more

this

capsule

Hogan

adult

suture

Cells

the

cortex

anteriorly

lens

and

anterior Y

adult

farther

shape

plane,

cortex

epithelium,

is

as

the

of

but

and

and

shown.(From

Saunders;

1971 .)

101

CHAPTER

102

Fig.

7 .8

Cross-section

capsule

(red

dot),

(yellow

dot),

by

zones

gray

the

cortex

the

of

and

of

the

7

Crystalline

the

dark

bright

lens

area

showing

of

newly

remodeling

discontinuity

Lens

zone

the

bright

anterior

synthesized

(blue

representing

dot),

the

cortex

followed

remainder

of

nuclei.

Fig.

7 .10

Scanning

insertions

ZONULES

(OF

between

ZINN)

to

e

like

of

lens

is

bers,

the

attached

the

lens

the

zonules

(Fig.

microbrils

to

7.10).

which

ciliar y

(of

Zinn),

e

have

body

or

bers

by

the

group

of

suspensor y

belong

remarkable

a

to

a

ligament

categor y

extensibility

thread-

the

after

the

lens

Ocular

anterior

&

of

and

capsule.(From

Anatomy,

Harper

electron

removal

Row;

micrograph

the

cornea

posterior

the

anterior

iris.

Note

zonules

and

BW.

Jakobiec

Streeton

Embr yology,

of

and

In:

and T eratology.

the

zonular

the

angle

att achment

JA,

editor.

Hagerstown,

Md:

1982.)

termed

because

of Most

bers

attach

to

the

lens

capsule

at

the

preequatorial

and

36

their

supramolecular

organization.

e

zonules

appear

to

be 38

postequatorial formed

of

extracellular

matrix

that

includes

brillin

and

regions;

few

attach

directly

at

the

equator.

e

elastin, zonules

are

inter woven

into

the

components

the

capsule.

primar y

of

zonules.

36,37

both

of

which

have

a

role

in

the

synthesis

of

elastic

bers. ose

However,

biomolecular

analysis

indicates

that

there

are

no

that

attach

to

the

lens

are

known

as

true Secondar y

zonules

join

the

primar y

zonules

with

each

other

or

36,37

elastic

bers

present

in

the

zonules. connect

ciliar y

Tension

bers

processes

to

one

another

or

to

the

pars

plana.

to

the

ciliar y

e zonular bers arise from the basement membrane of the

nonpigmented

ciliar y

epithelium

in

the

pars

plana

and

anchor

the

primar y

zonules

38

leys the

valleys

between

the

ciliar y

processes

in

the

pars

to

form

two

column-like

structures

(tines)

on

both

(see

Fig.

a

ciliar y

process

and

end

at

the

lens

capsule

a

fulcrum

and

stabilize

the

39

valleys.

ere

endings

and

mechanoreceptors

near

zonules

that

are

origi-

sides nate

of

form

plicata. ner ve

ey

val-

from

at

the

base

of

the

pars

plicata

valleys

and

interact

with

the

5.21). primar y

zonules,

suggesting

a

role

in

measuring

tension

in

the

39

zonular

the

apparatus

anterior

vitreous

lize

the

to

and

vitreous

the

39

and

capsule.

the

posterior

vitreous

36

lens

to

pars

lens

allow

Vitreous

plicata,

(Wieger

smooth

as

zonules

well

as

ligament),

for ward

and

connect

the

to

anterior

help

stabi-

backward

lens

40

movement.

ACCOMMODATION

When the emmetropic eye is viewing a distant object, the ciliar y

muscle

large,

is

relaxed,

and

the

the

zonules

diameter

are

in

a

of

the

ciliar y

stretched

ring

is

relatively

conguration

exerting

tension on the lens capsule. e zonular tension holds the lens in

the unaccommodated state such that the image of a distance tar-

get

lies

retina,

is

Fig.

7 .9

The

posterior Y

suture

is

seen

as

an

upside-down Y .

on

an

the

increase

plished

retina.

increase

by

a

in

in

When

the

power

change

in

is

a

near

refractive

called

lens

object

is

power

to

of

be

the

focused

eye

accommodation

shape

brought

about

must

and

by

is

on

the

occur.

accom-

contraction

CHAPTER

7

Crystalline

103

Lens

41

of

the

ciliar y

muscle.

According

to

the

classic

Von

Helmholtz maximal

theor y,

the

following

occur

during

contractile

ability

of

the

muscle

decreases

only

slightly

if

at

all

with

accommodation: 7

55

age.

No

loss

of

parasympathetic

innervation

occurs

that

would

account

42–45

1.

Lens

thickness

increases

anterior

to

posterior

7

for

decreased

muscle

contraction.

The

diameter

of

the

unaccommodated

44–46

2.

3.

e

lens

equatorial

e

anterior

lens

rior

chamber

diameter

surface

decreases

moves

for ward

42

ese

cur ved

that

becomes

factors

result

surfaces

initiates

and

the

and

thus

the

ante-

in

a

ciliary

body

decreases

and

in

lens

older

eyes,

equator

thus

decreases

the

circumlental

with

56

zonular

thickened

increased

accommodative

ring

43

shallower

thus

ciliary

lens

lens

with

more

power.

mechanism

is

e

sharply

to

retinal

blur.

whether

age.

stimulus

tension

The

capsule

e

the

in

the

unaccommodated

zonule-free

increase

in

thickness

area

anterior

might

at

lens

cause

the

There

anterior

lens

and

appearance

space

causing

a

between

decrease

in

57

eye.

convexity

the

age,

the

of

is

some

surface

decreases

increase

what

is

dispute

in

with

anterior

called

as

lens

an anterior

57

shift

accommodative

mechanism

is

dependent

on

cone

with

little

inuence

by

in

the

anterior

zonule

insertion

on

the

capsule.

There

is

no

apparent

stimulation

increase

47

in

zonular

length

that

presumably

would

accompany

such

an

ante-

rods. 58

rior

When

the

ciliar y

muscle

contracts,

the

muscle

area

37

shift.

Some

loss

of

ber

extensibility

with

age

has

been

elastic,

and

more

58

measured.

increases 59

The

and

the

diameter

of

the

ciliar y

ring

surrounding

the

lens

capsule

becomes

thicker,

less

brittle

with

age.

lens Older

lens

bers

become

more

resistant

to

deformity,

and

thus

the

ability

of

decreases, reducing the tension that the zonules exert on the lens the

and

allowing

the

lens

capsule

to

assume

its

preferred

lens

to

e

lens

the

lens,

pull

to

e

anterior

capsule

transmits

molding

the

lens

the

reduction

into

its

in

lens

surface

becomes

increases

in

more

sharply

cur vature

the

zonular

accommodated

42

terior

44

form.

e

slightly ;

mass

lens.

and

The

with

age.

volume

of

the

anterior

surface

does

not

pos-

however,

become

the

lar

the

greater

increase

vector

force

lens

than

in

the

relationship

to

be

of

the

posterior

surface.

capsule

occurs

14

that

As

the

lens

thickens

axially,

in

more

bulk

posterior

43

diameter

the

cornea,

pole

may

decreases.

and,

e

although

move

a

small

anterior

not

lens

found

amount

in

in

the

pole

all

the

forces

a

forward

the

lens

to

exerted

grow

by

the

capsule

movement

and

the

throughout

of

anterior

the

life,

center

the

of

displacement

the

alter

lens

the

and

lens

the

zonules

surface

and

causing

less

able

the

zonu-

to

change

little

change

64

As

power,

the

to

the

greater

lens

force

becomes

will

be

more

curved

required

to

and

increase

the

power

the

for

near

65

focus.

moves

studies,

posterior

the

direc-

e

cur vature

of

the

internal

surfaces,

seen

at

the

LENS

ics

to

continues

48–50

tion.

zones

of

between

60

toward

lens

with

tangential

tension.

lens

necessary

equatorial

response

the

increase,

48

steepness

in

As

45

cur ved.

only

shape

60–63

diminishes

shape.

change

spherical

of

the

discontinuity

changes

in

the

and

the

surface

boundaries

cur vatures

of

and

the

nuclei,

contributes

PHYSIOLOGY

mim-

to

the

e

primar y

function

of

the

lens

is

the

refraction

of

light,

and

48

increase

from

in

the

anterior

total

to

dioptric

posterior

power.

occurs

is

in

the

thickening

nuclear

of

the

region,

lens

but

the

it

is

imperative

scatter.

that

the

Transparency

is

transparent

a

function

of:

lens

(1)

have

the

minimal

absence

of

light

blood

51

thickness

e

of

the

lens

vitreous

has

cortex

a

remains

passive

role

unchanged.

in

vessels, (2) few cellular organelles in the light path, (3) an orderly

accommodation,

probably

arrangement

of

bers,

and

(4)

the

short

distance

between

com-

52

ser ving

only

contraction,

ing

in

as

the

orienting

entrance

pupil.

support

for

choroid

the

is

the

pulled

shape

also

During

for ward

photoreceptors

Scleral

66

lens.

slightly,

correctly

changes

ciliar y

in

muscle

perhaps

relation

during

ponents

aid-

to

the

accommoda-

of

diering

Because

extensive

epithelium

equatorial

indices

to

metabolic

maintain

region

has

relative

a

cell

high

to

the

activity

and

level

ber

of

wavelength

occurs

in

function,

miotic

of

the

and

activity,

a

light.

anterior

the

pre-

signicant

53

tion.

e

attached

widening

ow

ciliar y

to

and

the

of

muscle

scleral

the

and

spur,

intertrabecular

decreasing

trabecular

and

spaces,

intraocular

meshwork

accommodation

facilitating

are

can

both

cause

aqueous

a

out-

pressure.

amount

of

therefore

aqueous

energ y

most

with

is

used

nutrients

a

small

by

these

are

cells.

obtained

contribution

and

sue

the

of

sion

the

ciliar y

Bruch

in

ciliar y

the

muscle

body

is

stretched

membrane.

zonules

unaccommodated

relaxes,

e

stretches

the

muscle

posteriorly

ciliar y

the

ring

capsule,

moves

by

the

expands,

restoring

outward,

elastic

and

the

the

lens

tis-

ten-

to

its

state.

sium/adenosine

maintain

of

the

Free

triphosphatase

electrolyte

energ y

lication

but

CLINICAL

lens

from

the

the

is

avascular,

surrounding

vitreous.

us

the

epithelium is rich in transport mechanisms (e.g., sodium/potas-

+

When

e

from

balance.

required

within

the

radicals

+

/K

Anaerobic

cellular

/ATPase]

pumps)

glycolysis

is

metabolism

and

the

that

source

cellular

rep-

lens.

are

ultraviolet

for

[Na

a

normal

light

byproduct

absorption

can

of

metabolic

also

processes,

produce

oxidative

changes within tissue causing the formation of free radicals. Free

COMMENT: Presbyopia

The ability to focus at near distances decreases with age, and this loss in accom-

radicals

disrupt

cellular

processes

and

cause

cellular

damage.

modative ability is called presbyopia. The objective measurement of accommo-

dation

nears

zero

by

the

age

of

50

years,

although

subjective

measurements

of

Lens accommodative

amplitude

may

be

higher

because

of

the

depth

of

e

Changes

in

inuence

the

the

ciliary

loss

of

body,

zonules,

accommodation,

lens

yet

capsule,

the

and

precise

the

lens

nature

Capsule

focus.

of

itself

the

all

lens

ment

capsule

and

is

rst

completely

evident

in

surrounds

early

the

embryological

early

lens

bers.

develop-

e

lens

is

impact

said

to

have

immune

privilege

and

protection

from

infectious

each has is still unclear. Because of the inability of the lens to change shape,

viruses there

is

no

increase

in

lens

thickness

with

attempted

accommodation

and

epithelium 3

age

50

years.

bacteria

because

the

capsule

sequesters

the

lens

over

and

bers

beginning

in

early

prenatal

development.

50

Although

ciliary

muscle

tissue

is

lost

and

replaced

by

con-

Postnatally,

the

anterior

lens

epithelium

and

the

posterior

lens

54

nective

tissue,

this

occurs

in

very

old

age,

not

at

the

onset

of

presbyopia.

bers continue to secrete and deposit matrix into the inner aspect The

force

of

ciliary

muscle

contraction

does

not

decrease

with

age,

and

of the capsule. As the lens itself grows throughout life, the capsule

CHAPTER

104

must

expand

as

well,

7

Crystalline

although

the

Lens

molecular

mechanisms

that

anterior

surface;

other

growth

factors

that

inuence

dierentia-

74

regulate this are unknown. e capsule is permeable to water and

tion

small

interactions

solutes,

as

well

as

the

proteins

necessary

for

lens

growth

are

concentrated

among

at

the

actin

equator.

laments,

Biomolecules

adhering

that

junction

regulate

integrins,

76

and

function.

Size

and

molecular

charge

may

inuence

passage

and

extracellular

matrix

increase

ber

mass.

Signicant

protein

67

through the capsule.

A slow turnover of radiolabeled substances

synthesis

must

occur

to

form

crystallins,

aquaporin

channel

pro-

76

has been demonstrated within the capsule matrix (over months to

teins,

years),

the ber cell elongates, the cell membrane permeability increases,

as

compared

with

basement

membranes

elsewhere

(over

and

gap

junction

components

67

as

the

bers

+

hours).

e

capsule

acts

as

a

reservoir

for

the

accumulation

of

causing

the

accumulation

of

elongate.

As

−

K

and

chloride

(Cl

)

in

the

cyto-

77

molecules and growth factors that promote and regulate lens pro-

plasm,

driving

water

entrance

and

cell

volume

increase.

67

cesses,

such

as

proliferation,

migration,

and

dierentiation.

As

cal

Lens

Epithelium

along

+

Aquaporins

epithelium

and

of

Na

the

+

/K

lens

ATPase

regulate

pumps

nutrients

within

the

anterior

and

enhance

Paracellular

connex-

and

ions

68

water

ins

movement

also

aid

involved

in

in

the

in

and

out

nutrition

synthesizing

of

and

the

lens.

homeostasis.

glutathione,

e

which

acts

epithelium

as

an

is

antioxi-

cell

aspect

the

the

end

lens,

the

of

an

capsule.

forming

and

once

organelles

apical

aspect

epithelium,

elongating

join,

capsule

the

anterior

posterior

of

they

bound

elongates,

the

Once

ber

a

the

from

suture.

this

and

e

along

basal

end

occurs,

endoplasmic

end

opposite

basal

the

aspect

elongating

the

detachment

(nucleus,

slides

the

reaches

side

of

detaches

the

api-

slides

the

from

membrane-

reticulum,

mitochon-

dria) degrade in an apoptosis-like process. e loss of organelles

76,78,79 68,69

dant,

and

metabolites,

which

lter

ultraviolet

is

light.

complete

Fiber

Lens

a

few

hours.

Junctions

Fibers e

Fiber

membranes

of

adjacent

bers

interdigitate,

forming

inter-

Components locking

e

within

lens

is

65%

to

70%

water

and

30%

to

35%

protein;

the

junctions

along

their

long

lateral

sides.

as

lens

ese

junctures

cortex help

to

stabilize

the

bers

so

that

the

changes

shape

in

70,71

has

a

higher

water

content

(73%–80%)

than

the

nucleus

(68%). accommodation,

the

lateral

membranes

slide

against

each

other

e proteins manufactured during lens development must be dura-

ble

because

proteins

they

within

need

the

to

lens

last

are

a

lifetime.

water

Some

soluble

80%

to

crystallins.

90%

is

of

and

remain

eral

membrane

close

lens

shape

together.

Adhesion

complexes

joining

the

lat-

the also

enable

close

contact

between

bers

during

concenchange

and

decrease

extracellular

space,

minimizing

27

tration

is

3

times

higher

than

in

typical

cells.

Lens

crystallins

are spacing

between

bers

and

decreasing

light

scatter.

from the alpha family or the beta/gamma super family. Interaction Although mature lens bers lack cellular organelles, they still

among

crystallins,

particularly

the

alpha

crystallins,

produces

a require

phenomenon

that

contributes

to

lens

transparency

and

gives

the

lens

a

signicantly

higher

index

of

refraction

than

nutrients.

e

bers

deep

within

the

lens

are

far

from

the aqueous

and

vitreous,

and

ber-to-ber

transport

is

impor-

surrounding tant.

An

intracellular

network

of

gap

junctions

facilitates

move-

28,72

uids.

Alpha

crystallins

are

molecular

chaperones

and,

as

such,

80

ment

they

stabilize

beta

and

gamma

proteins,

preventing

them

of

ions

and

small

molecules

between

bers.

e

lens

has

from a

higher

concentration

of

gap

junctions

than

other

cells

in

the

undergoing chemical changes and forming aggregates. When crysbody,

tallins

aggregate

they

undergo

a

change

in

density,

become

and

the

lens

gap

junctions

water

contain

some

channel

proteins

humor.

B ecause

16,27

that

are

unique

to

the

lens.

73

insoluble, and when of sucient size cause light scatter.

Insoluble proteins include those proteins that form the cell mem-

brane

and

the

cytoskeleton.

Actin

is

an

insoluble

protein

and

Lens

e

important

component

in

the

lens

ber

cytoskeleton.

part

of

the

cytoskeleton

and

help

to

stabilize

lens

the

ber

the

ey

may

also

have

a

role

in

transporting

vesicles

low

glucose

oxygen

from

the

concentration

aqueous

in

the

neighborhood

of

the

memlens,

brane.

obtains

Microtubules of

are

Metabolism

an

to

70%

of

adenosine

triphosphate

(ATP)

production

is

via

the anaerobic

metabolism.

Aerobic

glycolysis

and

the

Krebs

cycle

27

ends

of

the

elongating

bers.

Numerous

actin

microlaments, are

just

inside

the

cell

membrane,

are

linked

to

the

adhesive

limited

to

the

mitochondria.

between

lens

bers.

Actin

also

helps

to

maintain

epithelium

or

supercial

bers

that

still

have

junctions

crystallin

e

lens

cortex,

in

which

newer

bers

that

still

organicontain

organelles

are

present,

has

a

thickness

of

approximately

74

zation.

Lens ber membranes have the highest cholesterol content

27

100

of

human

cells

and

a

high

concentration

of

sphingomyelin.

μm.

newer

function

of

sphingomyelin

is

unclear

because

it

can

cause

ATP

activity

is

higher

in

the

epithelial

cells

and

the

near

the

e bers

of

the

cortex

near

the

equator

and

is

lower

rigidity poles.

ere

is

no

such

activity

in

the

lens

nucleus,

and

bers

in

27

in membranes and lens bers must exhibit exibility.

78

the

Formation

of

Lens

nucleus

are

not

capable

of

protein

synthesis.

Fibers

Ionic

Current

Lens ber formation is a complex and multistep process and vari-

An

ionic

ous

the

equator

current

has

been

identied

owing

out

of

the

lens

at

26,78,81,82

in

molecules

the

e

inuence

aqueous

and

concentration

the

and

the

mechanism.

vitreous,

the

Growth

accumulate

distribution

of

in

factors,

the

specic

lens

present

capsule.

factors

along

of

blood

help

and

into

vessels

circulate

in

the

the

solutes

to

lens

at

lens,

the

the

this

deep

lens

surface

inuence

direct

proliferation

cellular

and

processes.

migration

are

In

circulating

lens

75

the

poles.

bers

the

ionic

and

absence

ow

might

transport

waste

77

Growth

factors

concentrated

that

along

the

products

pathway

out

as

of

the

the

bers

ionic

and

current,

the

lens.

Fluid

facilitating

follows

water

and

the

same

metabolite

CHAPTER

7

Crystalline

44

(glucose, ascorbate, and amino acids) movement into the deeper

there

is

some

change

105

Lens

90

thereaer.

e

thickness

change

is

26

bers.

Water

spaces

at

the

and

solutes

anterior

enter

and

the

lens

posterior

through

polar

extracellular

regions,

cross

ber

accompanied

a

for ward

by

a

steepening

movement

of

the

to

the

lens

interior,

and

then

ow

through

bers

in

anterior

chamber

the

center

44

membranes

of

45

62

91

anterior

of

the

surface

lens,

back

to

the

surface

at

the

equator,

matching

the

distribution

of

lens

surface

does

e

not

and

a

decrease

92

depth.

cur vature

1

terior

cur vature,

change

with

of

the

pos-

44

age.

Other

physical

77

the

ionic

pumps

contributes

to

and

this

channels.

current

It

is

because

likely

the

that

ATPase

distribution

80

pumps

is

activity

generates

of

the

coincident

lens

more

an

with

this

negative

than

its

of

+

pattern.

electrochemical

e

gradient

Na

ATPase

changes

section

accompany

age

were

described

in

the

presbyopia

ATPase

the

interior

environment.

CLINICAL

COMMENT: The

Because

lens

should

ULTRAVIOLET

that

earlier.

+

/K

with

surrounding

activity

RADIATION

the

change,

decreases.

continues

yet

The

it

to

remains

anterior

Lens

grow,

Paradox

it

would

constant.

radius

of

seem

With

curvature

that

age,

its

the

refractive

radii

decreases

to

of

power

curvature

approximately

65

8.25

mm

and

the

posterior

radius

to

about

7

mm

by

80

years

of

age.

As

the

e cornea absorbs wavelengths below 300 nm, the lens absorbs lens

wavelengths

between

300

and

400

nm,

and

wavelengths

surface

400

nm

are

transmitted

to

the

retina.

e

lens

all

ultraviolet

radiation

to

which

it

is

exposed,

steeply

curved,

refractive

power

should

increase.

the

lens

thickness

increases

primarily

in

the

width

of

the

lens

cor-

absorbs tex,

almost

more

greater However,

than

becomes

and

and

as

the

lens

becomes

more

optically

homogeneous,

there

is

less

of

any an

effect

from

the

gradient

nature

of

the

index

of

refraction.

These

changes

83

resulting

unstable

free

radicals

cause

molecular

changes.

e

is

the

lens

radicals.

to

epithelium,

which

Morphological

irreversible

Ultraviolet

changes

is

susceptible

changes

in

throughout

radiation

absorbed

the

the

by

to

damage

epithelial

from

layer

may

association

exists

between

tion

also

risk

of

lens

increases

remains

the

lens

Changes

bers

causes

ultraviolet

for

the

increased

surface

curvatures,

and

the

power

stable.

free

lens.

lens

ocular

84

increased

compensate

of

lead

oxidative

damage, leading to degradation and modication of lens proteins.

An

apparently

93–96

rst active tissue of the lens that encounters ultraviolet radiation

exposure

and

lose

all

port

occur

cellular

of

ions,

in

lens

physiolog y

organelles.

nutrients,

A

as

coincident

and

mature

decrease

antioxidants

may

lens

in

bers

the

lead

trans-

to

dam-

97

age

that

contributes

to

cataract

formation.

With

age,

there

85

opacity.

Ultraviolet

chromophore

radiation

concentration;

yellow

absorp-

pigments

is

an

increase

pumps

may

in

not

ber

be

membrane

able

to

permeability,

compensate,

and

disrupting

the

ion

ionic

balance.

83

accumulate in the center of the lens.

e yellowing may progress

Circulation

within

the

lens

changes

and

restriction

of

the

ow

29

to

a

dark-brown

hue,

which

is

called lens brunescence

of

water

and

Signicant

glutathione

changes

in

occurs

at

aquaporins

the

cortex/nucleus

occur,

also

causing

border.

a

disrup-

98

tion

OXIDATIVE

of

e

the

by

cellular

rate

of

free

ow.

STRESS

Free radicals are generated both by ultraviolet radiation absorption

and

water

metabolic

radical

processes.

production

Oxidative

is

greater

stress

than

results

the

rate

when

of

their

degradation. Oxidative stress can impair the structure and function

of connexins (gap junction proteins), modify lens crystallins, cause

aggregation of proteins, and result in deoxyribonucleic acid (DNA)

age,

in

amount

and

the

vent

by

lens

other

of

age

water

40

soluble

years,

nucleus.

there

Because

cr ystallins

from

the

increase

with

cr ystallins

no

alpha

alpha

forming

86

aggregates

alpha

are

decreases

cr ystallins

cr ystallins

aggregates,

help

water

with

evident

to

pre-

insoluble

99

age.

Some

components

of

the

cyto-

100

skeleton

in

the

disassemble.

lens

decrease

Levels

of

ultraviolet

approximately

12%

radiation

per

decade,

lters

allowing

86 87 72

damage, all of which contribute to cataract development.

Glutathione

and

is

the

is

main

a

reducing

factor

in

agent

that

preventing

detoxies

such

increased

free

damage

radicals

within

the

ultraviolet

Clinical

radiation

manifestations

formation.

Both

of

processes

damage.

aging

aect

are

presbyopia

vision

and

are

and

a

cataract

signicant

87

lens.

It

is

aqueous

found

humor

in

high

and

is

concentration

transpor ted

into

within

the

the

lens

lens

from

and

the

the

aque-

ous. It can be synthesized and regenerated by the lens epithelial

concern

few

to

the

patient

preventive

patients

and

measures

should

include

to

the

are

the

clinician,

available.

use

of

particularly

because

Recommendations

ultraviolet

radiation

to

absorb-

77

cells

and

young

lens

bers.

e

deeper

bers

rely

on

diusion

ing

lenses

when

outdoors,

as

the

incidence

of

cataract

is

higher

69

of

glutathione

from

supercial

bers.

Glutathione

also

has

a

83

in

those

exposed

to

greater

levels

of

sunlight.

88

role

in

maintaining

Ascorbic

acid,

membrane

which

is

transpor t

present

in

mechanisms.

relatively

high

levels

in

the

aqueous humor, also provides some protection against oxidative CLINICAL

damage to DNA within the lens epithelium. It also prevents per-

68

oxidation

of

the

lipid

membrane

and

protects

cation

Although

COMMENT: Cataracts

any

lens

opacity

is

accurately

called

a

cataract,

the

clinician

should

89

pumps.

be

aware

racts

are

of

the

the

impact

leading

that

cause

the

of

word

cataract

blindness

may

worldwide,

have

on

a

particularly

patient.

in

Cata-

middle

and

101

low-income

AGING

CHANGES

IN

THE

CRYSTALLINE

countries.

The

etiology

of

cataract

formation

is

complex,

and

LENS cataract

development

is

often

the

result

of

multiple

factors,

including

oxida-

99

tive

Epithelial

cells

migrate

from

the

proliferate

zone

to

form

stress.

bolic

lens

bers

causing

the

lens

to

grow

throughout

life.

e

Risk

factors

include

aging,

disease,

genetics,

deciencies,

trauma,

congenital

factors,

and

major102

radiation),

ity

of

the

increase

in

thickness

occurs

before

age

50

nutritional

or

meta-

new

years,

but

with

age

being

the

major

contributor.

environmental

stress

(e.g.,

CHAPTER

106

Cataracts

severity

called

onset

are

(Fig.

a

of

named

7.11).

nuclear

a

according

An

opacity

cataract

nuclear

7

to

location

located

(Fig.

cataract

Crystalline

7.12).

can

in

The

increase

or

the

cause

Lens

and

embryonic,

center

can

be

fetal,

opacication

refractive

power.

In

graded

or

adult

based

accompanying

a

on

nucleus

hyperopic

is

the

patient,

this myopic shift causes a temporary improvement in vision. Brunescence accom-

panies

nuclear

cataracts

caused

by

increased

chromophore

concentration.

The

increase in yellow coloration results in the absorption of wavelengths in the blue

end of the spectrum, which may actually provide some protection for the macula.

A

cortical

periphery

bers

cataract,

and

(Fig.

located

tapering

7.13).

in

the

toward

Cortical

cortex,

the

lens

cataracts

has

a

spoke-like

center,

generally

it

follows

progress

shape;

the

thicker

shape

slowly.

With

103

spoke

width

expands

as

the

opacity

spreads

to

adjacent

of

in

the

the

lens

time,

the

Fluid

ac-

104

bers.

105

cumulates,

cataracts

cause

and

membrane

affect

light

vision

scatter

in

rupture

only

the

when

in

the

they

pupillary

equatorial

spread

into

area

the

can

occur.

center

of

Cortical

the

lens

and

region.

A posterior subcapsular cataract is a disturbance located just beneath the posterior

Fig. 7 .12

Nuclear

cataract

seen

with

an

optic

section. (Courtesy

capsule (Fig. 7.14). This type of cataract impacts vision early and signicantly given

Lorne its

location

along

the

visual

axis

and

near

the

nodal

point

of

the

eye.

A

Y udcovitch,

Pacic

University

Family

Vision

Center,

Forest

accumulation

aects

signicant

Grove,

Ore.)

risk factor for posterior subcapsular cataracts is long-term, high-dose steroid use.

oxidative

THE

PHYSIOLOGY

OF

CATARACT

cellular

Numerous

mechanisms

are

presumed

damage

as

a

result

of

free

radical

FORMATION

to

cause

cataracts,

tion,

function,

and

causes

damages

lens

DNA,

causes

high-molecular-weight

protein

cr ystallin

modica-

aggregations,

29

including

uid

and

ion

imbalance,

oxidative

damage,

protein

any

of

which

can

increase

light

scatter.

Alpha

cr ystallins,

as

74

modication, and metabolic disruption.

regulation

can

membrane

+

tion.

If

Na

be

caused

permeability

by

ionic

increase

A disturbance in uid

pump

that

dysfunction

allows

water

molecular

and/or

chaperones,

conguration.

accumula-

peared

from

By

the

age

lens

help

40

to

stabilize

years,

nucleus,

beta/gamma

alpha

although

cr ystallins

the

normal

+

cr ystallin

have

lens

disap-

usually

106

/K

ATPase

pump

activity

decreases

signicantly,

an

remains

fairly

transparent

for

years

past

that

age.

As

the

con-

+

increase

in

Na

in

the

cytoplasm

is

accompanied

by

an

inux

centration of alpha cr ystallins is reduced, aggregates accumulate

78

of

water,

lens

bers

swelling,

and

diminished

transparency.

and

with

time

form

light-scattering

opacities.

++

An

increased

level

of

cytoplasmic

Ca

is

also

associated

with

Glutathione

and

ascorbate

maintain

a

reducing

environ-

78

a

loss

of

transparency.

can

form

vacuoles

and

increased

Water

causing

a

accumulation

disruption

of

between

ber

bers

ment

arrangement

and

providing

preventing

some

protein

protection

from

modication.

free

radical

Reduced

levels

damage

of

gluta-

86

light

scatter

(Fig.

7.15).

Ultraviolet

radiation

and

thione

allow

oxidative

damage

to

membranes

e cnecselapO

/roloC

raelcuN

NO1

NC1

NO2

NC2

NO3

NC3

NO4

NC4

NO5

NC5

NO6

NC6

lacitroC C1

C2

roiretsoP

7 .1 1

upper

of

&

Grading

row.

bottom

JA,

C4

C5

raluspacbuS P1

Fig.

C3

Cortical

row.

L T .

for

changes

Cortical

Chylack

P2

system

and

Clinical

phacoemulsication.

are

in

posterior

Cataract

the

cataracts.

middle

subcapsular

application

J

P3

age-related

of

the

Refract

lens

row,

P4

Nuclear

and

changes

posterior

are

opacities

Surg.

sclerotic

seen

P5

changes

subcapsular

in

are

retroillumination.

classication

2003;29(1):138-145.)

system

shown

cataracts

III

in

are

(From

the

in

the

in

the

Davison

performance

and

proteins.

CHAPTER

cortex

into

the

nucleus

7

and

Crystalline

might

107

Lens

account

for

the

reduction

105

of

glutathione

nexins

in

between

97

gap

the

nucleus.

junctions

bers

and

causes

might

be

A

a

modication

disruption

one

cause

of

in

of

the

con-

communication

this

barrier

forma-

108

tion.

Changes

innermost

and

in

by

occur

nuclear

middle

age

in

regions

(age

aquaporin

of

the

40–50

channel

lens

years),

as

proteins

early

half

of

as

age

in

5

the

years,

such

channels

ese

changes

are

98

lost

in

lead

the

the

to

region

the

barrier

of

the

occlusion

of

the

water

barrier.

channels

and

can

contribute

to

function.

Diabetes-Related

Cataracts

speculated

are

more

Cataract

common

in

diabetic

patients

compared

with

109

nondiabetic

cr ystallin Fig.

7 .13

Spokes

of

a

cortical

patients.

is

concentration,

may

in

part

oxidative

be

stress,

caused

or

by

altered

genetic

altera-

cataract. 109

110

tions.

In

addition,

with

increased

blood

glucose,

excess

glu-

cose present in the aqueous enters the lens. As this excess glucose

is metabolized, sorbitol accumulates faster than it is converted to

fructose. Because sorbitol does not readily pass through the ber

membrane,

the

concentration

of

sorbitol

increases

within

the

lens bers which draws water into the bers. e bers swell, the

lens

loses

transparency,

Age-Related

High

lifetime

increased

most

Cortical

exposure

incidence

severe

and

of

damage

the

may

eventually

rupture.

Cataract

to

ultraviolet

cortical

in

bers

radiation

cataracts.

cortical

e

cataracts

is

associated

paradox

occurs

near

is

with

that

the

the

equator

initially, the area most protected from sunlight by the iris. Cortical

cataracts

ity

and

are

ion

associated

with

transporters,

increased

pumps,

and

membrane

exchangers

permeabil-

are

not

able

to

80

maintain

the

homeostatic

concentration.

An

increased

concen-

++

tration Fig. 7 .14

of

Ca

in

the

ber

cytoplasm

also

drives

uid

accumula-

Posterior subcapsular cataract seen on retroillumination. 78

tion.

Aected

regions

of

the

ber

show

disruption

of

structure

and can include membrane rupture. e changes rst occur in the

center of the elongated ber (that is at the equatorial region), with

the

apical

tapered

and

ber

basal

ends,

ends

remaining

located

at

the

transparent.

sutures

in

the

In

general,

optical

the

axis,

are

only aected very late in the process of cortical cataract formation.

Age-Related

Nuclear

Cataract

Age-related

nuclear

cataracts

glutathione,

making

the

Binding

of

alpha

are

bers

crystallins

associated

susceptible

to

the

lens

with

to

a

decline

oxidative

membranes

of

damage.

that

occurs

between age 40 and 50 years occludes the membrane pores dimin-

ishing

the

molecules

movement

out

of

the

28

a

nuclear

reduced

99

in

the

normal

nucleus

aer

and

Levels

into

may

the

lead

nucleus

to

the

and

reactive

development

while

of

glutathione

levels

in

the

can

be

of

cortex

signicantly

remain

within

108

range.

signicantly

glutathione

111

cataract.

88

the

of

nucleus

Oxidative

age

50

years,

protein

modication

contributing

to

the

increases

damage

seen

106

in

age-related

accompany Fig.

7 .15

Lens

nuclear

nuclear

sclerosis.

cataracts

are

e

color

usually

seen

changes

as

that

various

oen

hues

of

vacuole. 105

yellow or brown; this pigmentation is primarily protein-bound.

A

decrease

in

glutathione

concentration

is

associated

with

Posterior

Subcapsular

Cataract

69,106,107

cataract

in

development.

middle

nucleus,

age

seems

and

to

A

located

impede

at

the

barrier,

the

ow

speculated

interface

of

small

of

the

to

develop

cortex

molecules

from

and

the

An

opacity

thelial-like

cells

in

the

cells

accumulate

posterior

that

at

subcapsular

migrate

the

from

posterior

the

pole

region

is

formed

equatorial

forming

by

region.

an

epi-

ese

opacity.

It

is

CHAPTER

108

7

Crystalline

Lens

speculated that radiation damage is one causative factor as patients

undergoing

radiation

therapy

for

cancer

treatments

develop

10.

27

terior

subcapsular

cataracts

and/or

cortical

induced

cataracts

are

also

located

in

the

posterior

region.

Dosage

and

the

duration

of

steroid

use

appear

controlling

factors,

although

individuals

may

have

varying

of

susceptibility.

Children

develop

such

cataracts

at

R,

Iribarren

R,

etal.

population-based

Lens

study.

Br

power

J

in

Iranian

Ophthalmol.

He

J,

Lu

a

L,

He

and

X,

etal.

refractive

e

error

relationship

in

older

between

Chinese

cr ystalline

adults:

e

lens

Shanghai

study.

PLoS

ONE.

2017;12(1):p.e0170030.

lev12.

els

a

to eye

be

Pakzad

sub-

power

capsular

H,

2018;102(6):779–783.

cataracts.

11.

Steroid

Hashemi

schoolchildren:

pos-

faster

Garner

LF ,

Smith

G.

Changes

in

equivalent

and

gradient

refrac-

rate tive

index

of

the

cr ystalline

lens

with

accommodation.

Optom

Vis

74

than

do

adults.

Reversal

of

the

cataract

can

occur,

but

this

is

rare. Sci.

1997;74(2):114.

e opacity appears to be formed of undierentiated epithelial cells 13.

at the interface of the posterior cortex and capsule. ese misplaced

cells

(which

aberrant

from

should

behavior.

the

only

e

preequatorial

be

present

in

the

lens

undierentiated

cells

area,

by

inuenced

epithelium)

may

a

have

change

display

the

of

growth

factors.

Growth

factors

governing

mitosis,

Vis

15.

and

dierentiation

are

obtained

from

inuence

production

aqueous

Ţălu

in

the

lens

capsule.

If

steroids

of

factors

in

the

aqueous,

and

the

concentration

and

Refraction.

Ş,

Handelman

cur vature

3rd

ed.

Chicago:

Professional

as

GH,

a

Brown

function

NP .

of

Analysis

of

human

accommodative

state

cr ystal-

and

age.

1984;24:1141.

Sueiras

anterior

VM,

human

Moy

lens

VT,

etal.

capsule.

Micromorpholog y

Mol

Vis.

analysis

of

2018;24:902–912.

Kuszak

JR,

Brown

HG.

Embr yolog y

and

anatomy

of

the

lens.

In:

these Albert

growth

Clinical

and

16.

reside

JF ,

lens

Res.

the

migration,

IM.

1975:169.

Koretz

line

con-

74

centration

14.

migrated

in

Borish

Press;

DM,

Jakobiec

FA,

eds.

Principles

and

Practice

of

Ophthal-

location molog y.

Philadelphia:

Saunders;

1994:82.

74

in the capsule is altered, cellular processes can be aected. 17.

Barraquer

thickness

18. CLINICAL

COMMENT: Cataract

decision

on

the

for

cataract

patient’s

removal

everyday

life.

is

a

R,

function

Invest

Alexander

RA,

Abreu

of

age

Ophthalmol

Garner

A.

R,

and

Vis

etal.

Sci.

Elastic

Human

location

lens

along

the

capsule

sagittal

lens

2006;47:2053–2060.

and

precursor

bres

in

the

nor-

Surgery

determined

by

the

effect

the

When

a

person

is

not

able

to

human

eye.

Exp

Eye

Res.

1983;36:305.

cataract

19. has

as

Michael

perimeter.

mal The

RI,

perform

Kuwabara

T.

e

maturation

of

the

lens

cell:

a

morphologic

study.

the

Exp

Eye

Res.

1975;20:427.

usual daily activities because of reduced vision caused by the opacity, the lens

20. should

be

removed.

Cataract

extraction

is

a

relatively

safe

surgical

Bassnett

tion usually

done

under

local

or

topical

anesthesia.

A

small

incision

S,

Kuszak

JR,

Reinisch

L,

etal.

Intercellular

communica-

procedure

is

made

between

epithelial

and

ber

cells

of

the

eye

lens.

J

Cell

Sci.

to

1994;107:799. allow

entrance

of

surgical

instruments

into

the

anterior

chamber.

The

anterior

21. lens

capsule

is

opened

and

the

lens

epithelium

and

all

bers

are

Rae

J.

Physiolog y

Principles leaving

the

remaining

lens

capsule

intact.

An

intraocular

lens

of

the

lens.

In:

Albert

DM,

Jakobiec

FA,

eds.

removed,

(IOL)

can

and

Practice

of

Ophthalmolog y.

Philadelphia:

Saunders;

then

1994:123. be

inserted

into

the

lens

capsule

to

replace

the

power

of

the

missing

lens.

22. Multifocal

IOLs

that

correct

for

presbyopia

may

be

an

Kuszak

JR,

Novak

LA,

Brown

HG.

An

ultrastructural

analysis

of

option.

the

epithelial-ber

interface

(EFI)

in

primate

lenses.

Exp

Eye

Res.

1995;61:579.

23.

Lo

in

WK,

lens

Harding

CV .

epithelium

Structure

and

ber

and

cells.

distribution

Cell

Tissue

of

Res.

gap

junctions

1986;244(2):253.

REFERENCES 24.

Hejtmancik

Transl 1.

Birkenfeld

J,

de

Castro

A,

Marcos

S.

Contribution

of

shape

25. gradient

human

refractive

lenses.

index

Invest

to

the

spherical

Ophthalmol

Vis

Sci.

aberration

of

Rosales

P ,

Wendt

M,

Marcos

S,

etal.

Kuszak

JR,

vations

of

of

cur vature

in

cr ystalline

and

in

lens

rhesus

tilt

and

decentration

monkeys.

J

Mathias

Vis.

Doyle

L,

Little

J,

Saunders

K.

during

measures

with

age

and

of

the

lens.

Prog

Mol

Biol

Peterson

the

KL,

Brown

cr ystalline

lens.

HG.

Electron

Microsc

Res

microscopic

Tech.

obser-

1996;33:441.

RT,

Kistler

J,

Donaldson

P .

e

lens

circulation.

J

Membr

2007;216:1–16.

dynamic

Repeatability

of

OCT

lens

Beebe

DC.

accommodation.

Optom

of

the

e

Eye.

lens.

10th

In:

ed.

Kaufman

St

Louis:

PL,

Alm

Mosby ;

A,

eds.

Adler’s

Physiol-

2003:117.

thick-

28. ness

Over view

2008;8(1):18.1-12.

og y 3.

A.

lens

27. accommodation

Shiels

2014;55:2595–2607.

Changes

Biol. radii

JF ,

2015;134:119–127.

isolated

26. 2.

Sci.

and

Vis

Su

SP ,

Mcarthur

JD,

Friedrich

MG,

etal.

Understanding

the

Sci.

α-cr ystallin

cell

membrane

conjunction.

Mol

Vis.

2011;17:2798–

2013;90(12):1396–1405.

2807. 4.

Jonas

JB,

Nangia

V ,

Gupta

R,

etal.

Lens

thickness

and

associated

29. factors.

Clin

Exp

Ophthalmol.

Vavvas

D,

Azar

Ophthalmol 5.

Erb-Eigner

K,

Hirnschall

N,

Hackl

C,

etal.

Predicting

lens

ocular

biometr y

with

high-resolution

MRI.

Invest

mol

Vis

Clark

JI.

Sci.

MJ,

DT.

Mechanisms

of

disease:

cataracts.

2002;15:49.

Jakobiec

and

FA,

maintenance

eds.

Principles

of

lens

and

transparency.

Practice

of

In:

Ophthal-

2015;56(11):6847–6854.

Alvarado

JA,

Weddell

JE.

Lens.

In:

Histolog y

of

Eye.

Philadelphia:

Saunders;

Philadelphia:

Saunders;

1994:114.

the

31. Human

Azar

Am.

Development

DM,

molog y. Hogan

N

Ophthal-

Albert

6.

Clin

diam-

30. eter :

NF ,

2012;40(6):583–590.

Mathias

RT,

Rae

JL.

Transport

properties

of

the

lens.

Am

J

Physiol.

1971:638–676.

1985;249(3):181. 7.

Strenk

SA,

Semmlow

JL,

Strenk

LM,

etal.

Age-related

changes

32. in

ciliar y

muscle

and

lens:

a

magnetic

resonance

imaging

Dahm

R,

van

Marle

Ophthalmol

Vis

Sci.

Jones

CE,

Atchison

DA,

Prescott

(MP70)

in

AR,

the

etal.

adult

Gap

junctions

mammalian

lens

containing

epithe-

1999;40:1162.

lium 8.

J,

study.

alpha8-connexin Invest

Pope

JM.

Changes

in

lens

suggests

a

re-evaluation

of

its

role

in

the

lens.

Exp

Eye

Res.

dimensions

1999;69:45. and

refractive

index

with

age

and

accommodation.

Optom

Vis

Sci.

33.

Kuszak

JR,

Peterson

KL,

Sivak

JG,

etal.

e

interrelationship

of

2007;84:990–995.

lens 9.

Rosen

AM,

Denham

DB,

Fernandez

V ,

etal.

In

vitro

anatomy

and

dimensions

1994;59(5):521. and

cur vatures

of

human

lenses.

Vis

Res.

2006;46:1002–1009.

optical

quality,

II

Primate

lenses.

Exp

Eye

Res.

CHAPTER

34.

Fagerholm

tinuity

35.

Bahrami

of

the

Res.

36.

in

De

M,

lens:

Philipson

human

Hoshino

an

BT ,

lens.

M,

Lydahl

E.

Ophthal

Subcapsular

Res.

Pierscionek

explanation

for

the

zones

1990;22(Suppl

B,

etal.

zones

of

Optical

of

discon-

54.

1):S51–S55.

properties

discontinuity.

Exp

A,

bovine

Wilmarth

and

human

PA,

David

ciliar y

LL,

zonule.

etal.

Proteomic

55.

Eye

Invest

analysis

Ophthalmol

Vis

of

56.

Sci.

Bourge

lar

Robert

composition

Pathol

38.

JL,

Biol

Rohen

JW .

apparatus

to

G.

Zonular

function

bers,

(elasticity)

multimolecu-

and

57.

patholog y.

human

Flügel‐Koch

located

tion.

40.

electron

and

microscopic

monkey

eyes.

studies

Invest

of

the

zonular

Ophthalmol

Vis

58.

Sci.

CM,

zonular

Ophthal

Cro

bres

Physiol

MA,

as

a

Kaufman

tool

Optic.

for

ne

PL,

etal.

Anteriorly

regulation

in

59.

accommoda-

42.

Helmholtz

2016;36(1):13–20.

muscle,

during

Clin

A,

by

tomography.

Richdale

K,

age-related

45.

and

ciliar y

mol

Vis

60.

Optom

LT,

per

muscle

61.

A,

NY:

62.

the

dynamic

and

changes

anterior

OCT.

D,

in

the

63.

Arch

etal.

Dynamic

Refract

Surg.

Bullimore

the

optical

of

accom-

coherence

MA,

etal.

emmetropic

Bullimore

Sci.

and

MA,

eye.

of

the

Invest

of

66.

lens

E,

Sun

coherence

tomography

equatorial

diameter,

M,

based

and

LT,

error

etal.

on

e

the

eect

adult

Ophthal-

67.

of

age,

human

Glasser

A,

St

49.

Louis:

Drexler

Kaufman

PL,

Alm

Mosby ;

W ,

estimates

of

position.

M,

etal.

cr ystalline

Invest

Optical

myopes.

50.

Cro

ments

the

in

Invest

MA,

of

in

the

to

Adler’s

lens

volume,

Ophthalmol

Vis

69.

Sci.

humans:

G,

and

Physiolog y

lens/capsule

vitreous

the

Vis

and

zonule

vitreous

L,

etal.

dierences

Sci.

Mcdonald

of

presbyopia.

the

Eye.

In:

10th

70.

elongation

between

strand

and

Eye

etal.

insertion

face

71.

Koretz

rhesus

ness

JF ,

Bertasso

monkey

and

eye,

position

II

Neider

Changes

during

emmetropes

and

73.

Accommodative

that

zone

aging.

extends

&

the

Ophthal

move-

MW ,

in

Fisher

RF .

thalmol

53.

e

Soc

Consejo

A,

vitreous

etal.

between

lens

74.

equator,

Physiol

Slit-lamp

cr ystalline

accommodation

and

lens

in

accommodation.

Ophthal

H,

Fan

e

T T.

and

Surg.

Change

eye

resonance

with

of

imaging

pseudophakic

in

age.

ciliar y

of

muscle

2006;32:1792–1798.

Anterior

human

RC,

etal.

anterior

age

on

index

shi

of

zonular

cr ystalline

e

lens

relationship

capsule

some

and

ocular

contours

Mechanical

Invest

MC.

human

inser-

with

age.

between

zonules.

Invest

basement

in

the

properties

Ophthalmol

Biometric

cr ystalline

mem-

human

lens.

Exp

Vis

optical

lens

with

of

Sci.

and

age

the

human

2003;44:691.

physical

in

changes

relation

to

pres-

1999;39:1991.

Heijde

GL.

Age-related

Optom

change

in

physical

lens

basis

Ophthalmol.

Duncan

lens

and

studies

shape,

aging.

of

the

Vis

Sci.

changes

in

the

accom-

1996;73(4):235.

cur vature

with

age.

Exp

Eye

Res.

for

transparency

of

the

cr ystalline

1962;1:493.

MK.

Eye

accommodation.

Trans

Iskander

Optic.

DR.

Scleral

e

lens

capsule.

Exp

Eye

Res.

Res.

with

2017;37(3):263–274.

RG,

Pierscionek

opportunities

deliver y

to

the

B.

Age‐related

and

lens.

J

challenges

Pharm

cata-

for

Pharmacol.

X,

Monnier

Cell

JF .

Dev

RJ.

Biol.

condition.

Eye

Exp

L,

AI,

of

the

Res.

Eye

glutathione

standing

Res.

in

homeostasis:

the

way

of

novel

2017;156:103–111.

and

their

Physiolog y,

Jordan

Emerging

molecular

genetics.

Butter worth

Hill;

from

basis

Heinemann,

1996:41.

a

for

blur

this

towards

most

an

common

eye

2009;88:241–247.

CM.

Res.

Augusteyn

PS,

Eye

molecular

Sorensen

Exp

Lens

cataracts

UK:

Protein-protein

interactions

and

lens

2008;87:496–501.

RC.

steroid-induced

Optom.

Z elenka

Exp

Ocular

Presbyopia.

of

J.

knowledge

2008;19:134–149.

Oxford,

understanding

Jobling

in

Congenital

Clinical

House.

Takemoto

Whitson

gaps

approaches.

HNV .

Truscott

VM,

and

What

induces

posterior

steroid

subcapsular

cataracts?

cataracts.

A

Clin

2002;85:61–75.

Arpitha

migration

in

P .

the

C oordinating

lens

cell

and

cornea.

role

of

proliferation

Semin

Cell

Dev

Bio.

2008;19:113–124.

76.

Oph-

changes

Alany

therapy :

antioxidant

Chong

and

thick-

Exp

H,

drug

Hejtmancik

Exp

Rao

PV ,

Maddala

cell

R.

elongation

e

and

the

lens

dierentiation.

actin

cytoskeleton

Semin

Cell

Dev

Donaldson

volume:

PJ,

Chee

implication

2009;88:144–150.

KS,

for

Lim

lens

JC,

etal.

Regulation

transparenc y.

E xp

of

Eye

in

Biol.

2006;17:698–711.

77.

Physiol

Magnetic

etal.

of

Refractive

der

e

BP ,

and

review

Optic.

1982;102:318.

Radhakrishnan

etal.

1991;32:2835–2839.

mechanism.

Abdelkader

ber

UK.

the

inuence

Res.

transparency.

1987;45:317.

52.

S.

Danysh

75.

AM,

SJ,

surface

capsule.

van

N.

Linacre

during

2016;36(1):21–32.

51.

Refrac

of

Campbell

Invest

Semin

ed.

1998;39(11):2140.

JP ,

the

S.

phakic,

Morgan

Sci.

BK.

discrepancies

72.

Schmetterer

Ophthalmol

Heatley

posterior

relation

O,

A,

therapeutic

Accommodation

eds.

GL,

human

2015;67(4):537–550.

2003:197.

Findl

accommodation

PL.

A,

Trokel

ract

Johnson CA. Eects of luminance and stimulus distance on accom-

Kaufman

the

1987;1:184–189.

lens

AP ,

Brown

68.

eye.

modation and visual resolution. J Optic Soc Am. 1976;66:138–142.

48.

Heijde

of

1997;64:887.

Vis

topical

Velasco-Ocana

plane

der

lens

Koretz JE, Strenk SA, Strenk LM, etal. Scheimpug and high resolu-

lens.

2016;93(1):3–11.

Martinez-Enriquez

van

the

2009;88:151–164.

Sinnott

refractive

muscle.

1974;19:175.

Quantication

changes

human

ciliar y

tive study. J Optic Soc Am. A Optic Image Sci Vis. 2004;21:346–354.

65.

2015;41(3):501–510.

accommodative

e

modation

64.

human

tion magnetic resonance imaging of the anterior segment: a compara-

imaging

segment

Beers

DJ,

Vis

isolated

byopia.

chamber

Graefe’s

the

in

1998;105(2):295.

Andreassen

Glasser

M,

on

Guo

Lim

capability

Eye.

S,

T,

anterior

Apple

RF .

Res.

Krag

LM,

Cataract

Pierscionek

in

Monsálvez-Romín

high-resolution

anterior

diopter

in

A,

morpholog y,

a

Mineola,

1962:143.

2016;57(9):OCT600–OCT610.

47.

J

the

posterior

2013;54(2):1095–1105.

K,

Vis

Protti

Sinnott

accommodation,

46.

with

of

Optics.

Fisher

Eye

2017;255(7):1385–1394.

Cataract

and

Sci.

Richdale

M,

lens

swept-source

J

Physiologic

measurements

cr ystalline

Ruggeri

on

Southhall);

Domínguez-Vicent

Ophthalmol.

modation

44.

JPC

accommodation

Exp

Neri

J,

Treatise

by

Non-invasive

ciliar y

43.

HH.

(Translated

Esteve-Taboada

etal.

Strenk

Oshika

EI,

branes.

monkey eyes. Invest Ophthalmol Vis Sci. 2010;51(3):1554–1564.

Von

I,

onto

Assia

force

accommodating,

Sakabe

changes

109

Lens

2008;48:119–126.

SA,

stretching

Lütjen-Drecoll E, Kaufman PL, W asielewski R, etal. Morphology

Dover

Res.

Ophthalmol

and accommodative function of the vitreous zonule in human and

41.

Vis

Strenk

Age-related

Dubbelman

Ophthalmolog y.

1979;18:133.

39.

EA,

J.

Crystalline

2000;77:204.

accommodative

tion

2007;55:347–359.

Scanning

in

Renard

related

(Paris).

Hermans

Sivak

Sci.

diameters.

AM,

as

MT,

Vis

the

aging,

2017;58(1):573–585.

37.

Pardue

Optom

2014;124:93–99.

Maria

the

P ,

the

7

lens

Res.

CHAPTER

110

78.

Delamere

Tink

J,

NA,

NJ:

79.

in

Humana

B assnett

and

Tamiya

Barnstable

Transporters

S,

CJ,

Crystalline

S.

Lens

eds.

Press;

Na+,

Lens

K+-ATPase.

Ophthalmolog y

Ophthalmic

B e eb e

nuclei

7

Diseases

and

In:

Research:

Drug

Tombran-

Delivery.

dur ing

le ns

f ib er

c el l

loss

of

mito chond r i a

d i f fe re nt i at ion .

Dev

97.

D y n.

80.

Delamere

concepts

NA,

to

Tamiya

S.

Lens

ion

regulation

of

Na+,

transport:

K-ATPase

from

activity.

Exp

Eye

Res.

98.

81.

Berthoud

Biol.

82.

Y oung

Vis

84.

element

West

and

e

87.

SK,

KR.

of

aging

eye:

for

VN.

over view.

Reddy

ascorbate

lium.

90.

Beyer

J

J

Eye

Res.

FJ,

MC,

human

van

Alió

Schimchak

measured

Vis

Biomed

eye

diseases.

epithelium

in

etal.

BK.

by

YE.

of

lens

Reactive

oxygen

102.

Arch

metabolically

and

onset

in

active

the

cataract—A

and

103.

and

with

novel

broad

detoxication

platform

its

function

in

LR,

etal.

Vis

Sci.

e

oxidants

in

105.

the

of

aqueous

damage

in

lens

changes

Heijde

in

cr ystalline

etal.

lens

A

obtained

Negri

Eye

DA,

Liu

YC,

Weeber

from

HA.

e

corrected

HP ,

etal.

response

Res.

of

thickness.

108.

optical

109.

JM.

and

of

the

changes

human

micro-imaging

in

accommodation

Truscott

ibault

human

Exp

Eye

RJ,

in

D,

lens

Res.

MG.

Truscott

of

lens

and

presby-

etal.

Age-related

normal

human

changes

lenses.

Exp

etal.

Protein

regions

is

a

aging:

trunca-

continuous

age-

2009;88:966–973.

e

don’t

RJ.

lens:

life.

M,

etiolog y

last

of

forever.

Membrane

profound

Invest

Kim

lens

Klein

Harris

due

folds,

Vrensen

the

human

BBA

-

age-

Gen

association

changes

Ophthalmol

T,

etal.

BE,

take

Vis

Cataracts.

Klein

Beaver

to

ML,

lens

R.

Dam

bre

Shun-Shin

bre

breaks,

breaks?

Sub.

of

proteins

place

in

Sci.

e

Lancet.

Ultraviolet

Eye

GA,

e

watercles

as

Willekens

Vis

Truscott

Age-related

Eye

RJ.

Res.

Sweeney

in

Study.

light

Am

J

exposure

Public

etal.

Is

cortical

relationship

and

spoke

spoke

between

cataract.

Eye.

MH,

RJ.

L,

MH,

XH,

cell

Res.

Y ong

Y ,

MG,

can

be

scanning

human

lens.

electron

Invest

is

the

key.

Eye

to

glutathione

possible

cataract:

An

a

impediment

lenses:

Res.

diu-

precondition

for

lens

transport

prob-

1

C,

etal.

of

the

risk

Dierential

cataract

Large-scale

normal

mild

diu-

precondition

for

of

cataract

in

and

protein

age-related

2015;61(2):74–80.

RJW .

aged

glutathione

2014;14:94.

diabetic

Biol.

to

possible

Meta-analysis

Zhaodon

by

a

1998;67:587–595.

Ophthalmol.

Folia

induced

a

1998;67:587.

nuclear

RJ.

type

of

impediment

2000;32:185.

Truscott

membranes

Sci.

and

aging

cataract-oxidation

lenses:

Res.

GH.

BMC

between

An

human

Exp

Zhao

patients.

Friedrich

RJ.

Eye

Truscott

diabetes.

Y ,

Exp

normal

cataract.

Wan

2

the

nuclear

human

Age-related

older

Qianqian

Vis

Truscott

Ophthalmol

in

in

1990;31(8):1582.

normal

cataract.

Sweeney

that

Sci.

Biomicroscopy

opacities

2005;80:709–725.

older

Truscott

Li

early

B.

Ophthalmol

to

Vis

G,

of

cataract

in

vitro.

KJ,

opacities:

expression

111.

Age-related

power

resonance

110.

to

1995;60:325.

Pope

the

1992;82(12):1658.

nuclear

thickness

lenses

Y ,

in

microscopy

lem.

simple

2005;112:2022–2029.

human

0

human

Wilkins

NP ,

nuclear

Scheimpug

lens

focus:

transport

proteins

decade

lens

Brown

type

Cr ystalline

in

Friedrich

MG,

Cruickshanks

sion

Ophthalmology.

distribution

magnetic

GL,

RJW ,

h

epithe-

107.

V ,

aging

and

2008;91:207–225.

KA,

Berr y

process.

aging

sion

2001;78(6):411.

aging.

Exp

the

humor

1998;39(2):344.

Garcia

A,

cataract,

Friedrich

Exp

lens—an

106.

eect

DNA

MA,

104.

therapeutic

of

the

1993;7:672.

the

1990;50:771–778.

lens

P ,

Truscott

bre

mitochon-

of

of

index

1999;69(6):663.

cataract

and

initiation

eye

water

aquaporin

Health.

junctions,

species

shape

2017;390(10094):600–612.

exposure

gap

e

refractive

2009;50:4786–4793.

development

study.

of

e

of

GL.

2001;41:1867.

Landman

Korlimbinis

in

Optom

2009;11:339–353.

antioxidants

Age-related

2002;42:1683.

stress,

Signal.

Díez-Ajenjo

Sci.

Atchison

index

Res.

Heijde

equivalent

2016;1860(1):192–198.

Eng

101.

Sunlight

BA,

der

Optom.

kinetics

related

a

2016;23(1):e98–e117.

Lin

der

through

forces.

BA,

refractive

Res.

of

2011;21(5):597–603.

Optom

Pierscionek

B,

function

age-related

images.

JL,

lens

Oxidative

role

lens

er.

of

aging

the

and

regulation

M,

Moat

Development

population-based

Redox

Ophthalmol

of

Moat

dependent

Cell

1995;14:71.

a

maturity

Dubbelman

the

etal.

microcirculation.

ultraviolet-B-induced

Ophthalmol.

stretching

94.

Am

on

dysfunction

93.

EC.

specic

García-Domene

Eur

92.

in

Y egorov

Giblin

Invest

the

Res.

Muñoz

Antioxid

redox

Exp

description

91.

of

Glutathione

VN,

Exp

the

opacities

MA,

diseases.

Reddy

lens

MD,

sunlight-related

mitochondria-targeted

eye

89.

of

Eye

DD,

maintaining

potential

88.

Jacobs

of

role

Curr

oxidation-induced

of

BMC

1998;116:1666.

VM,

Babizhayev

in

connexins.

100.

e

lens

cataracts.

dria

model

Duncan

Berthoud

the

lens

99.

DTK,

family

cataract.

risk

and

on

1994;71(2):125.

Ophthalmol.

86.

Focus

2012;11:69.

RW .

Sci.

UV

A.

1).

Malcolm

Hightower

of

85.

E,

nite

Online.

83.

Ngezahayo

2017;18(Suppl

Vaghe

3D

V ,

WN.

tion

2009;88:140–143.

Res.

Charman

Eye

basic

Vis

Clin

van

cur vature,

opia.

in

1992;194:85–92.

M,

lens:

paradox.

Totowa,

96.

C oi nc i d ent

Dubbelman

human

2008:111–123.

D C.

95.

Ocular

thermal

2010;51(10):5145–5152.

binding

human

lenses:

stress.

Invest

of

a

α-cr ystallin

phenomenon

Ophthalmol

8

Retina

1

e

innermost

between

the

coat

of

choroid

the

and

eye

the

is

a

neural

vitreous.

It

layer,

the

includes

retina,

the

located

macula,

the

the

the

macular

layer

area.

nears

e

the

cells

ora

the

nerve

with

the

bers

embryological

derm

and

outer

layer

the

inner

tightly

is

origin.

of

the

layer

of

adherent

in

a

to

the

eye,

layers

consists

attached

only

exit

epithelial

of

to

the

of

an

cup,

the

and

is

throughout,

epithelium

it

at

ecto-

from

derived

the

thus

shares

neural

pigmented

and

where

continuous

derived

but

and

disc

is

retina,

e

disc,

which

from

layer,

9).

It

with

neural

the

optic

serrata.

derived

the

around

the

body,

(see Ch.

choroid

ring

ora

of

pigmented

cup

pigmented

peripapillary

edge

ciliary

retina

outer

optic

the

to

the

e

optic

the

circular

to

the

from

layer

neural

the

the

is

retina

is

is

serrata.

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site

of

transformation

of

light

energy

into

a

of

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of

parts

the

in

of

the

the

germ

and

to

the

in

which

its

as

pig-

retina

with

the

it

is

into

the

cells,

the

neu-

and

part

to

of

the

choroid,

from

the

ectoderm.

the

pigment

middle

nucleus,

density

individual

a

melanosomes,

obscure

the

forms

because

area

Pigment

faces

of

infoldings

attachment

association

apical

Because

surface

numerous

numerous

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region.

and

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layer—neural

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basal

retina

the

cell

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located.

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close

of

contain

extend

cell

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part

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membrane,

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cells

that

the

contains

basement

considered

RPE

located

the

strong.

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granules,

neural retina has the appearance of a thin, transparent membrane.

is

its

and

aspect

embr yological

tion

retina

is

RPE

same

to

choroid

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membrane

choroid

the

the

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adherent

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e

to

retina.

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cuboidal

orientation of the embr yological cells, the basal aspect of the cell

the

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epithelium

become

serrata,

diers

which

por-

which

in

can

is

various

give

the

neural signal. It contains the rst three cells (photoreceptor, bipolar,

fundus a mottled appearance when viewed with the ophthalmo-

and ganglion cells) in the visual pathway, the route by which visual

scope.

information

in

In

the

retina,

melanin

is

densest

in

the

RPE

cells

located

2

from

the

environment

reaches

the

brain

for

interpre-

the

macula

tation. Photoreceptor cells transform photons of light into a neural

lipofuscin

signal through the process of phototransduction. is signal is then

tosis,

transferred

also

and

at

granules,

the

equator.

contain

Other

degradation

products

1

cells,

to

which

Other

retinal

integrate

bipolar

transmit

the

cells,

cells,

the

which

signal

horizontal

signal

before

it

in

from

cells

turn

the

and

leaves

the

synapse

eye

to

amacrine

eye.

with

areas

is

in

cells,

ganglion

the

brain.

modify

chapter

which

increase

contains

apparatus,

and

e

discusses

extend

in

smooth

number

and

mitochondria,

apical

into

outer

portion

the

layer

rough

and

an

RPE

cell

reticulum,

Golgi

lysosomes.

consists

of

microvilli

enveloping

RETINAL

HISTOLOGICAL

light

microscopy,

the

epithelial

remnant

cell

of

and

the

the

gap

intercellular

that

special-

photoreceptor.

formed

between

is

the

junctions

subretinal

two

layers

of

FEATURES the

Under

a

No

the

connect the RPE and photoreceptor cells. A potential space sep-

the

8.2).

cytoplasm

ized

is

(Fig.

cell

the visual pathway is described in Chapter 15.

space

tips

e

endoplasmic

photoreceptors,

phagocy-

3–5

age.

numerous

of

bodies,

these cells and the detailed anatomy of the retina. e remainder of

arates

segment

of

of

with

pigmented

retina

has

a

laminar

appearance

in

optic

cup

Terminal

aer

bars

invagination

consisting

of

of

the

optic

zonula

vesicle

(see Ch. 9).

occludens

and

zonula

1

which 10 layers are evident (Fig. 8.1). Closer examination reveals

adherens

that these are not all layers, but rather a single layer of pigmented

present

epithelium

cells

and

three

layers

of

neuronal

cell

bodies,

between

join

the

RPE

throughout

allow

for

cells

the

near

layer,

electrical

their

and

apices.

gap

coupling,

Desmosomes

junctions

providing

a

between

are

the

low-resistance

6

which lie their processes and synapses. is section describes the

pigment

epithelial

layer

ral

e

section

cells.

the

10

retinal

tomography

will

next

view

layers.

retinal

the

types

discusses

ese

(OCT)

the

and

are

images

on

a

this

daily

functions

of

components

compared

because

anatomy

and

the

with

is

optical

how

the

of

for

the

passage

of

ions

and

metabolites.

neu-

each

of

coherence

many

pathway

clinicians

basis.

Photoreceptor

Photoreceptor

containing

cells

Cells

cells,

the

rods

photopigments

originally

were

named

and

that

for

cones,

absorb

their

are

special

photons

shapes,

but

sense

of

the

light.

name

cells

e

does

not always reect the shape, particularly in the cone population.

Retinal

e

retinal

layer,

cells.

and

Pigment

is

a

are

pigment

single

ese

Epithelium

cells

even

cell

are

longer,

epithelium

thick

and

More

(RPE),

consists

columnar

narrower,

in

the

and

of

the

pigmented

area

more

outermost

of

the

retinal

of

hexagonal

in

posterior

densely

pole

pigmented

in

important

illumination

dim

Visual

tion

by

in

in

the

illumination,

pigments

in

designation

which

and

the

each

cones

is

of

a

rod

active.

are

active

photoreceptors

or

Rods

in

are

cone

are

is

the

more

well-lit

level

active

conditions.

activated

on

excita-

light.

111

CHAPTER

112

8

Retina

10

9

8

7

m

6

m

5

4

3

2

1

A

Fig.

B

8.1

layers

the

Layers

(B

10

from

retinal

membrane;

layer;

cells

Retinal

Pigment

S everal

factors

8,

of

layers.

4,

outer

ganglion

(m)

and

the

Leeson

retina

CR,

1,

Retinal

nuclear

cell

A,

9,

choriocapillaris

S.

5,

(arrow)

ber

are

image.

B,

Philadelphia:

epithelial

outer

ner ve

histology

Histology.

pigment

layer;

layer;

Epithelium-Neuroretinal

Retinal

Leeson

layer;

2,

plexiform

layer;

internal

also

6,

inner

layer;

nuclear

limiting

drawing

1976.).

photoreceptor

layer;

10,

Represent ative

Saunders;

3,

layer;

7 ,

membrane.

inner

mation

between

Passive

forces,

involved

the

such

in

photoreceptor

as

intraocular

cell

10

uid

transport

across

the

layer

e

close

and

pressure,

7–9

sure,

the

approxi-

the

osmotic

to

limiting

plexiform

Fibers

of

Müller

indicated.

Interface

maintaining

retinal

refer

external

adhesive

mechanism

is

attributed

13

are

of

Numbers

RPE.

of

pres-

and

these

bonds

choroid.

is

not

e

as

great

interface

as

to

molecular

bonds

15–18

within this extracellular material.

Nonetheless, the strength

the

adhesion

between

the

RPE

between

and

the

the

RPE

photore-

11

RPE,

and

the

presence

of

ceptor

layer

is

the

common

location

of

separation

in

a

retinal

12

the

vitreous,

help

Interdigitations

cone

outer

preser ve

between

segments

the

the

provide

position

RPE

a

of

the

microvilli

physical

neural

and

closeness

the

retina.

rod

detachment.

and

between

the CLINICAL

two

entities.

e

When

interphotoreceptor

extracellular

space

matrix,

between

the

material

RPE

cells

that

and

occupies

the

photoreceptors,

RPE

a

cells

cells.

COMMENT: Neurosensory

retinal

and

The

detachment

the

RPE

occurs,

photoreceptors

cells

remain

the

because

attached

to

Retinal

separation

no

the

Detachment

usually

intercellular

choroid

and

lies

between

junctions

cannot

be

join

the

these

separated

13–15

provides

adhesive

forces.

is

honeycomb-like

structure

16

is

composed

of

proteins

and

glycosaminoglycans.

e

outer

from

it

large

without

adhesive

difculty.

Bruch

glycoproteins

membrane

with

many

contains

binding

bronectin

sites

that

help

and

laminin,

maintain

the

19

adherence

segments

of

the

photoreceptors

are

surrounded

completely

subretinal

the

interphotoreceptor

matrix,

and

the

photoreceptors

e

to

both

openings

in

its

RPE

and

the

cells

to

the

membrane.

Fluid

can

accumulate

within

the

space

choroid

(Fig.

separating

the

photoreceptors

from

the

nutrients

supplied

by

8.3).

meshwork.

interphotoreceptor

the

RPE

extend the

through

of

by

matrix

constituents

photoreceptor

cells

are

and

bound

may

tightly

exceed

the

e

interphotoreceptor

matrix

provides

a

means

for

the

20

strength

of

separation

the

RPE

between

cells.

these

In

laborator y

two

layers

experiments,

oen

ruptures

a

the

forceful

RPE

cell,

exchange of metabolites

and

photoreceptors.

In

and for interactions between the RPE

addition,

the

interphotoreceptor

matrix

17

leaving

remnants

of

pigment

attached

to

the

photoreceptors.

may

be

partly

responsible

for

orienting

the

photoreceptor

CHAPTER

Fig.

and

8.2

portions

the

Three-dimensional

cells

of

of

the

the

retinal

rod

outer

photoreceptors

bottom

contains

endoplasmic

tered

free

of

reticulum

the

(j). The

rod

(g);

the

relationship

(b).

(RPE). Thick

Numerous

pigment

granules

pigment

granules

a

developed,

Stacks

poorly

of

periphery

cilium

of

epithelium

segments

contain

numerous

ribosomes.

cross-section

body

and

drawing

pigment

extend

rod

of

outer

the

nger -like

(d). The

(f);

the

discs

are

of

outer

RPE

processes

of

the

endoplasmic

(k).

(c)

are

RPE

in

a

one

such

the

found

layer

of

113

Retina

of

rods

external

between

cells

at

the

smooth-surfaced

reticulum

meridional

Microtubules

segment;

segments

enclose

well-developed,

depicted

scalloping

outer

a

the

(a)

portion

rough-surfaced

shows

into

villous

apical

mitochondria

segment

discs

externally

(e);

between

sheaths

8

(h);

and

section

originating

microtubule

in

is

(i)

scat-

and

the

in

basal

shown

in

cross section (l). (From Hogan MJ, Alvarado JA, Weddell JE. Histology of the Human Eye. Philadelphia:

Saunders;

1971 .)

14

outer

the

segments

for

optimal

interphotoreceptor

light

matrix

capture.

that

e

surrounds

constituents

rods

dier

of

from

signal;

ment,

(2)

a

connec ting

cont aining

t he

st a lk,

t he

met ab olic

ci lium;

apparatus;

(3)

(4)

t he

t he

inner

outer

s eg-

b er ;

16,21,22

those

around

cones.

ese

areas

are

believed

to

be

bound

(5)

t he

cell

b o dy ;

and

(6)

t he

inner

b er,

w hich

ends

in

a

syn-

16

together

laterally,

forming

a

highly

coherent

structural

unit.

aptic

ter minal

Outer

Composition

Ro ds

est

and

t he

Rods

cones

RPE:

pigment

of

are

(1)

outer

for

t he

of

8.4).

Segment. e

outer

s eg ment

is

made

up

of

a

st ack

of

2

Cones

comp os ed

t he

molec ules

and

(Fig.

membranous

s e veral

s egment,

conversion

par ts,

st ar t ing

cont aining

of

lig ht

t he

into

a

ne ar-

visual

neural

dis cs

plasmalemma

s ac

top

wit h

of

a

one

of

(600–1000

t he

nar row

anot her

cell.

E ach

intradis c

and

p er

are

ro d)

dis c

space.

is

and

a

e

s eparate d

is

enclos ed

attened

dis cs

by

an

are

by

t he

membrane

st acke d

ext radis c

on

space.

CHAPTER

114

8

Retina

Visual

pigment

brane.

A

ec ules

t he

w hen

outer

apical

inner

pro cess es

A

as

a

Retinal

tear

and

detachment.

Neural

retinal

tissue

central

cilium

from

the

underlying

retinal

pigment

epithelium

RPE.

wit hin

initiated

by

a

photon

toward,

e

bas e

of

and

is

t he

dis c

wit hin

mem-

t hes e

lig ht.

envelop ed

or iented

mol-

e

t ip

of

by,

t he

toward

t he

pair,

of

a

around

and

with

or

outer

that

outer

of

the

inner

them

nine

present

the

e

of

cilium,

segment

between

series

usually

Segment.

stalk,

the

(Fig.

pairs

in

extends

with

from

inner

It

is

tubules

cilia,

segment

inner

8.5).

of

motile

the

is

is

a

the

in-

segment

modied

from

which

missing.

continuous

e

across

segment.

segment

contains

cellular

struc-

is

tures

separated

t he

conduit

consisting

Inner

8.3

or iented

joining

plasmalemma

Fig.

is

of

lo cated

is

ac tivate d

connecting

disc,

acting

cilium

the

are

s egment

Cilium.

the

t he y

are

change

s egment.

nermost

and

molec ules

bio chemical

and

can

be

divided

into

two

parts.

e

ellipsoid

zone

is

and

nearer

the

outer

segment

and

contains

numerous

mitochondria

choroid.

necessar y

cesses.

Spherule

Pedicle

called

the

for

e

the

the

part

myoid

from

is

a

the

and

endoplasmic

thesis

many

of

reticulum

area

segment

contains

concentrated

similar

energ y-dependent

inner

in

in

other

and

this

to

cellular

Golgi

area.

photoreceptor

closer

term

that

cell

such

Protein

myoid,

contains

pro-

body

organelles,

apparatus.

e

amphibians

the

a

is

is

as

syn-

derived

contractile

Outer

plexiform

Inner

structure

that

segments

of

produces

orientational

movements

of

the

outer

layer 23

fiber

the

cones.

e

human

myoid

does

not

have

con-

24

tractile

Müller

properties,

segments

is

although

oriented

toward

the

the

axis

exit

of

the

pupil

of

inner

the

and

eye,

outer

maximiz-

cell

ing

the

ability

of

the

photoreceptor

to

capture

light.

e

radial

Cell

body

Outer

orientation

becomes

more

evident

in

cells

located

farther

from

nuclear 25–27

the

layer

macula.

Outer

Outer

External

Fiber,

Cell

Body,

and

Inner

Fiber.

e

outer

b er

ex-

fiber

limiting

tends

f rom

t he

inner

s eg ment

to

t he

cel l

b o dy,

t he

p or tion

membrane

Myoid

cont aining

t he

cont aining

microtubules

nucleus.

e

inner

b er

is

an

axonal

pro cess

Inner

segment

Ellipsoid

ending

in

sp ecialize d

and

r uns

synaptic

inward

ter minals

f rom

t hat

t he

cell

cont ain

b o dy,

synapt ic

Cilium

Cilium Photoreceptor

layer

Outer

segment

Basal

body

A

Rod

Cone

Mitochondria

Nucleus

of

rod

Nucleus

of

cone

Exter nal

Modified limiting

cilium membrane

Cone

Rod

Pigment

epithelium

Membranous

B

discs

of

outer

Fig.

8.4

Photoreceptor

cells.

A,

Drawing

of

a

rod

and

cone. segment

Portions

rods

the

of

and

layers

B,Retinal

Müller

cones.

in

cells

The

which

(dotted

retinal

the

parts

photoreceptors.

Concise T ext

of

Histology.

lines)

layers

of

the

(×1000.)

are

listed

shown

to

the

adjoining

right

photoreceptor

(B

from

are

Krause WJ,

Baltimore: Williams

the

indicate

Fig.

located.

(T ransmission

Cutts

& Wilkins;

JH.

1981 .)

8.5

Cutts

Junction

JH.

1981 .)

of

the

electron

Concise T ext

outer

and

microscope;

of

Histology.

inner

segments

×45,000.)

(From

of

the

Krause

Baltimore: Williams

rod.

WJ,

& Wilkins;

CHAPTER

vesicles.

lar

and

Rod

e

and

Cone

Rods.

is

e

separate

the

base

the

space

(see

rounding

uniform

located

Fig.

8.4A).

both

a

ment,

where

in

the

to

the

wit h

of

and

the

of

free

with

the

of

a

small

the

bip o-

discs.

the

discs

e

at

the

are

a

than

that

RPE

One

the

that

by

trum.

rhodopsin

is

the

amino

acids

moved

into

the

into

from

newly

discs

nally

of

in

the

the

discs

disc

from

seg-

discs

the

phagosomes

base

of

the

to

three

to

(green),

cones

Electron

discs

nections

ecules

the

able

membrane

each

in

peak

588

a

specic

to

nm

short

rather

than

the

at

the

cone

outer

the

tip,

outer

segment

RPE

apical

layer.

surface

of

segment.

is

contained

molecule

range

in

L-cones

occur

is

the

at

within

activated

color

spec-

M-cones

are

respectively.

green

420

At

are

sensitive

nm

to

(blue),

least

90%

of

cones.

suggest

but

that

because

formation

of

the

plasmalemma,

throughout

being

cone

wavelengths,

and

(red),

or

base,

diuse

from

outer

those

some

reach

molecules

studies

the

e

not

pigment

surrounding

to

rod.

absorptions

red

microscope

with

are

pigment

either

at

cone

than

although

may

wavelengths,

e

occurs

the

light

and

are

a

and

115

Retina

wider

protrude

sensitive

medium

to

rod

and

of

are

are

shape,

similar

the

visual

membrane,

wavelengths.

cone

of

base

cone

processes

absorption

nm

the

surround

S-cones

human

com-

inner

assembled

moved

seen

rod

of

sensitive

long

at

shape

tubular

cell

disc

531

labeled

was

have

shorter

sur-

fairly

discs

is

discs.

sacs

to

the

characteristic

segments

the

form

discs

the

region

form

pigment

formation

synthesized,

e

label

cones,

However,

membrane.

is

many

segment,

extracellular

attachment

photosensitive

radioactivity

segment.

for

outer

plasmalemma

adjacent

radiolabeled

protein

outer

tip,

of

band

the

are

rod

except

remainder

the

disc

of

investigating

pulse

e

synaps e

the

continuous

and

and

and

the

is

e

ends

width,

within

membrane

space

membrane

in

ponents.

disc

enclosing

invaginations

Researchers

applied

the

intradisc

at

endings

giving

plasmalemma,

from

closed

ner ve

cells.

Morphology

where

Here,

are

photoreceptor

hor izont al

8

the

conned

to

the

cone

discs,

of

new

extensive

labeled

outer

as

con-

mol-

segment

occurs

in

the

of

the

35

RPE

cells.

is

study

established

that

the

components

of

disc

rods.

Cone

discs

are

shed

periodically,

oen

at

the

end

35–37

membranes

the

are

produced

connecting

segment

base.

formation

of

stalk

e

new

to

in

be

discs

discs

the

inner

segment

incorporated

gradually

and,

as

are

they

into

and

discs

displaced

reach

the

at

taken

cess,

the

up

rod

by

the

outer

RPE

cells,

segment

and

the

outward

tip,

are

28

o,

move

system,

by

discs

processes

are

shed

in

both

the

regularly,

RPE

with

and

appears

most

the

outer

the

shedding

of

late

the

sloughed

is

to

pro-

involve

30

active

outer

day, and are phagocytosed by the RPE.

the

cycle

of

disc

shedding

are

e factors that regu-

still

under

investigation.

e shape of the inner segment contributes to the cone shape.

e

ellipsoid

area

of

the

cone

is

wider

and

contains

more

mito-

29

phagocytosed.

renewal

along

chondria

than

may

be

even

the

rod.

absent

in

e

the

outer

cone;

ber

thus

is

cone

short

and

nuclei

lie

stout

outer

and

to

rod

31

segment.

e

occurring

in

nuclei.

called

e

a

inner

pedicle,

ber

terminates

which

has

in

several

a

broad,

attened

invaginated

areas

structure

within

its

32–34

the

early

e

same

morning.

rod

relatively

from

inner

width.

e

long

the

cell

attened

and

inner

and

body

outer

segments

segment

narrow

and

is

outer

are

joined

ber.

terminates

in

to

e

a

approximately

the

cell

inner

body

ber

rounded,

by

surface

(see

Fig.

8.4A).

Cone

pedicles

have

of

the

called

spherule

contains

release

a

is

bipolar

the

spherule

(see

invaginated

dendrites

8.4A).

forming

and

neurotransmitter

Fig.

a

e

of synaptic contacts. Triads involving ON bipolar cells are found

the

within

the

on

at

extends

pear-shaped

internal

synaptic

horizontal

cell

surface

complex

processes.

types

the

the

invaginations,

surfaces,

expansions

and

contacts

gap

(telodendria)

with

junctions

of

the

OFF

are

pedicle

bipolar

located

communication

that

Rods

As

with

between

rods,

the

adjacent

rods

and

or

neurotransmitter

cells

on

the

permit

25

structure

three

occur

lateral

electrical

38

cones.

released

by

cones

is

glutamate.

glutamate.

Cones. As in the rod, the outer segment of the cone is enclosed

by a plasmalemma, but in this case the plasma membrane is con-

tinuous

with

the

membranes

forming

most

of

the

discs,

and

the

Bipolar

e

Cells

bipolar

cell

is

the

second-order

neuron

in

the

visual

path-

35

discs

are

not

separated

easily

from

one

another

(Fig.

8.6).

In

way. e nucleus of the bipolar cell is large and contains minimal

cell

and

body

amacrine

relay

and

Membranous

cytoplasm.

horizontal

cells.

amacrine

dendrite

and

its

Glutamate

information

ganglion

Its

cells,

cells

cells.

from

and

More

is

synapses

axon

its

than

to

extensive

10

photoreceptor

with

ganglion

neurotransmitter.

photoreceptors

receive

with

synapses

types

of

Bipolar

horizontal,

synaptic

bipolar

amacrine,

feedback

cells

and

cells

have

from

been

discs

classied

on

the

basis

of

morpholog y,

physiolog y,

and

dendritic

39–41

contacts

lar

cell

are

Only

a

photoreceptors.

associated

one

relatively

type

large

arising

from

appear

1

e Fig. 8.6

with

a

mm

expanse

of

with

rod

cell

of

the

bipolar

body

single,

from

and

thick

the

All

types

except

the

rod

bipo-

cones.

cell

process.

fovea

dendritic

has

several

and

tree

been

spiky

Rod

identied.

dendrites,

bipolar

continue

widens

into

and

cells

the

the

It

has

usually

begin

to

peripher y.

reach

of

the

Cone outer segment. (T ransmission electron microscope;

×56,000.)

(From

Krause WJ,

Baltimore: Williams

Cutts

& Wilkins;

JH.

1981 .)

Concise T ext

of

Histology.

axonal

the

terminals

peripheral

increases

retina

in

the

compared

rod

with

bipolar

those

in

cells

the

located

central

in

retina.

CHAPTER

116

Rod

bipolar

c.

8

Retina

Midget

bipolar

c.

Flat

bipolar

have up to three such dendritic expansions, with the capacity to

c.

41

contact

bipolar

several

cell

pedicles.

synapses

e

with

axon

the

of

the

dendrite

of

invaginating

a

single

midget

midget

gan-

1

glion Horizontal

cell

and

with

amacrine

processes.

c.

e

type

two

a

types

and

type

of

b,

diuse

called

cone

at

bipolar

bipolars

cells

and

are

designated

brush

bipolars

by

45

Polyak.

tacts

er y,

In

the

central

approximately

each

contacts

retina,

ve

10

the

diuse

neighboring

to

15

cone

cones,

neighboring

bipolar

and

cones.

in

cell

the

e

con-

periph-

location

of

41

the

axon

e

terminal

blue

dierentiates

cone

bipolar

cell

the

two

types.

synapses

with

up

to

three

cone

41

pedicles.

It diers from diuse cone bipolar cells in that it con-

41

tacts

widely

e

of

trees,

Rods

Cones

(spherules)

(pedicles)

Fig.

8.7

Rod

Rod

and

cone

spherule

and

cone

pedicle

its

spaced

giant

cone

tree.

and

clusters

then

cells

also

nections

(From

make

are

show

synapses

shown

Hogan

cells

MJ,

with

between

Alvarado

both

rod

their

synapses.

contacts.

Horizont al

JA,

rods

and

spherules

Weddell

diuse

Eye.

Philadelphia:

Saunders;

cell

derives

major

of

its

name

dendrite

processes

cones.

from

branches

branch

from

the

extent

into

three

these,

each

and

bistratied,

cones.

and

JE.

dier

only

in

the

location

of

their

axon

46

terminations.

Intercon-

cone

pedicles.

Histology

of

Ganglion

Cells

the

e Human

e

neighboring

group being the size of a cone pedicle. e two types, designated

and

extensive

than

bipolar

dendritic

41

bipolar

rather

next

cell

in

the

visual

pathway,

the

third-order

neuron,

is

1971 .)

the

ganglion

axon

and

a

cell.

Ganglion

single

cells

dendrite)

or

can

be

bipolar

multipolar

(a

(e.g.,

single

a

single

axon

and

47

more

than

one

dendrite).

Cell

size

varies

greatly,

with

some

41

e

in

dendrites

central

of

retina

a

single

and

up

rod

to

bipolar

80

rods

41

spherule

invagination

in

contact

the

15

to

peripher y,

20

rods

large

improving

cell

bodies

Various

measuring

methods

are

28

used

to

to

36

μm.

classif y

ganglion

cells,

includ-

42

sensitivity to light and motion.

a

cell

Oen two dendrites lie within

anked

by

two

horizontal

cell

processes

ing

classication

acteristics,

on

the

basis

termination

of

of

cell

body

dendrites

or

size,

branching

axons,

and

the

char-

expanse

41

(Fig. 8.7). e rod bipolar axon is large and unbranched. It rarely

of

synapses

with

ganglion

syn-

which

directly

with

ganglion

cells

but

instead

synapses

the

dendritic

cells

tree.

based

One

on

the

common

lateral

designation

geniculate

classies

nucleus

layer

in

43

amacrine

aptic

processes,

arrangement

which

allows

then

a

signal

ganglion

ganglion

cell

to

cells.

carr y

is

information

layers

they

of

terminate.

the

lateral

P

cells

terminate

geniculate

nucleus.

in

e

the

P1

par vocellular

ganglion

cell,

43

from

both

e

the

rod

midget

synapse

on

and

the

bipolar

either

the

cone

cell

at

has

or

pathways.

a

also called the midget ganglion cell, is the most common P cell.

relatively

invaginating

small

body

portion

of

and

the

can

pho-

is

relatively

ferentiated

small

into

two

cell

has

types

a

single

according

dendrite

to

the

and

can

be

stratication

dif-

of

the

41

toreceptor.

end

in

a

Dendritic

at

terminals

expansion

and

of

the

make

at

midget

contact

only

bip olar

with

cel l

the

at

dendritic

to

only

branching.

one

midget

C ertain

bipolar

P1

cell,

midget

cells

invaginating

are

or

connected

at,

which

in

48

area

of

each

at

dritic

the

or

the

cone

midget

bouquet

bipolar

is

peripheral

three

pedicle

(see

cell

dendritic

each

clusters

41

three

neighboring

8.7).

contacts

small—the

retina,

Fig.

size

at

and

In

only

of

a

one

single

midget

thus

the

central

cone

cone

bipolar

each

cell

so

retina,

its

den-

pedicle.

cell

has

contacts

In

two

two

or

turn

might

channel

tion.

that

is

pathway

bipolar

be

linked

to

processes

situation

occurs

is

in

a

single

cone

high-contrast

likely

some

to

P1

occur

cells

receptor,

detail

in

that

the

providing

and

fovea.

receive

color

A

a

resolu-

convergent

input

from

two

axons.

44

cones.

A

single

cone

pedicle

may

have

e P2 ganglion cell also terminates in the par vocellular lay-

2

as

many

at

as

midget

500

contacts

bipolar

cell

on

has

its

at

many

surface.

endings

e

and

axon

of

synapses

the

with

ers

of

the

lateral

branched,

geniculate

compact

nucleus,

dendritic

tree

but

that

these

have

spreads

a

densely

horizontally.

1

ganglion

cells

of

all

types.

ese

cells

can

be

dierentiated

into

two

types

depending

on

41

e

invaginating

midget

within

a

bipolar

the

triad.

A

anked

by

cell,

pedicle

triad

two

midget

but

bipolar

its

dendritic

invaginations,

consists

horizontal

of

cell

a

cell

similar

processes

usually

single

is

in

are

the

bipolar

within

an

at

the

located

groupings

central

processes

to

called

dendrite

invagination

location

e

layers

of

the

M-type

of

the

dendrites

dendrite

ganglion

lateral

(because

termination.

cell

projects

geniculate

nucleus.

of

its

shape

it

can

to

the

e

also

M

be

magnocellular

cell

has

called

a

coarse

parasol

ganglion cell) with spiny features, and the dendritic tree enlarges

41

in

the

dritic

of

a

lar

cone

pedicle

bouquet

single

cell

is

of

cone

(see

an

Fig.

8.7).

In

invaginating

pedicle,

inner vated

by

implying

only

one

the

central

midget

that

bipolar

each

cone.

retina,

cell

the

is

the

invaginating

Each

pedicle

den-

size

bipo-

can

from

to

25

triads.

to

of

the

lateral

have

large

receptive

may

color

signals.

49

In

the

peripheral

retina,

each

bipolar

cell

peripheral

Koniocellular

ers

2

12

central

ganglion

cells

genicular

elds

50

retina.

and

project

nucleus.

carr y

to

the

ese

koniocellular

ganglion

information

about

cells

lay-

have

blue-yellow

CHAPTER

Intrinsically

photosensitive

retinal

ganglion

cells

can

tors.

be

(also

called

depolarized

ey

perform

opsin

by

light

4)

on

the

without

nonimage

cell

surface.

input

forming

from

tasks,

such

ese

COMMENT: Sleep

melatonin

and

synthesis,

sleep/wake

response.

In

cycle,

contributing

and

addition,

to

the

modulation

they

may

play

a

of

Ganglion

Cell

role

Glaucoma

is

characterized

rhythm

extreme

light

sensi-

sitive

visual

ganglion

eld

by

the

cells

are

defects

loss

of

ganglion

also

because

lost

and

in

of

that

cells,

severe

53

suppression

cells

that

of

are

melatonin

displaced

and

and

sleep

located

loss.

to

light

responses

(the

retinal

from

rods

suprachiasmatic

tectal

nucleus),

as

e

ganglion

and

well

the

signal

cells,

cones,

nucleus)

patients

exhibit

glaucoma

in

the

this

photosen-

may

Photosensitive

result

in

inner

nuclear

layer

may

ganglion

be

spared

53

(photophobia).

photosensitive

and

Intrinsically

55–57

disorders.

51

tivity

With

regulation

pupillar y

in

Associated

Loss

photorecep-

as

circadian

the

Disruption

cells

characteristic

of

117

Retina

contain CLINICAL

melanopsin

8

which

projects

and

lateral

from

is

to

combined

the

midbrain

and

olivar y

nucleus

this

could

reduce

the

effect

of

the

disease

on

sleep.

with

hypothalamus

(the

geniculate

intrinsically

pre-

allowing

Each

cell

ganglion

body

and

cell

turns

has

to

a

run

single

axon,

parallel

to

which

the

inner

emerges

surface

from

of

the

the

ret-

ina (Fig. 8.8). e axons come together at the optic disc and leave

52

integration

ere

glion

are

with

vision.

several

cells.

e

Peak

subtypes

majority

of

sensitivity

of

is

intrinsically

intrinsically

around

480

nm.

photosensitive

photosensitive

the eye as the optic nerve. e termination for approximately 90%

gan-

of

these

ganglion

to

subthalamic

axons

is

the

areas

lateral

geniculate

involved

in

nucleus.

processes

such

e

as

rest

the

project

pupillary

2

cells

are

found

in

the

ganglion

cell

layer,

but

about

45%

can

be

reexes,

the

circadian

rhythm,

and

reexive

eye

41

movements.

53

displaced

ganglion

to

the

cells

inner

only

nuclear

about

layer.

7520

Of

the

1.0

(0.3%–0.75%),

to

are

1.5

million

considered

e

ganglion

cell

axon

releases

glutamate

at

its

synaptic

cle.

e photoreceptor cells, bipolar cells, and ganglion cells carr y

52–54

intrinsically

mainly

photosensitive

located

in

the

retinal

parafoveal

ganglion

region

and

cells.

nasal

ey

are

hemiretina.

the neural signal in a three-step pathway through the retina. e

neural

signal

is

modied

within

the

retina

Internal

limiting

Nerve

membrane

fiber

layer

Ganglion

Ganglion

cell

cell

layer

Inner

plexiform

layer

Amacrine

cell

Horizontal

cell

Inner

nuclear

layer

Bipolar

cell

Outer

plexiform

layer

Outer

nuclear

layer

External

limiting

membrane Rod

Photoreceptor

layer Cone

Retinal

pigment

epithelium

Fig.

8.8

Retinal

cells

and

synapses. The

10

retinal

layers

are

indicated.

by

other

cells

that

CHAPTER

118

8

Retina

62,63

create

intraretinal

mation,

or

cross-connections,

integrate

retinal

provide

feedback

infor-

function.

allows

may

integration

receive

between

input

from

the

as

two

many

pathways.

as

300

rods

An

AII

through

cell

80

rod

26

bipolar

Horizontal

e

Cells

horiz ontal

direc tion,

one

long

and

cel l

parallel

pro cess,

transfers

to

t he

or

axon,

infor mation

retinal

sur face

and

in

(s ee

s e veral

a

hor izont al

Fig.

shor t

8.8).

It

dendr ites

has

wit h

cells.

may

cone

e

also

pathway.

munication

they

have

AII

relay

AII

with

cell

then

synapses

information

amacrine

other

one-way

AII

from

cells

cells

synapses

also

and

with

with

the

rod

have

ON

ganglion

bipolar

bipolar

the

com-

cells,

cells

cell

to

bidirectional

cone

OFF

a

pathway

and

and

OFF

61

branching

ter minals.

t he

sur face,

retinal

layer.

Hor izont al

e

and

cells

pro cess es

all

spre ad

ter minate

synaps e

wit h

in

out

t he

p arallel

outer

to

ganglion

plexifor m

photore ceptors,

bip olar

cells.

Wide-eld

with

rod

amacrine

bipolar

cells

(A17)

and

cells

appear

form

to

reciprocal

modify

the

synapses

signal

trans-

41

cells,

to

and

e ach

typ e

of

ot her

ot her

hor izont al

by

an

hor izont al

cells.

extensive

cell

Hor izont al

network

synaps es

on ly

of

cells

gap

wit hin

are

joined

junc t ions.

a

cone

One

p edicle

in

mitted

from

contain

acid

the

rod

bipolar

inhibitor y

(GABA)

or

to

AII

cells.

Most

neurotransmitter

glycine

and

have

amacrine

cells

gamma-aminobutyric

both

presynaptic

and

post-

2,62

t he

sp ecial

tr iad

junc tion.

Hor izont a l

cel ls

can

cont ac t

bip olar

synaptic

endings.

Amacrine

cells

are

joined

to

one

another

62

cells

lying

vated

t he

s ome

dist ance

hor izont al

cell.

f rom

t he

photoreceptor

Hor izont al

cells

caus e

an

t hat

ac t i-

in hibitor y

via

gap

junctions,

information

and

from

rod

some

and

cells

cone

have

been

pathways

found

before

to

combine

inner vating

a

48

resp ons e,

t hus

playing

a

role

in

t he

complex

pro cess

of

visual

ganglion

cell.

46 ,58

integration.

ree

HII,

and

cones

in

a

as

types

HIII.

of

horizontal

HI

lateral

cells

have

elements

fan-shaped

in

expanse

cells

triads

of

have

dendrites

and

been

that

a

terminals

dierentiated:

synapse

large,

that

with

thick

end

in

7

axon

rod

HI,

to

18

ending

spherules

Neuroglial

Cells

Neuroglial cells, although not actively involved in the transfer of

neural

the

signals,

neural

provide

tissue

structure

reaction

to

and

injur y

support

or

and

infection.

have

a

Types

role

of

in

neu-

59

more

than

axons)

1

mm

away.

apparently

All

contact

of

the HII

cones

and

processes

might

be

(dendrites

specic

and

for

blue

synapses

with

roglial

cells,

cells

and

found

in

the

retina

include

Müller

cells,

microglial

astrocytes.

41

cones.

many

er y)

HIII

cones

not

these

cells

have

(9–12

all

of

in

which

horizontal

a

the

cells

large

dendritic

macular

are

area

neighboring;

avoid

blue

tree

and

cones,

that

20–25

in

evidence

thus

the

periph-

suggests

being

that

selective

Müller

Cells

Müller

cells

are

and

neuroglial

cells

that

extend

throughout

much of the retina. ere are 10 million Müller cells in the mam-

yet

malian retina.

41,60

red

large

for

64

green.

e

termination

of

the

HIII

axon

has

not

ey play a supportive role, providing structure.

58

been

determined

Horizontal

cells

but

probably

provide

contacts

inhibitor y

both

rods

feedback

to

and

cones.

photoreceptors

Besides

lating

providing

the

structure,

concentration

of

Müller

cells

potassium

act

as

ions;

a

buer

they

help

by

regu-

maintain

65

or

inhibitor y

modulate

feed

the

for ward

cone

to

bipolar

response

but

cells.

are

not

Horizontal

thought

to

cells

can

inuence

the

extracellular

they

recycle

pH

by

GABA

absorbing

and

metabolic

glutamate,

waste

removing

products;

them

from

the

synthesize,

and

43,59

that

of

the

rod.

extracellular

space;

and

Müller

cells

metabolize,

66–68

store

Amacrine

Cells

glycogen.

innate

Müller

immunity

cells

through

may

Toll-like

also

play

receptors,

a

role

in

retinal

phagocytic

abili-

controversial,

there

69

e

amacrine

and

a

into

t he

sing le

cel l

has

pro cess

a

large

wit h

cell

b o dy,

extensive

a

lobulate d

branches

nucleus,

t hat

extend

ties,

is

and

some

secretion

evidence

of

cytokines.

that

Müller

Although

cells

aid

in

guiding

light

through

70,71

inner

dendr itic

and

hor izont ally,

cells,

axona l

for ms

dendr ites,

amacr ine

broad

t ant

plexifor m

in

of

its

e

pro cess,

charac ter istics

and

complex

synaps es

t he

of

pro cess es

spre ad

role

and

layer.

s oma

(s ee

Fig.

pro cess,

mo dulating

t he

t he

car r ies

wit h

gang lion

8.8).

cells,

amacr ine

cell

t hat

of

and

of

has

b ot h

the

infor mat ion

axons

B ecaus e

infor mation

w hich

bip olar

wit h

t he

plays

ot her

inner

e

apex

whereas

the

processes

extremely

ll

an

elements

re aches

imp or-

t he

gan-

retinal

in

the

basal

form

most

within

of

of

(Fig.

the

layers

a

toward

Müller

aspect

is

cell

at

reticulum

the

space

8.9).

synaptic

of

the

Müller

is

the

in

photoreceptor

retinal

the

retina

cells

the

inner

among

the

layers,

photoreceptors.

retinal

not

cell

occupied

ensheathe

giving

surface.

bodies

by

dendritic

structural

layer,

Cellular

and

neuronal

processes

support,

and

their

72

g lion

cell.

As

processes

many

as

30

to

40

dierent

amacrine

cell

types

may

be

and

their

envelop

most

processes

ganglion

appear

to

axons.

reside

in

Neuronal

tunnels

cell

within

the

bodies

Müller

42

described

four

as

stratied

groups—narrow

or

diuse.

eld,

ey

small

can

eld,

also

be

medium

classied

eld,

and

into

large

cell.

Delicate

between

the

apical

inner

villi,

ber

segments

of

baskets

the

(of

Schultze),

photoreceptors

at

terminate

the

myoid

1,23

eld—according

branching

into

to

the

processes.

dierent

types

extent

Each

of

according

of

coverage

these

to

the

by

groups

level

of

their

can

the

be

intertwined

subdivided

retinal

layer

in

zone.

On

passing

glion

light

through

cells,

microscopy,

the

layer

Müller

containing

perpendicular

to

the

cell

the

processes

ner ve

retinal

can

bers

surface.

of

An

be

seen

the

gan-

expanded

41,61,62

which

their

ner ve

endings

terminate.

process,

One of the most common and widely studied amacrine types

cell

called

the

contributes

to

endfoot,

the

along

membrane

the

basal

aspect

separating

the

of

the

retina

Müller

from

the

63

is

the

e

AII

AII

ganglion

cell

cells

(i.e.,

are

cells,

Roman

the

but

numeral

conduit

they

do

by

play

2),

which

a

role

a

narrow-eld

the

in

rod

cone

signal

type.

reaches

circuitr y

which

vitreous,

sels.

e

and

extensions

per vasiveness

extracellular

space

in

of

of

the

Müller

the

retina

cells

Müller

wrap

cell

(see Fig.

around

results

8.9).

in

blood

ver y

ves-

little

CHAPTER

Inter nal

limitimg

8

119

Retina

membrane

Inter nal

Ner ve

fiber

layer

limiting

Ner ve

membrane

fiber

layer

Ganglion

cell

layer

Ganglion

cell

layer

IPL

INL Inter nal

plexifor m

layer

OPL

ONL

Exter nal Inter nal

nuclear

limiting

layer

membrane

Photoreceptor

layer

Retinal

pigment

epithelium

Exter nal

plexifor m

layer

Fig.

8.10

INL,

nuclear a–Radial

nuclear

7.

Inner

8.

Ganglion

MJ,

Alvarado

adelphia:

the

JA, Weddell

Saunders;

Müller

JE.

plexiform

layer;

ONL,

outer

layer.

plexiform

9.

Ner ve

cell

layer

layer

baskets

limiting

cell

(dark

Histology

of

gray).

the

(From

Human

ber

layer

membrane

Internal

Retinal

of

inner

plexiform

layer

10.

Structure

IPL,

outer

fibers

Exter nal

8.9

layer;

OPL,

meshwork

Exter nal

c–Horizontal

Fig.

nuclear

layer;

processes

b–Honeycomb

d–Fiber

Light micrograph of a full-thickness view of the retina.

Inner

Hogan

Eye.

Phil-

e

Pigment

RPE

ously

limiting

consists

discussed.

membrane

Epithelium

of

a

ere

single

are

4

layer

to

6

of

pigmented

million

1971 .)

RPE

32

interacts

with

30

to

40

73

cells,

cells,

as

and

previ-

each

cell

74

photoreceptors.

ere

is

little

cell

division in the layer. e RPE is an active area with several func-

Microglial

Cells

Microglial

cells

be

found

response

and

are

anywhere

to

tissue

Astrocytes

wandering

in

the

tions

phagocytic

retina.

inammation

or

eir

cells

number

and

increases

in

injur y.

axon

perivascular

bundles

cells

form

and

an

between

irregular

retinal

blood

supportive

vessels.

network

will

be

described

Photoreceptor

e

Astrocytes are star-shaped brous cells found along bipolar and

ganglion

that

in

a

later

section.

might

that

ese

Layer

photoreceptor

rods

and

cones.

layer contains

Projections

from

the

the

outer

and

apical

inner

surface

of

segments

Müller

of

cells

extend into the photoreceptor layer and separate the inner segments.

encir-

cles nerve bers and retinal capillaries. As they surround the retinal

External

Limiting

Membrane

69

blood vessels, they become part of the blood retinal barrier.

e

external

limiting

membrane

(ELM,

outer

limiting

mem-

brane) is not a true membrane but is actually composed of zonula

adherens

TEN

RETINAL

junctions

between

photoreceptor

cells

and

between

LAYERS photoreceptors and Müller cells at the level of the inner segments.

e

10-layered

arrangement

able

organization

just

described

names

were

of

and

given

of

alternate

their

to

the

retina

groupings

processes.

these

so-called

is

of

actually

the

a

remark-

On

retinal

neurons

of

Traditionally,

layers,

and

descriptive

these

designa-

light

microscopy,

dashes,

cesses

has

of

the

the

resembling

the

rods

potential

and

to

act

a

so-called

cones

as

a

pass.

are

still

in

use

1.

Retinal

2.

Photoreceptor

3.

External

4.

Outer

5.

Outer

6.

Inner

today

pigment

layer

membrane

layer

plexiform

nuclear

8.10).

sage

of

some

large

appears

through

band

barrier,

of

as

a

series

which

zonula

pro-

adherens

restricting

the

pas-

75

molecules.

epithelium

cell

limiting

nuclear

(Fig.

sheet

is

metabolic

25

tions

membrane

fenestrated

layer

layer

Outer

e

Nuclear

outer

bodies.

of

the

cone

Layer

nuclear

e

rod.

cone

Cone

nuclei

lie

layer

cell

outer

in

a

(ONL)

body

bers

single

contains

the

rod

nucleus

are

larger

and

are

layer

ver y

close

short,

to

the

and

and

cone

than

therefore

external

cell

those

the

limiting

CHAPTER

120

membrane.

Cell

bodies

8

of

Retina

the

rods

are

arranged

in

several

rows

inner

plexiform

layer,

and

the

axon

of

the

at

midget

bipolar

cell

41,44

inner

nine

to

the

cells

thick

at

cone

thick

the

cell

on

bodies.

the

nasal

temporal

e

edge

edge.

It

outer

of

is

the

nuclear

optic

thickest

in

layer

disc

the

is

and

eight

four

fovea,

to

rows

where

it

ends

in

also

(2)

the

occur

outer

half

between:

amacrine

of

(1)

processes

the

inner

plexiform

amacrine

and

processes

ganglion

cell

layer.

and

Synapses

bipolar

bodies

and

axons,

dendrites,

2

contains

approximately

10

layers

of

cone

nuclei.

(3) amacrine cells and other amacrine cells (see Fig. 8.8). e pro-

cessing

Outer

e

Plexiform

outer

plexiform

layer

of

motion

detection

and

changes

in

brightness,

as

well

as

78

Layer

recognition

(OPL;

also

outer

synaptic

layer)

has

a

Ribbon

wide external band composed of inner bers of rods and cones and

tact

a narrower inner band consisting of synapses between photorecep-

which

tor

synapse,

of

contrast

synapses

among

a

and

in

bipolar

hue,

the

axon

begin

inner

and

a

in

this

layer.

plexiform

pair

of

layer

involve

postsynaptic

con-

processes,

25,79

cells

cone

and

cells

pedicles

from

the

synapse

inner

with

nuclear

bipolar

cell

layer.

Rod

dendrites

spherules

and

and

horizontal

of

an

may

be

an

thought

amacrine

amacrine

to

be

or

ganglion

inhibitor y,

process

with

a

cell.

involves

bipolar

A

the

axon,

reciprocal

second

contact

providing

nega-

42

cell

processes

consist

of

in

the

outer

invaginations

plexiform

in

the

layer.

Many

photoreceptor

of

these

terminal;

synapses

invagina-

tive

feedback.

located

in

Gap

the

junctions

inner

between

plexiform

layer.

amacrine

Some

cells

displaced

are

also

amacrine

25

tions

In

are

these

nous

to

deep

the

junctures,

plate,

the

in

the

ribbon

spherule

the

more

photoreceptor

synaptic

near

but

the

ribbon.

site

supercial

element

Synaptic

where

the

in

the

contains

vesicles

a

are

pedicle.

connected

neurotransmitter

and

ganglion

cell

bodies

may

also

be

seen.

membra-

is

released

Ganglion

e

Cell

ganglion

Layer

cell

layer

is

generally

a

single

cell

thick

except

76

allowing

quick

and

sustained

invaginating

synapse

and

a

is

called

cesses

the

and

center

are

are

triad.

deep

process

involved

in

generally

e

(see

has

lateral

within

cone

neurotransmitter

the

Fig.

and

elements

are

cones

bipolar

midget

have

at

cone

processes

horizontal

a

Invaginating

all

e

postsynaptic

invagination,

8.7).

triads,

three

release.

cell

pro-

dendrite

bipolar

least

one

is

cells

invagi-

near

at

the

the

macula,

temporal

Although

where

side

lying

of

side

it

the

by

might

optic

side,

be

eight

disc,

to

where

ganglion

10

it

cells

cells

is

are

two

thick,

cells

and

thick.

separated

from

each other by glial processes of Müller cells. Displaced amacrine

cells,

which

ganglion

send

cell

their

layer,

processes

as

may

outward,

some

may

displaced

be

found

Müller

cell

in

the

bodies

25

nating midget bipolar and one at midget bipolar contact.

Synaptic

in

the

contacts

outer

contact

with

also

plexiform

bipolar

occur

layer.

outside

invaginating

Horizontal

dendrites

and

cells

contact

make

other

and

synapses

astroglial

glion

cells

cells.

Toward

diminishes,

and

the

the

ora

serrata,

ner ve

ber

the

layer

number

of

gan-

thins.

synaptic

horizontal

cell

Nerve

Fiber

Layer

59,77

processes

called

via

inter woven,

processes

ties

are

in

seen

resemble

ing

gap

synaptic

a

junctions.

densities

are

branching,

the

as

outer

a

series

bipolar

of

is

within

dendrites

plexiform

dashed

discontinuous

membrane.

Desmosome-like

located

layer.

lines

membrane,

membrane

the

and

ese

on

light

termed

attachments

arrangement

horizontal

synaptic

the middle

demarcates

the

extent

nerve

ber

layer

(NFL) consists

of

ganglion

cell

axons.

eir

course runs parallel to the retinal surface. e bers proceed to the

cell

optic disc, turn at a right angle, and exit the eye through the lamina

densi-

microscopy

e

of

and

cribrosa

limit-

the

of

that

the

as

the

optic

nerve.

e

bers

generally

are

unmyelinated

within the retina. e nerve ber layer is thickest at the margins of

optic

disc,

radiate

where

to

the

all

disc

the

bers

from

the

accumulate.

macular

e

area

is

group

called

of

the

bers

papil-

23

retinal

vasculature

and

may

prevent

retinal

exudates

and

hem-

lomacular

bundle.

is

important

grouping

of

bers

carries

the

42

orrhages

from

spreading

into

the

outer

retinal

layers.

information that determines visual acuity.

Supercial

Inner

e

Nuclear

inner

Layer

nuclear

layer

horizontal

cells,

sometimes

displaced

cells

are

next

to

nate.

layer

e

inner

inner

axon

outer

to

e

cell

in

vasculature

and

cells,

the

to

has

the

of

cells.

outer

of

its

of

the

cells,

plexiform

dendrite

capillar y

nuclear

their

in

the

layer

of

the

layer,

amacrine

where

cell

bodies

Müller

nuclei

plexiform

deep

inner

e

the

layer,

inner

the

the

consists

amacrine

nuclei

plexiform

bipolar

its

(INL)

ganglion

next

synapse.

the

and

retinal

bipolar

located

processes

ber

cells,

are

is

termi-

plexiform

(see Fig.

network

their

located

processes

outer

and

common

and

e

inner

sists

and

Plexiform

of

8.8).

e

located

just

layer.

Internal

e

dendrites

layer

ganglion

the

Limiting

internal

face

of

this

expanded

covered

membrane

by

a

8.11).

is

basement

basement

in

(IPL;

also

inner

between

cells.

e

the

synaptic

axons

inner

of

layer)

bipolar

plexiform

layer

con-

cells

con-

Anteriorly,

continuous

body.

It

is

the

Müller

the

as

they

and

Müller

and

is

cells

in

the

Müller

ner ve

cells

ensheathe

limiting

composed

(oen

Vitreous

may

periphery

Fig.

8.8).

In

general,

the

axon

disc,

internal

cause

are

over

the

where

cells.

bipolar

cell

ends

in

the

inner

half

of

leave

the

limiting

internal

are

vessels

membrane)

of

called

bers

extensive,

footplates)

may

fuse

vitreomacular

vitreal

bers

globe.

membrane

limiting

macula

processes

Astrocytes

47

midget

they

(inner

membrane.

the

the

present

of

(see

the

with

of

invaginating

where

of

with

traction

typically

incor-

42

ron

the

uneven

of

membrane

Only

optic

pathway

layer,

primarily

Processes

membrane

terminations

the

visual

located

Membrane

limiting

at

the

ber

are

layer.

bers.

tains the synapse between the second-order and third-order neu-

in

ner ve

cell

porated into the internal limiting membrane.

connections

of

vessels

ganglion

forms the innermost boundary of the retina. e outer retinal sur-

this

Layer

plexiform

synaptic

in

ner ve

(Fig.

Inner

retinal

and

horizontal

where

cells

of

layer

of

membrane

but

undergoes

from

surround

astrocytes

the

ner ve

the

of

retina

the

is

ciliar y

modication

replace

ber

those

bundles

CHAPTER

8

121

Retina

and hyporeective layers (Fig. 8.13). Layers with axons and synapses are relatively

hyperreective,

and

layers

with

nuclei

are

relatively

hyporeective.

The

internal

limiting membrane is thin and brighter than the nerve ber layer.

Four

plex

bright

is

the

bands

most

represent

posterior

the

of

outer

the

four

retina.

The

RPE/Bruch

hyperreective

bands

membrane

(see Fig.

com-

8.13).

Al-

80

though there is some uncertainty about the exact histological correlation,

second

tor

and

layer.

third

The

bands

are

thought

hyperreective

band

to

represent

next

to

the

portions

RPE/Bruch

of

the

the

photorecep-

membrane

complex

likely represents the tips of the outer segments and is called the interdigitation

zone.

The

third

band

is

generally

thought

to

be

created

by

the

mitochondria

81

Fig.

8.11

Vitreomacular

traction

(red

arrow)

causing

distor -

within the ellipsoid zone.

Inner to the bright ellipsoid zone, the line represent-

81

tion

and

reous

a

pseudocyst

surrounding

the

(blue

fovea

arrow)

is

in

the

detached

foveal

(yellow

area. The

vit-

ing

the

external

limiting

membrane

is

dimmer

than

the

other

three

bands.

arrow).

NUMBER AND DISTRIBUTION OF NEURAL CELLS

It

is

4

million

estimated

that

there

are

80

82

than

are

to

5

of

cones

that

million

concentrated.

center.

fovea,

Rod

except

Rods

density

beginning

at

million

is

e

in

are

at

types

20

of

to

25

the

absent

greatest

macular

from

in

an

approximately

degrees

from

photoreceptors

110

density

3

the

million

the

rods

is

and

greater

where

the

concentric

degrees)

cones

macular

with

and

the

peak-

84

fovea.

diminishes

rods

foveola,

(7

58

of

region,

area

mm

42

ing

to

83

cones.

e

toward

number

the

ora

of

both

serrata.

85

ere

are

approximately

35.68

million

bipolar

cells

and

86

1.12

million

numerous

cating

to

8.12

from

Normal

the

around

internal

the

right

fundus

limiting

macula

and

of

a

young

membrane

blood

is

adult.

visible

as

The

and

ganglion

converge

renement

cells.

at

of

one

the

e

signals

ganglion

initial

from

cell,

response

indi-

of

the

cells.

sheen

reections

RETINAL

FUNCTION

vessels.

Light

and CLINICAL

million

photoreceptors

integration

photoreceptor

Fig.

2.22

COMMENT: Fundus

View

of

the

Internal

passes

through

stimulating

most

the

of

the

retinal

photoreceptor

layers

outer

before

segment

reaching

discs.

e

Limiting

neural

ow

then

proceeds

back

through

the

retinal

elements

Membrane

in Reections

from

the

internal

limiting

membrane

produce

the

retinal

sheen

the

opposite

direction

of

the

incident

light.

e

ecient

and

seen

accurate

performance

of

the

retina

is

not

hampered

by

this

with ophthalmoscopy. In younger persons, this membrane gives off many reections

seemingly

reversed

situation.

and appears glistening (Fig. 8.12). The sheen is less evident in older individuals.

Physiology

CLINICAL

OCT

provides

COMMENT: Optical

high

resolution,

Coherence

cross-sectional

in

Tomography

vivo

images

of

the

e

RPE

fosters

retina,

and

choroid

anatomy.

In

a

healthy

retina

the

the

the

RPE

health

of

the

neural

retina

and

the

cho-

vitreoretinal

riocapillaris

interface,

of

nerve

ber

in

several

ways.

First,

the

zonula

occludens

join-

layer,

ing

the

RPE

cells

are

part

of

the

blood-retinal

barrier.

e

ganglion cell layer, inner plexiform layer, inner nuclear layer, outer plexiform layer,

RPE and

outer

nuclear

layer

are

visible.

These

are

seen

as

alternating

selectively

controls

movement

of

nutrients

from

the

choriocapillaris

into

the

retina

Internal

Nerve

Vitreous

and

limiting

fiber

Ganglion

limiting

metab-

hyperreective

olites

External

and

removal

membrane

layer

cell

layer

membrane

Ellipsoid

zone

Interdigitation

zone

RPE/Bruch

Inner

plexiform

Inner

nuclear

layer

layer

Outer

plexiform

Outer

nuclear

layer

complex

Fovea

Fig.

8.13

The

retinal

layers

as

seen

externa

with

optical

coherence

tomography.

layer

CHAPTER

122

8

Retina

Rod

and

cone

outer

segments

Aquaporin

2HCO 3

H

O

+

2

+

H

Na +

+

K

Na

+

2Cl

Lac

H

+

3Na +

+

2K

Na

+

K

Cl Cl

+

H

Lac

Bruchs

membrane

Choriocapillaris HCO 3

Choroid

Fig.

of

waste

products

laris. A proposed

f rom

model

8.14

the

for

Proposed

retina

RPE

model

into

ion

the

8.14.

+

Na

Ion

movement

+

/K

occurs

by

Na

is

shown

and

Na

ATPase

in

pumps,

+

/2HCO

pigment

e

a

epithelium

relationship

reciprocal

one.

ion

transport.

between

When

the

either

RPE

layer

and

the

photoreceptors

dysfunctions,

the

other

is

is

+

/K

+

/2Cl

retinal

choriocapil-

transport

+

Fig.

showing

cotransporters,

Na

ultimately

aected.

Retinal

degenerative

diseases

and

dystro-

+

/H

and

phies

oen

cause

changes

in

the

RPE

that

are

clinically

visible.

3

Cl

/HCO

exchangers,

and

gated

and

ungated

ion

chan-

3

87

nels.

A

proton-lactate-water

cotransporter

moves

a

signiCLINICAL

cant

amount

of

lactate

(the

product

of

anaerobic

COMMENT: Retinal

Degenerations

metabolism) Retinitis pigmentosa is a hereditary retinal dystrophy resulting in a progressive

87

across

the

RPE

88

layer.

Water

passage

occurs

through

aqua-

loss

of

RPE

and

photoreceptor

function.

Both

rods

and

cones

undergo

apop-

+

porins

and

Cl

and

K

are

thought

to

be

the

primar y

ions

driv-

tosis.

Rods

are

affected

rst,

followed

by

loss

of

cone

function.

Cones

may

defect

with

89

ing

the

both

of

movement

the

apical

glucose

to

of

and

the

water.

basal

active

Glucose

membrane

transporters

maintain

a

located

steady

in

supply

remain

sparing

the

photoreceptors.

functional

of

the

sensory

s econd

retina

and

met ho d

in

w hich

chor io capi llar is

f rom

t he

continual

ment

dis cs.

is

shedding

Numerous

t he

by

of

RPE

t he

phago c ytosing

t he

lys os omes

supp or ts

wit hin

e ach

RPE

outer

cell

and

pattern

fovea,

eld.

resulting

As

the

RPE

accumulates

(Fig.

in

an

overall

visual

degenerates,

around

blood

eld

pigment

vessels

in

a

migrates

into

characteristic

8.15).

neural

f ragments

photoreceptor

the

central

retina

bone-spicule

A

in

s eg-

enable

Stargardt

macular

sulting

in

a

that

gene

vision

dystrophy

loss

directs

is

occurring

the

a

at

hereditary

an

production

early

of

a

autosomal

age.

protein

A

recessive

defect

that

has

been

facilitates

disorder,

re-

identied

transport

to

in

and

90

it

to

ingest

as

many

as

2000

dis cs

dai ly.

Undigested

mater ial

87

acc umulates

(A2E)

has

as

dep osits

b een

of

identied

lip of us cin.

in

Recent ly,

lip of us cin

dep osits

a

subst ance

t hat

from photoreceptor cells. Early in the disease, the RPE degenerates, and as the

disease

progresses,

lipofuscin-like

deposits

accumulate

in

the

macular

area.

app e ars

to inhibit RPE degradation of t he outer s eg ment remnants and

91

contr ibutes

and

stores

to

RPE

vit amin

92

ment

cell

A,

de at h.

one

of

ird,

t he

t he

RPE

comp onents

met ab olizes

of

photopig-

93

molec ules.

It

is

t he

site

for

par t

of

t he

bio chemical

90

pro cess

in

t he

contr ibute

to

ro d

t he

dis c

rene wa l

for mation

of

system.

t he

Four t h,

t he

75

b etween

RPE

t he

RPE

pro duces

cess es.

w hich

It

growt h

s ecretes

helps

t he

RPE

epit helial

als o

and

of

t hat

dr ive

endot helial

VEGF

fac tor.

cou ld

an

e

cer t ain

g rowt h

resu lt

in

t he

pro-

(VEGF),

Howe ver,

t he

neovas c ular izat ion,

antiangiogenic

balance

Fi h,

cellular

fac tor

f unc t ion.

cells

mat r ix

94

photoreceptors.

chor io capi llar is

pro duces

der ived

t he

fac tors

vas c ular

maint ain

over pro duc tion

so

layer

RPE

inter photoreceptor

fac tor,

b etween

t hes e

pig ment

cont r ibFig. 8.15

Fundus

of

a

patient

with

retinitis

pigmentosa.

Bone

95

utes

to

he alt hy

vas c ular

f unc tion.

Sixt h,

pigment

granules spicule-shaped

wit hin

lig ht

t he

RPE

s catter.

cells

abs orb

excess

lig ht,

t hereby

reducing

retina. The

center

subcapsular

retinitis

deposits

of

the

cataract,

pigmentosa.

of

pigment

image

another

is

are

evident

cloudy

common

in

because

feature

the

of

peripheral

a

posterior

associated

with

CHAPTER

bipolar

cells

and

250

AII

amacrine

8

123

Retina

cells

before

converging

onto

98

a

single

the

ganglion

cone

drive

ratio

a

between

single

cle,

axon

cells

rod

that

with

bipolar

Ganglion

cone

a

a

cells,

on

can

can

contact

a

single

drive

bipolar

the

is

cells

a

1:1

signicant

discriminate.

only

one

cone

cell.

whereas

because

rod

synapse

the

bipolar

with

connection

A

pedi-

ganglion

chain,

then

direct

cones

there

midget

chain

which

a

cone

reecting

three-neuron

being

ganglion

of

of

situations,

population

cells

there

number

number

some

four-neuron

amacrine

axons

small

may

synapses

involves

and

In

ganglion

the

than

cell

small

dendrite

then

rather

a

cell.

and

involves

synapse

glion

relatively

and

bipolar

pathway

pathway

cells

cell,

detail

its

cone

rod

the

of

A

ganglion

cones

midget

and

e

bipolar

single

amount

cell.

gan-

between

cells.

be

thought

of

as

carrying

informa-

tion in processing streams, such that certain types of information

25

are directed toward specic destinations.

lateral

geniculate

nucleus,

wherein

e major target is the

some

axons

terminate

in

the

parvocellular layers, which process wavelength, shape, ne detail,

and

lar

resolution

layers

ments

Fig.

8.16

with

Photo showing the right fundus of a 26-year -old patient

Stargardt

generation

is

seen

as

is

macular

present

yellow

dystrophy.

in

the

Retinal

macular

ecks. Visual

pigment

area.

acuity

is

epithelial

Lipofuscin

reduced

to

de-

deposition

of

and

Visual

bers

and

by

and

age

are

yellow

changes

50

to

years,

and

the

eck-shaped

photoreceptors

50%

of

patients

(Fig.

8.16).

follow.

affected

Eventually

Vision

can

loss

have

is

to

20/200

or

but

in

the

have

the

ciliary

end

poor

iris

the

magnocellu-

discern

wavelength

midbrain

and

in

which

are

move-

sensitivity.

important

muscles.

Other

in

the

centers

eye,

in

the

RPE

head,

and

vision,

neck

ganglion

nucleus

to

aid

in

movements.

cells

bers

regulating

Although

connect

the

not

with

circadian

directly

the

supra-

rhythm.

at-

progressive,

reduction

of

visual

CLINICAL

96

acuity

of

axons

nucleus,

that receive visual information can inuence motor pathways that

chiasmatic deposits

light

terminating

control

Other

geniculate

20/200.

involved

rophies

contrast.

lateral

ickering

autonomic

control

These

of

the

COMMENT: Electroretinogram

worse.

An electroretinogram is a recording of the electrical response of the retina to a

light

stimulus.

measured

Scotopic

In

dim

light

and

light,

Photopic

the

detection

detection

by

cones

ing

Vision

by

rods

takes

predominates,

precedence.

Rods

and

are

in

in

certain

a

The

retinal

are

least

retina

Its

in

is

light

to

In

recognize

scotopic

of

wavelengths.

the

seen

retina

Bright

in

is

vision),

conditions,

at

detail

are

dominates

when

(scotopic

objects

ne

Objects

activity

light),

conditions

detection

absent.

Cone

bright

lit

responsive.

allows

ability

vision

poorly

low

is

in

poor,

photopic

responsive

is

of

illumination.

and

a

color

gray.

(i.e.,

broader

necessar y

e

complex

lions

of

for

of

the

ash

be

of

light

useful

or

a

light

pattern.

diagnostically

in

It

can

be

differentiat-

8.17).

Neural

tigated

range

the

structure

neurons

in

and

studies

knowledge

conditions

to

(Fig.

a

can

Retina

cones

light-sensitive

of

diseases

be

and

bright

when

however,

shades

illumination

the

levels

may

setting

extremely

Physiology sensitive

stimulus

clinical

of

the

of

of

the

retina

synapses,

cats,

and

rabbits,

retinal

contains

has

and

circuitr y

is

been

millions

monkeys.

based

and

extensively

on

Although

animal

mil-

inves-

most

models,

in

of

sharp

visual acuity and color discrimination of photopic vision. Cones

are

as

designated,

red

(588

depending

nm)

or

on

L-cones,

the

green

wavelength

(531

nm)

or

that

they

absorb,

M-cones,

or

blue

97

(420

nm)

Neural

e

or

Signals

neural

processed

it

S-cones.

passes.

ganglion

signal

within

ere

cell

generated

the

is

a

when

by

complex

greater

signals

photoreceptors

synaptic

convergence

originate

is

pathway

from

of

modied

through

information

rods

rather

and

which

onto

than

a

from Fig.

cones.

e

regions,

light

ratio

of

resulting

and

motion.

rods

in

It

to

ganglion

tremendous

is

estimated

cells

is

high

sensitivity

that

75,000

for

in

the

rods

most

retinal

detection

drive

5000

of

rod

8.17

Multifocal

idiopathic

creased

blind

signal

retina. The

right

in

electroretinogram

spot

the

eye

enlargement

left

(OD)

eye

has

a

(OS)

in

a

patient

syndrome.

corresponding

normal

signal.

with

Note

to

acute

the

the

de-

nasal

CHAPTER

124

visual

scientists

applicable

Retinal

to

have

the

8

found

human

ion

activity

channel

in

synapse,

is

a

chemical

allowing

rapid

rate

necessar y.

and

of

the

information

to

be

gap

current

of

Gap

signal

to

e

pass

or

gap

are

cells,

neurons

by

directly

found

between

an

follow

a

by

cells,

and

ensur-

mediator

photoreceptor

horizontal

bipolar

axon

cell,

and

an

and

current

bipolar

and

occurs,

with

the

ow

horizontal

more

cell

hyperpolarizes,

through

cells,

the

some

organization

retina.

which

e

organization

and

starts

signal

processing

and

an

passes

to

processing

occurring

as

the

signal is transferred to amacrine and ganglion cells. Once a gan-

glion

electrical

chemical

between

photoreceptor

and

is

between

No

occurs

neurotransmitter

junction

transmission.

between

horizontal

retinal

junctions

junctions

photoreceptor,

between

at

between

synapses.

changes

electrical

Synapses

transmission

ing

much

retina.

Information

release

Retina

cell

A

a

is

activated,

visual

membrane

opsin

ecule

the

protein,

forms

membrane

that

a

long

bilayer

actually

looped

its

pigment

axon

called

helix

an

that

seven

the

opsin,

loops

times.

absorbs

protein.

carries

(photopigment)

the

and

a

back

e

to

of

a

brain.

parts,

chromophore.

and

and

the

two

forth

chromophore

photon,

11-cis-retinal,

message

consists

is

is

the

contained

derivative

of

e

across

the

mol-

within

vitamin

A,

is

25

amacrine

process.

Chemical

synapses

neurotransmitter

tic

cle.

e

the chromophore present in all photoreceptors. e seven-looped

contain

from

the

transmitter

synaptic

presynaptic

binds

to

vesicles

terminal

specic

sites

that

into

on

release

the

the

a

synap-

postsynap-

opsin

determines

its

protein

is

tic membrane, eliciting an excitator y or inhibitor y change in that

throughout

neuron.

brane

Outer

part

of

e

synapses

which

the

plexiform

pedicle

allow

in

for

electron-dense

or

in

the

fast

bar

layer

synapses

invaginations

invaginations

and

sustained

surrounded

occur

in

are

either

spherules

oen

and

ribbon

neurotransmitter

by

a

large

on

the

at

pedicles.

synapses,

release.

number

of

An

synaptic

the

wavelength

absorbed

by

a

photoreceptor.

e photopigment in rods is arranged in the disc membranes and

is

that

red

ture

deep

form

sensitive

of

acids,

the

rhodopsin.

the

these

and

the

cone

and

two

the

In

cones,

infoldings

in

discs.

of

e

M-cones

for

X-chromosome.

them

Blue

are

photopigment

continuous

protein

is

photopigments

genes

the

the

green

opsin

diers

by

in

sensitive

in

only

a

S-cones

located

mem-

L-cone

sensitive.

located

is

plasma

e

a

few

tandem

cells

struc-

amino

array

(comprising

on

only

78

vesicles

aptic

extends

into

membrane.

vesicles

to

sustained

a

the

e

release

release.

cytoplasm

ribbon-like

site

on

Calcium

the

ion

perpendicular

structure

seems

presynaptic

channels

to

the

to

presyn-

guide

membrane,

facilitate

the

causing

vesicle

5%–10%

fusion

e

of

cone

population)

photoreceptor

stimulated

state,

the

the

by

light.

is

As

in

the

are

depolarized

neurons

photoreceptor

structurally

usually

secretes

its

dierent.

state

do

in

when

the

it

is

not

depolarized

neurotransmitter.

During

++

with

the

more

membrane

vesicles

per

and

promote

second

are

high-speed

released

at

a

release.

ribbon

T en

synapse

times

than

at

depolarization,

cium

ions

voltage-gated

facilitate

the

Ca

process

channels

by

which

are

the

open,

vesicles

and

cal-

containing

19

a

conventional

synapse.

Triads

are

ribbon

junctions,

located

in

glutamate

the outer plexiform layer, that have three postsynaptic processes.

of

Dyads

the

with

are

two

occurs

ribbon

synapses

postsynaptic

in

the

striate

found

processes.

cortex,

in

the

inner

Although

there

is

plexiform

visual

signicant

layer

interpretation

organization

and

merge

with

neurotransmitter

photoreceptor

the

into

cell

the

terminal

membrane

synaptic

is

enabling

cle.

continually

us

the

in

releasing

release

the

dark,

glutamate.

e depolarized state occurs because of an ion circuit within the

photoreceptor.

e

photoreceptor

outer

segment

is

permeable

+

processing

within

of

the

neural

retina.

signals

e

in

excitator y

process

is

and

extremely

inhibitor y

complex

circuits

and

most

to

Na

.

e

cyclic

guanosine

monophosphate

(cGMP)-gated

cationic channels in the outer segment membrane are kept open

+

current

understanding

is

based

on

animal

studies.

because

moves

Neurotransmitters

the

of

into

ions

a

high

the

pass

concentration

outer

easily

segment,

into

the

is

the

excitator y

neurotransmitter

released

by

where

+

Na

is

extruded

by

cytoplasmic

through

inner

+

Glutamate

of

Na

the

segment

open

cGMP .

Na

channels

through

the

and

cilium,

+

/K

ATPase

pumps

(Fig.

8.18).

+

photoreceptors,

GABA

crine

are

cells.

bipolar

inhibitor y

It

is

cells,

and

ganglion

neurotransmitters

unclear

what

cells.

Glycine

released

neurotransmitter

from

and

ama-

horizontal

cells

is

circuit

exiting

state

the

the

(caused

inner

by

Na

moving

segment),

photoreceptor

is

is

into

called

the

the

depolarized

outer

dark

with

a

segment

current.

In

membrane

and

this

poten-

99,100

secrete,

but

GABA

rotransmitters,

neuron

may

be

involved.

neuromodulators

transmission.

ey

are

are

In

addition

chemicals

released

by

that

retinal

to

neu-

can

cells

tial

alter

into

the

of

approximately

Within

a

a

−40

picosecond

biochemical

cascade

mV .

of

light

occurs

activating

that

results

the

in

visual

a

pigment,

decrease

+

extracellular

space

the

cle.

synaptic

but

not

ey

necessarily

include

by

synaptic

dopamine,

nitric

vesicles

oxide,

at

and

concentration

inside

of

the

of

cGMP

cell

thus

increases

closing

in

the

negativity

Na

in

the

78

channels.

because

of

e

the

con-

+

retinoic

mine

acid.

can

As

an

change

horizontal

cells

example

the

and

of

a

neuromodulator

conductance

modulate

of

gap

responses

eect,

junctions

to

changes

dopa-

between

in

back-

tinued

loss

of

membrane,

brane

Na

and

potential

through

the

cell

the

pumps

becomes

approaches

−75

in

the

inner

hyper polarized.

mV .

e

change

in

segment

e

mem-

potential

is

101,102

ground

illumination.

graded,

of

Phototransduction

Phototransduction,

light

the

process

by

which

a

photon

of

light

of

absorbed

activated.

the

level

e

is

the

change

photoreceptors.

ing

or

the

ion

in

hyperpolarization

and

the

number

magnitude

the

amount

of

of

the

of

depends

visual

on

the

pigment

hyperpolarization

transmitter

released,

amount

molecules

determines

either

slow-

78

changed

Visual

light,

to

an

electrical

pigments

initiating

in

the

the

signal,

occurs

photoreceptor

process

of

vision.

in

the

outer

A

segment

series

of

absorb

biochemical

stopping

larized

the

channels

and

ow.

open

releases

Once

and

the

the

cell

glutamate.

level

once

e

of

cGMP

again

amount

is

restored,

becomes

of

depo-

transmitter

CHAPTER

indicate

ing

up

that

the

Müller

cell

all-trans-retinol

has

and

a

role

8

125

Retina

in

the

visual

reisomerizing

it

to

cycle

by

tak-

11-cis-retinol.

is is then transported back to the cone and oxidized to 11-cis

103

retinal,

steps

cone

which

of

the

rod

renewal

Information

Once

its

the

are

a

+

renewal

system

through

will

take

Because

hundred

into

system

are

still

are

the

104

photopigment.

well

known,

but

e

those

of

the

unclear.

Processing

integrated

sity.

incorporated

photoreceptor

circuit

cessing

is

the

place

and

neurons,

the

better

million

million

activated

before

allowing

a

is

retinal

signal

detection

ganglion

cells

photoreceptors,

the

message

organization

exits

of

the

there

eye.

contrast

receive

be

pro-

Signals

and

input

must

begins

and

inten-

from

a

over

systematic

2K

Inner

process

to

control

and

relay

photoreceptor

messages.

Retinal

segment

neurons

+

have

been

given

designations

as

ON

cells

or

OFF

cells

3Na

as

a

means

to

Vertical

cells

by

describe

the

Processing.

the

light

processing

Retinal

condition

schematic.

neurons

when

the

are

cell

named

is

ON

or

depolarized.

OFF

A

cell

that is depolarized with light OFF is called an OFF cell and a cell

that

all

is

depolarized

photoreceptors

with

light

ON

depolarize

in

is

the

called

dark,

an

all

ON

cell.

Because

photoreceptors

are

+

Na

OFF

cells.

Glutamate

will

cause

a

bipolar

cell

to

either

depolarize

or

Outer

+

Na

hyperpolarize

segment

depending

on

the

type

of

receptor

105

plasma

with

ionotropic

mate

a

membrane

(which

that

respond 8.18

Photoreceptor

dark

current.

The

dotted

lines

released

105

bipolar

in

by

are,

their

the

with

Bipolar

membrane

respond

photoreceptor

OFF

in

the

bipolar

receptors

a

in

in

the

106

dendrite.

therefore

metabotropic

glutamate

repre-

bipolar

and

have

to

the

receptors

depolarization

cells

Fig.

is

of

present

to

dark)

cells.

their

hyperpolarization

cells

gluta-

with

Bipolar

membrane

and

are

ON

106

cells

e

neurotransmitter

at

the

axon

terminal

in

+

sent

the

dark

current.

Na

enters

the

outer

segment

through

bipolar cells is also glutamate and bipolar cells release glutamate +

ligand-gated

channels,

+

truded

by

Na

ions

pass

through

the

cilium,

Na

is

ex-

when

+

/K

ATPase

pumps

in

the

cell

membrane

of

they

When inner

segment.

proximately

The

−40

cell

membrane

potential

in

the

dark

is

light

mV .

absorbed

In

the

the

photoreceptor

decreases

as

the

amount

of

light

increases.

rod,

the

to

of

phototransduction

begins

with

the

of

and

is

II,

11-cis-retinal,

activated

stimulates

leading

the

to

form

of

forming

rhodopsin,

transducin,

closing

of

photoreceptor.

photopigment.

which

sodium

Finally,

e

All-trans-retinal

the

visual

also

is

the

metarhodopsin

breakdown

and

of

cGMP

hyperpolarization

all-trans-retinal

from

all-trans-retinal.

called

causes

channels

pigment

moves

isomer

dissociates

now

said

disc

lumen

to

be

from

the

the

cyto-

it

opened

it

is

cGMP

it

is

occurs,

causing

of

specic

carrier

proteins

within

the

it

must

be

transported

interphotoreceptor

state.

depolarized

by

matrix

glutamate.

on

cell

release

(thus

a

When

bipolar

membrane,

glutamate.

in

the

hyperpolarized

When

glutamate

at

the

the

cation

bipolar

glutamate

cell

release.

in

the

it

is

in

the

dendrite,

causing

is

dark.

glutamate

dark,

is

an

When

binds

cation

the

OFF

chan-

bipolar

cell

bipolar

cell

glutamate

binds

to

release

ionotropic

is

channels

to

in

the

hyperpolarize,

is

is

an

ON

cell

membrane

resulting

bipolar

cell

in

a

because

dark.

photoreceptor

reduced

receptor

is

or

hyperpolarized

stopped.

causes

the

e

(light

lack

of

is

ON),

glutamate

glutamate-gated

cationic

channels in the bipolar membrane to close. e OFF bipolar cell

glutamate

so

the

closing

the

hyperpolarizes,

molecule,

is

receptor

depolarized

cannot

the

depolarized

releasing

in

and

plasm where it is reduced to all-trans-retinol. e photoreceptor

reisomerize

is

ionotropic

are

decrease

of

bleached.

into

the

the metabotropic receptors on a bipolar cell dendrite, a decrease

ble

in

OFF),

because

process

in

photoreceptor

depolarize

absorption of a photon of light that causes the breaking of a dou-

bond

is

the

nels

by

a

ap-

to

released

are

the

at

the

is

reducing

reduced

metabotropic

or

its

no

release

longer

receptor

of

neurotransmitter.

present,

signals

a

the

lack

cGMP

of

When

glutamate

cascade,

cGMP

87

to

the

RPE.

trans-retinol

11-cis-retinal.

the

e

to

RPE

11-cis-retinol

11-cis-retinal

interphotoreceptor

opigment.

In

contains

the

cone

is

matrix

the

and

then

to

recycling

be

enzymes

nally

that

oxidize

transported

incorporated

process,

some

convert

it

back

into

back

all-

to

through

the

animal

increases,

cGMP-gated

cation

channels

open,

and

the

ON

bipo-

lar cell depolarizes, which increases its neurotransmitter release.

Succinctly

put:

phot-

hyperpolarize

in

models

hyperpolarize

in

OFF

light.

dark.

bipolar

ON

cells

bipolar

depolarize

cells

in

depolarize

in

dark

light

and

and

CHAPTER

126

8

Retina

Some current literature uses other terms. OFF bipolars are also

responds,

and

called hyperpolarizing bipolar cells and ON bipolars are also called

locations.

All

depolarizing bipolar cells. is terminology reects the state of the

intensity of which is determined by the intensity of the stimulus.

bipolar

cell

when

designation

does

the

not

light

is

imply

on.

that

Recognize

the

that

bipolar

cell

the

ON

itself

is

or

OFF

respond-

e

the

P

lar

light.

midget

OFF

bipolar

cells

may

also

be

referred

to

as

sign

preserving

signal

ganglion

lateral

ing to the light condition; only photoreceptors respond directly to

a

other

cells,

cells

geniculate

and

carr y

ganglion

is

sent

retinal

to

higher

neurons

terminate

nucleus,

color

cells,

in

are

ner vous

graded

the

e

concentrated

with

P1

in

system

responses,

par vocellular

associated

information.

are

central

give

layers

cone

cells,

of

bipo-

also

central

the

called

retina

and

78

because they have the same response as the photoreceptors, that is,

constitute

both

cells

are

depolarized

in

the

dark.

ON

bipolar

cells

are

sign

invert-

ing because they have the opposite response as the photoreceptor.

In

general,

toreceptor

only

with

central

the

ON

bipolar

invagination,

cones

retina

on

the

contacts

and

at

dendrite

the

part

both

an

OFF

of

bipolar

the

ON

synapses

dendrite

pedicle.

and

an

within

Each

OFF

a

pho-

synapses

cone

midget

in

the

late

project

have

of

such

they

can

of

to

nucleus.

because

bipolar

80%

the

the

ey

their

cell

magnocellular

have

large

expansive

respond

Horizontal

ganglion

also

been

spreading

processes

rapidly

to

Integration.

layers

of

called

and

cover

or

vertical

the

M

large

changing

genicu-

ganglion

cells

B ecause

they

trees.

a

ganglion

lateral

parasol

dendritic

moving

e

population.

area

of

retina,

stimuli.

connections

through

the

78

cell.

All

rod

Bipolar

aptic

a

the

and

of

outer

ON

the

tier,

ON

the

a

axon

and

inner

are

in

is

processes

dendrite.

tiers

cells

end

bipolar

amacrine

glion

ent

axons

conguration

between

two

bipolar

and

or

a

bipolar

the

OFF

the

inner

a

and

terminate

bipolars

syn-

synapse

elements,

inner

tier,

One

of

process

axons

layer.

retina

layer.

consists

postsynaptic

(nearest

in

8.19).

plexiform

amacrine

plexiform

synapse

(Fig.

which

two

one

OFF

cells

inner

dyad,

sublamina

bipolars

ON

either

one

in

gan-

nuclear

sublamina

in

layer),

b,

closest

been

interconnect

retina

to

be

with

in

Horizontal

gap

chemical

vide

a

location,

through

described,

by

a

thus

cells

signal

synapses

the

ganglion

ganglion

signal

cells

must

Bipolar

which

are

action

cell

directly

pass

cells

the

layer.

transfer

rst

potential.

cells

Once

bipolars

with

four

the

do

amacrine

neuron

information

in

a

a

signal

from

a

from

ey

sent

to

link

by

a

one

cells

region

of

photoreceptor

in

a

dierent

message.

with

receive

other

horizontal

excitator y

photoreceptors.

feedback

amacrine

photoreceptor

the

communicate

and

and

input

Horizontal

photoreceptors

and

cells

through

cells

pro-

inhibitor y

feed

78

Rod

but

through

a

modifying

78

to

horizontal

direction.

allowing

junctions

inhibitor y

but

horizontal

another

inuenced

retinal

dier-

synapse

have

visual

threshold

to

synapse

cells.

chain

to

reached,

us

respond

for ward

rod

8.19).

ganglion

the

with

the

(see Fig.

retinal

pathway

is

not

cells,

with

ganglion

an

cell

In

the

the

bipolar

dark,

excitatory

depolarized.

larizes

close

ize.

and

in

e

cells.

while

the

With

light

the

cell

and

is

the

continuously

duration

of

its

response

hyperpolarization,

98

to

are

channels

hyperpolar-

depends

and

thus

on

the

on

the

107

intensity and duration of the light stimulus.

Cone

it

cells

hyperpo-

Ligand-gated

causing

the

releasing

horizontal

photoreceptor

reduced.

membrane,

photoreceptor

is

glutamate,

stimulation,

release

horizontal

amplitude

of

photoreceptor

neurotransmitter

transmitter

the

strength

Rod

to

Because horizontal

cells are joined by gap junctions, a great number of horizontal cells

can be aected when just one is inuenced by a photoreceptor.

e

from

was

mechanism

the

once

tor y

by

horizontal

thought

which

cell

that

neurotransmitter

doubts

that

GABA

rod

a

bipolar

is

horizontal

GABA.

is

inhibitor y

cone

not

cell

player

in

is

passed

understood.

released

the

studies

have

Subsequent

major

message

fully

the

feedback

It

inhibi-

raised

process

108

cells.

It

is

speculated

(based

on

animal

bipolar

models)

cell ON

horizontal

the

the

the

101

from ON

to

that

a

change

in

the

horizontal

cell

polarization

causes

cell

a A-II

current

change

in

the

extracellular

potential

in

the

synaptic

cell ++

cle

OFF

bipolar

within

in

the

release

membrane

would

Glycine

junction

ganglion

OFF

cell

8.19

tion.

the

cases

Amacrine

ganglion

sublamina

sublamina

could

e

bipolar

cone

aect

the

Ca

without

change

dendrites

inuencing

channels

actually

in

might

cells

reverse

also

their

carr y

the

synaptic

changing

the

neurotransmitter

within

the

cone

release

invagination

107

and

108

reaction.

dendrite

OFF

synapses

on

synapses

bipolar

axon

the

within

at

part

the

terminates

of

the

cone.

photoreceptor

in

sublamina

ere

are

40

dierent

information

types

but

the

in

a

horizontal

circuitr y

of

direc-

only

a

few

a

b

Schematic of ON and OFF bipolar pathways. The

dendrite

The

glutamate

the

cell

ON

bipolar

is

of

101

OFF

bipolar

of

potential.

aect

some

tion.

Fig.

membrane

synapse

in

ON

invagination.

synaptic

vesicle

Gap

an

cell

has

been

established.

and

release

either

Amacrine

GABA

or

cells

glycine.

are

generally

Amacrine

inhibitor y

processes

make

OFF

The

conventional

synapses

cell

or

with

bipolar

axons

and

with

ganglion

ON

dendrites

soma.

e

conventional

chemical

synapse

with

invagina-

a,

and

the

bipolar

cell

axons

is

a

feedback

synapse;

synapses

on

ganglion

109

ON

bipolar

relays

rod

axon

terminates

signals

to

both

in

ON

sublamina

and

OFF

b. The

AII

ganglion

amacrine

cells.

cell

cells

are

with

other

feed-for ward

amacrine

synapses.

cells.

Amacrine

cells

also

synapse

CHAPTER

e

the

narrow-eld

intermediary

rod

amacrine

between

the

cell,

rod

AII,

bipolar

releases

and

the

glycine.

It

ganglion

is

cell.

inhibits

is

seen

the

at

response

the

level

from

of

the

the

cells

bipolar

8

in

127

Retina

the

cells,

center.

is

ganglion

pattern

cells,

lateral

78

An

AII

e

amacrine

AII

cell

pathways.

axon

(an

cell

gathers

provides

e

ON

AII

a

cell

cell)

in

information

connection

receives

from

between

information

sublamina

b

of

the

about

the

ON

from

inner

300

a

rods.

and

rod

geniculate

OFF

bipolar

plexiform

layer,

round

is

nucleus,

are

activated,

changed

response

and relays information by a conventional synapse to an OFF cone

zontal

bipolar

axon

and

to

the

occurs

cells

the

part

cor tex.

signal

opposite

in

and

striate

coming

response.

because

because

of

When

of

from

e

lateral

amacrine

cells

in

the

sur-

center

cell

center-surround

inhibition

cell

the

activity

by

on

hori-

bipolar

113

cell

in

sublamina

a,

thereby

inuencing

an

OFF

ganglion

cell. e AII cell also carries rod information to an ON cone bipo-

lar

axon

through

gap

junctions

in

sublamina

b

and

inuences

terminals.

e

center-surround

conguration

allows

a

neuron

to

not

an

only respond to a direct message but to gather information from

AII amacrine cells, whose processes are joined

neighboring areas providing details about the bigger picture that

59

ON ganglion cell.

78

by

gap

junctions,

e

A17

ing

cells.

not

appear

form

a

amacrine

ey

appear

weak

electrical

cells

are

to

syncytium.

wide-eld

interconnect

rod

then

diusely

bipolar

branch-

cells

but

do

of

inuences

edges

retinal

and

that

in

contrast

neuron.

the

is

recognition

sensitivity

process

of

through

aides

contrast,

a

wide

in

the

and

range

it

of

detection

maximizes

background

78

to

make

synapses

with

other

amacrine

or

ganglion

illuminations.

109

cells.

A

single

A17

amacrine

cell

can

receive

input

from

as

A

circular

receptive

eld

can

be

either

ON-center/OFF-

109

many

nals

as

in

1000

dim

e

of

synapse

amacrine

dendritic

scotopic

diering

bipolars.

ey

are

thought

to

amplify

sig-

vision

light

with

cell

tree.

ow

It

is

a

wide-eld

seems

and

conditions.

cone

surround

the

illumination.

A18

extensive

rod

in

It

bipolar

to

have

a

modulating

can

interfere

cells

and

amacrine

role

in

the

retinal

with

an

adaptation

the

eectively

with

regulation

AII

to

amacrine

reduce

the

or

annular

that

is,

OFF-center/ON-surround.

region,

when

message,

but

an

the

message

ON-center

when

cells

in

cell

its

from

is

When

the

stimulated,

surround

light

center

are

it

also

is

falls

on

inhibited:

sends

its

ON

stimulated,

the

ON-center cell will be inhibited and the ON message is not sent,

and

instead

size

if

the

can

sent

an

OFF

surround

of

message

an

is

recognized.

OFF-center

cell

is

e

converse

stimulated.

e

occurs

message

98

of the

receptive

disrupt

crine

the

cells.

eld.

gap

e

junctions

Dopamine

A18

that

releases

form

released

by

the

the

dopamine,

syncytium

A18

which

of

AII

amacrine

from

the

center

will

be

an

ON

message.

ama-

cells

may

Light

and

Dark

Adaptation

110

also

have

Some

has

some

function

researchers

processes

in

in

have

both

the

the

circadian

identied

outer

an

cycle.

e

interplexiform

plexiform

layer

and

cell

inner

that

plexi-

visual

analysis

of

system

is

patterns

highly

of

light.

specialized

By

visual

for

the

detection

adaptation,

it

can

and

modify

its capacity to respond at extremely high and low levels of illumi-

41,111

form

layer

and

Receptive

made

OFF

up

of

cells

a

dark

glion

e

light

that

two

and

on

a

signals

signal

information

image

cells

convey

Fields.

provide

ferentiating

to

could

from

reaching

many

information

dark

respond

to

a

each

layers.

ganglion

photoreceptors.

Ganglion

background

light

these

processing

signals.

lighter

between

image

are

on

a

ON

channels

cells

OFF

that

cells

darker

nation.

cell

for

is

a

dif-

longed.

gan-

background

e

and

and

respond

and

ease

level

the

signicant

going

At

It

the

take

which

light

are

are

illumination

a

to

occurs,

for

the

stimulated

but

and

aect

to

dark

can

adapt

(dark

because

the

both

responds.

adaptation

retina

complete

functioning,

not

can

photoreceptor

level

minutes

sunlight

cones

they

in

30

bright

only

dark

background

with

change

can

from

rst

of

speed

rods

the

When

be

fully

pro-

when

adaptation).

they

are

take

some

now

in

time

112

are ON cells.

Flat bipolar cells are the start of the OFF channel

and

invaginating

e

ON

and

bipolar

OFF

cells

channels

photoreceptor-bipolar

are

in

the

the

connection

start

cone

of

the

ON

pathway

because

cones

channel.

begin

at

synapse

the

with

to

reach

plete

e

maximum

dark

to

cones

do

rods.

tor

is

function.

bright

reach

e

light,

their

state

of

Light

takes

full

adaptation,

going

approximately

function

adaptation

much

5

to

more

(sensitivity)

of

from

10

com-

minutes.

quickly

a

than

photorecep-

++

both

rod

ON

and

synapses

OFF

only

bipolar

with

an

cells.

ON

In

the

bipolar,

rod

the

pathway,

because

competing

a

channels

of

regulated

cGMP ,

the

by

Ca

,

which

messenger

that

can

inuence

controls

gated

the

ion

concentration

channels

in

the

78

begin

with

Retinal

elds.

or

in

the

a

lar

A

are

of

the

contact,

can

joined

by

can

eld

retina

neuron.

consists

that

amacrine

processing

retinal

direct

AII

receptive

area

cell

cells

the

of

as

gap

that,

those

well

be

photoreceptor

described

consists

e

of

when

the

receptive

all

it.

the

the

terms

in

eld

for

cells

a

a

eld

which

and

bipo-

it

is

Retinal

extensive

tion

requires

primar y

horizontal

Glucose

cells

consequently

Metabolism

e

in

horizontal

is

eld

response

particular

with

membrane.

receptive

visual

elicits

neighboring

receptive

of

the

photoreceptors

Because

junctions,

in

area

stimulated,

photoreceptor

as

inuence

cell.

network

extensive

source

moves

of

out

of

energy

of

continual

energy

the

is

intracellular

utilization

provided

blood

and

by

by

into

communica-

retinal

glucose

retinal

tissue.

e

metabolism.

tissue

via

facili-

tated diusion. Glucose transporters are located on both the api-

cal

and

basal

membranes

of

the

retinal

pigment

epithelial

cell

19

enlarged

beyond

Retinal

pattern.

its

dendritic

receptive

When

light

elds

tree.

are

activates

and

arranged

cells

in

in

the

a

center-surround

center

of

the

eld,

a

on

switch

need,

the

endothelium

from

but

glycolysis

even

under

of

to

retinal

capillaries.

oxidative

normal

e

metabolism

physiological

retina

can

depending

conditions,

the

on

ret-

78

given

response

annular

region

occurs.

When

immediately

light

around

falls

the

on

the

surround

center),

an

(the

antagonis-

ina

has

a

pathway

high

is

rate

of

anaerobic

particularly

active

glycolysis.

in

e

monophosphate

photoreceptors

for

rhodopsin

19

tic

response

occurs.

e

response

by

the

cells

in

the

surround

regeneration

and

ribose

production

for

nucleotide

synthesis.

CHAPTER

128

Müller

cells

store

8

Retina

glycogen,

providing

a

ready

source

of

glucose.

Central Because

high.

in

energy

Capillar y

primates

requirements

blood

and

is

ow

are

in

high,

retinal

approximately

oxygen

tissue

60

consumption

has

been

mL/min/100

measured

g

of

Retina

is

tissue,

Macula

e

Lutea

macula

lutea

appears

as

a

darkened

region

in

the

central

114

similar to the ow in the brain.

ceptors

is

3

to

4

times

higher

Oxygen utilization by photore-

than

other

central

diuse

from

ner vous

system

retina

of

(see

the

Fig.

8.12)

xanthophyll

and

may

seem

pigments,

to

lutein,

have

and

a

yellow

hue

zeaxanthin.

because

ese

pig-

19

neurons.

laris

to

blood

Because

the

inner

ow

is

oxygen

segments

signicantly

must

where

higher

the

in

the

choriocapil-

mitochondria

the

are

located,

choriocapillaris,

that

is,

ments

are

2000

mL/min/100

g

of

tissue,

than

in

the

retinal

throughout

the

retina,

but

the

greatest

concen-

tration is in the macula. e pigments are primarily located in the

photoreceptor inner bers but are also found in the rod outer seg-

78

approximately

located

115

116

ments.

e

newborn

has

little

if

any

of

these

pigments,

but

114

capillaries.

oxygen

In

that

the

the

dark,

oxygen

the

photoreceptors

tension

in

the

tissue

consume

is

near

so

zero,

much

and

the

they

act

gradually

as

lters,

accumulate

absorbing

from

short

dietary

sources.

wavelength

ese

visible

pigments

light

to

reduce

78

photoreceptors

are

operating

under

near

ischemic

conditions.

chromatic

aberration

and

may

also

have

an

antioxidant

eect,

115

suggesting a protective role against ultraviolet radiation damage.

e

REGIONS

OF

THE

macula

lutea,

perifovea,

is

approximately

e retina is oen described as consisting of two regions: periph-

approximately

3.5

eral

approximately

1

and

central

detecting

gross

(Fig.

specialized

for

most

retina,

in

of

the

cones,

has

8.20).

form

and

visual

more

which

includes

the

5.5

in

fovea,

parafovea,

and

RETINA

e

acuity.

and

peripheral

motion,

rods

ganglion

In

area,

the

dominate.

cells

retina

whereas

per

is

designed

central

peripher y

e

area

the

central

than

for

area

makes

retina

is

elsewhere,

is

up

rich

and

is

nal

pigment

than

of

cells

this

from

mm

mm

inferior

epithelial

elsewhere

area.

cells

in

However,

person

to

lateral

the

the

person.

mm

to

to

are

the

the

of

and

the

of

of

the

center

disc

disc.

e

more

to

pigment

choroidal

Its

optic

the

contain

contributing

density

e

edge

center

taller

retina,

diameter.

reti-

pigment

the

darkness

varies

capillar y

is

and

greatly

bed

also

is

117

a

relatively

small

portion

of

the

entire

retina.

thicker

in

the

Useful

subfoveal

color

area

than

vision

occurs

center

of

elsewhere.

in

an

area

approximately

9

mm

25

CLINICAL

When

on

the

the

eyes

macular

sometimes

on

COMMENT: Peripheral

more

are

looking

area

in

described

peripheral

the

as

straight

central

that

retinal

seen

ahead,

retina.

“out

regions.

in

Vision

the

The

of

the

Detail

object

rest

of

corner

and

color

of

the

of

of

interest

eld

one’s

that

eye,”

objects

in

is

imaged

is

in

is

focused

the

view,

diameter,

of

vision

are

evident,

but

the

objects

in

the

periphery

are

less

is

peripheral

the

eye

or

quite

areas

head

sensitive

often

to

change,

stimulates

toward

the

the

and

even

retina

and

slight

movement

frequently

elicits

a

the

macula

lutea.

ere

are

is

insensitive

may

help

to

blue

decrease

light

the

and

creating

longitudinal

a

blue

118

scotoma.

chromatic

aberration.

central

clear.

in

is

70

mostly

the

foveola,

fovea,

parafoveal,

and

perifoveal

areas

(the

lat-

The

ter periphery

which

ver y few S-cones in the center foveola, making the central vision

e

area

the

two

are

annular

regions)

are

described

and

delineated

on

more

turning

the

basis

of

histological

the

number

ndings,

with

consideration

given

to

of

and

rows

of

cells

in

the

nuclear

layers

(Fig.

8.21).

motion.

However,

these

the

retina.

living

CLINICAL

The

terms

and

the

cian

a

size

as

area.

name

would

refers

the

The

fundus.

to

clinician.

clinician

usually

are

not

easily

dierentiated

when

viewing

COMMENT: Terminology

used

would

areas

to

optic

describe

The

the

is

no

the

area

disc;

posterior

There

macula,

name

the

the

histologist

area

word

and

fovea.

of

is

The

the

differ

term

term

agreement

that

is

in

the

foveola

a

histologist

what

to

the

clinical

its

very

a

that

approximately

clinical

regarding

the

describe

purely

is

refers

used

to

calls

macula

fovea

term

between

fovea

histologist

coloration

another

universal

the

the

darker

clinically,

pole

macular

uses

clini-

which

one

the

and

same

center

of

this

descriptions

of

the

denition,

and

its

usage

23

varies

Fovea

e

the

from

clinician

(Fovea

shallow

fovea,

nae).

is

to

clinician.

Centralis)

depression

or

central

depression

displaced,

leaving

in

the

fovea

is

only

of

center

the

formed

of

the

retina

because

photoreceptors

the

in

macular

(fovea

retinal

the

region

centralis

neurons

center.

e

is

reti-

are

fovea

has a horizontal diameter of approximately 1.5 mm. e cur ved

wall

of

slopes

the

to

centration Fig.

8.20

Fundus

image.

The

optic

disc

(A)

and

macula

depression

the

of

oor,

the

cones

in

is

known

foveola.

the

as

the

e

retina;

clivus,

fovea

has

estimates

which

the

var y

gradually

highest

from

con-

164,000

(B) are 83,84,119

within

(D)

are

the

central

found

in

area.

the

The

vortex

peripheral

veins

retina.

(C)

and

ciliar y

ner ves

to

300,000

o

rapidly

cones

as

per

one

square

moves

millimeter.

away

from

the

e

fovea

in

number

all

falls

directions.

CHAPTER

e

cells

displaced

of

the

inner

laterally

photoreceptor

and

axons

nuclear

layer

accumulate

become

the

as

129

Retina

and

on

longer

8

ganglion

walls

they

of

cell

the

deviate

layer

fovea.

away

are

e

from

the center; these bers are called Henle bers. ey must take an

oblique course to reach the displaced bipolar and horizontal cells

(Fig.

8.24).

Henle

are

is

ber

region

layer.

clinically

e

evident

of

the

outer

retinal

with

an

plexiform

layers

OCT

and

view

the

of

layer

is

foveal

the

known

as

indentation

retina

(Fig.

fovea,

is

8.25).

Foveola

e

diameter

mately

to

0.35

0.23

of

the

mm.

mm

At

thick,

foveola,

the

compared

1

0.11

est

mm

at

the

population

ora

of

the

foveola,

with

70

0.18

e

and

of

the

retina

is

mm

at

the

foveola

e

diameters

layers

receptor

(which

ber

layer,

ally

are

present

layer,

layer

along

(3)

the

When

the

light

central

parabolic

always

in

the

cones

foveola

about

of

the

10

have

the

foveal

shape

exactly

directly

reex

formed

(Fig.

by

parabolic,

the

8.26).

the

the

and

dens-

smallest

and

clivus.

other

cell

it

cross-

(2)

outer

nuclei),

photo-

nuclear

(5)

Henle

Moving

layers

of

later-

the

retina

are

found

areas.

Reex

pinpoint

may

RPE,

(4)

processes

reects

Because

reection

cone

foveolar

Foveal

This

(1)

membrane.

the

fovea,

the:

of

Müller

foveal,

into

are

rows

fovea,

COMMENT: Central

shines

the

70

membrane,

limiting

represented.

macular,

0.13

equator

photoreceptors.

limiting

internal

sides

the

the

external

(6)

increasingly

CLINICAL

all

contains

and

throughout

of

the

contains

25

sectional

approxi-

approximately

125

serrata.

cones,

oor

the

the

vary

a

pinpoint

reection

shape

in

is

of

of

light

caused

the

sharpness

called

by

fovea

and

the

is

not

regularity

from person to person. In younger persons, the sheen from the internal limiting

Foveola

membrane

sometimes

is

seen

as

a

circular

macular

reex.

Fovea

Parafoveal

Perifoveal

Fig.

8.21

Schematic

sponding

showing

histological

area

area

regions

of

the

retina

and

corre-

architecture.

CLINICAL

The

axis

of

COMMENT: Metamorphopsia

the

photoreceptor

outer

segment

is

oriented

to

capture

incident

light

rays. If a disruption occurs so that the outer segment is no longer oriented toward

the exit pupil, vision may be altered causing a distortion of the image, called meta-

morphopsia. With macular edema (Fig. 8.27), the orientation of the photoreceptors

In this area of the retina, specialized for discrimination of detail

and

color

vision,

the

ratio

In

more

between

cone

cells

and

ganglion

is changed, and metamorphopsia can often be elicited with an Amsler grid.

cells

25

approaches

are

1:1.

sensitive

tion,

there

to

is

a

light

high

peripheral

detection

ratio

of

but

rods

areas

have

to

of

poor

ganglion

the

retina,

form

which

discrimina-

cells.

e

Within the fovea is a capillar y-free zone called the foveal avas-

cular

zone

which

70

(Fig.

varies

in

size

from

0.4

to

0.7

Parafoveal

mm

in

diameter

and

annular

Perifoveal

zone

Areas

surrounding

the

fovea

can

be

divided

into

an

inner parafoveal area and an outer perifoveal area (see Fig. 8.21).

e

parafoveal

area

contains

the

largest

accumulation

of

reti-

120–123

8.22).

e

lack

of

retinal

blood

vessels

in

this

region

nal

bipolar

and

ganglion

cells.

e

inner

nuclear

layer

can

be

70

allows

light

to

pass

unobstructed

to

the

photoreceptor

outer

segments.

12

cells

thick

maximum

and

the

density

of

ganglion

cell

layer

ganglion

cells

nine

there

cells

can

be

thick.

40,000

At

the

cells

per

78

e

are

only

cones.

elongated,

pigments

ese

are

tightly

appearing

of

segments

photoreceptors

the

packed,

rod-like

cone

causes

located

an

in

in

the

and

shape

population.

is

indentation

into

center

the

yet

outer

of

fovea

segments

containing

lengthening

the

the

of

foveolar

the

the

are

visual

outer

tissue

vit-

square

glion

thick.

revert

e

millimeter.

cell

layer

Within

to

the

width

is

the

four

the

perifoveal

cells

thick

perifoveal

usual

of

e

area,

orientation

parafoveal

and

the

seen

area

area

is

in

0.5

begins

ends

bers

the

where

of

it

Henle

outer

mm,

where

and

is

the

one

ber

plexiform

the

gan-

width

cell

layer

layer.

of

the

1,70

really

(fovea

externa,

see

Fig.

8.13)

and

decreases

the

light

path

perifoveal

area

is

1.5

mm.

70

to

the

photoreceptors.

is

rod-free

region

has

a

diameter

of

83,124

approximately 0.35 to 0.7 mm

and represents approximately

Peripheral

Retina

119

1

degree

of

displaced,

without

visual

eld.

allowing

interference

Most

light

of

to

other

of

the

reach

other

the

retinal

retinal

elements

photoreceptors

cells

(Fig.

8.23).

are

directly

Approaching

replaced

the

by

the

retinal

malformed

plexiform

layers,

peripher y,

cones,

and

the

nally,

rods

nuclear

the

disappear

layers

neural

and

merge

retina

are

with

becomes

a

CHAPTER

130

8

Retina

A

B

Fig.

8.22

Capillary

capillar y-free

single

layer

of

irregular

nonpigmented

e

the

as

RPE

ciliar y

the

are

is

body,

internal

few

blood

becomes

and

with

the

limiting

vessels

thinner

in

with

of

the

the

the

cells

ciliar y

outer

internal

peripheral

of

macular

center

that

of

of

(see

the

deep

On

as

O CT,

e

and

optical

coherence

supercial

and

the

ellipsoid

zone

are

not

visible

in

Note

the

vessels.

2 mm wide and is the site of transition from the complex, multi-

layered neural retina to the single, nonpigmented layer of ciliar y

of

ere

each

epithelium.

the

A

vitreous

ora

rm

base,

attachment

extends

between

several

the

retina

millimeters

and

vitreous,

posterior

to

the

serrata.

layer

ganglion

the

angiography.

retinal

the

cell CLINICAL

layer

(B)

5.25).

continues

body.

with

(A)

epithelium

ciliar y

scans.

region

Fig.

membrane

retina.

peripheral

the

continue

body

pigmented

limiting

membrane

more

bed

in

columnar

epithelium

continuous

zone

COMMENT: Peripheral

Retinal

Degeneration

peripheral Cystic

spaces

and

atrophied

areas

are

often

found

in

the

peripheral

retina.

126

retina.

Although

e

ora

serrata

is

the

peripheral

termination

of

the

retina

the

incidence

increases

with

Its

name

derives

processes

(see

from

Fig.

the

5.21).

scalloped

e

pattern

retina

of

extends

bays

and

further

dentate

anteriorly

the

medial

side

of

the

eye.

e

ora

serrata

is

cystic

degeneration

is

found

One cause for these changes is the poor blood

42

supply

in

ripheral

the

the

extreme

retina

affected

tine,

on

this

128

in all people over age 8 years.

127

and lies approximately 5 mm anterior to the equator of the eye.

age,

are

retinal

normal,

individual

dilated-fundus

to

47

periphery.

age-related

more

serious

Some

changes,

conditions

and

conditions,

others

affecting

might

necessitating

the

pe-

predispose

periodic,

rou-

examinations.

approximately

Optic

Disc

e optic disc, or optic ner ve head, is the site where the ganglion

cell

axons

vertically.

accumulate

e

and

horizontal

exit

the

eye.

diameter

of

diameter

is

It

the

is

slightly

disc

is

elongated

approximately

129

1.7

mm,

e

and

number

with

the

more

size

bers

the

of

of

vertical

ner ve

the

than

bers

optic

smaller

appears

ner ve

to

head;

discs.

approximately

be

positively

larger

Smaller

1.9

discs

discs

correlated

have

may

mm.

relatively

demonstrate

86

optic

ner ve

head

crowding.

Fiber

number

decreases

with

age.

e optic disc lacks all retinal elements except the ner ve ber

layer and an internal limiting membrane. It is paler than the sur-

rounding

or

lamina

the Fig.

8.23

caused

Light micrograph of the foveal region. The

by

the

absence

of

several

retinal

layers

is

retina

salmon

color

cribrosa

openings

of

because

of

the

and

the

there

optic

the

is

disc

capillar y

lamina

no

is

evident.

ner ve

bers

cribrosa

(Fig.

e

8.28).

pale

combination

network.

indentation

transparent

RPE.

a

may

In

be

orange-pink

of

some

visible

the

scleral

individuals,

through

the

CHAPTER

Internal

limiting

8

131

Retina

membrane

Nerve

fiber

Ganglion

cell

layer

layer

IPL

INL

OPL

ONL

External

limiting

membrane

Photoreceptor

layer

RPE

Choroid

Fig.

8.24

retinal

layer

Light micrograph of foveal region. Layers

pigment

(ONL),

nuclei

from

middle

epithelium

Henle

the

limiting

Internal

Outer

ber

inner

(RPE),

layer

nuclear

membrane

photoreceptor

(note

layer

within

oblique

(INL),

the

orientation

and

outer

present

layer,

internal

plexiform

in

the

external

of

bers

limiting

layer

center

limiting

at

of

heav y

membrane.

(OPL).

IPL,

the

foveal

membrane,

arrow),

Light

Inner

a

area

outer

few

arrow

plexiform

are

the

nuclear

scattered

shows

the

layer.

limiting

nuclea r

layer

External

limiting

membrane

Ellipsoid

zone

Interdigitation

zone

RPE/Bruch

complex

Fig.

8.25

visualized;

Ocular

the

coherence

foveal

tomography

indentation

is

clearly

scan

of

the

macular

area.

The

retinal

layers

can

be

evident.

Fig.

8.27

Macular

edema

associated

with

central

serous

cho-

rioretinopathy.

Fig.

8.26

Foveal

light

reex.

Fig. 8.28

Lamina cribrosa is seen in a patient with a deep cup. This

patient also has a cilioretinal artery emerging from the temporal disc.

CHAPTER

132

8

Retina

A

B

Fig.

8.29

small

Because

the

disc

V ariability

and

shallow.

contains

no

in

B,

the

normal

Normal

cup-to-disc

fundus

photoreceptor

of

cells,

the

light

left

ratios.

eye

A,

Normal

showing

a

fundus

normal

on

the

disc

physiologic

the

to

does

blind

physiologic

spot.

cup,

embr yological

not

elicit

A

a

response;

depression

varies

greatly

development

in

(Fig.

in

thus

the

size

it

represents

surface

and

of

depth,

The

disc

color

of

ratio,

during

an

COMMENT: Optic

the

and

disc,

conguration

appearance

ocular

Disc

health

of

the

and

rim

the

disc,

according

8.29).

e

outer

illary

the

depth

of

the

and

physiologic

disc

borders

cup,

are

BLOOD

cup-to-

assessed

retinal

bed.

RPE

eye.

The

cup

is

cup.

SUPPLY

layers

into

the

to

the

divides

into

a

the

into

and

nasal

e

retinal

disc,

layers.

inferior

e

retinal

choroidal

cap-

membrane

retinal

slightly

temporal

the

Bruch

central

usually

and

from

through

retina.

inner

optic

superior

further

nutrition

diuse

neural

through

branches

receive

Metabolites

nutrients

retina

Assessment

tissue

left

deep

the

vides

CLINICAL

the

inci-

RETINAL dent

of

large,

artery

artery

nasal

artery,

of

enters

center,

each

branches.

and

pro-

of

ese

the

and

which

vessels

examination.

continue to bifurcate (see Fig. 8.26). e nasal branches run a rela-

tively straight course toward the ora serrata, but the temporal ves-

Normally,

the

retina.

the

disc

When

margins

optic

ner ve

are

at

head

and

in

edema

the

is

same

present

plane

the

as

tissue

sels arch around the macular area en route to the peripheral retina.

e

retinal

swells toward the vitreous. Various types of crescents or rings are

networks,

obser ved

the

als,

the

around

disc

the

edges

optic

are

disc

margin.

emphasized

by

a

In

almost

white

rim

all

of

individu-

scleral

tis-

e

vascular

including

supercial

deep

tissue

the

vascular

vascular

is

radial

plexus,

plexus

can

divided

into

peripapillar y

and

be

the

vascular

plexus,

vascular

plexus.

deep

further

three

capillar y

dierentiated

into

a

130,131

sue,

which

separates

congurations

produce

scleral

the

in

the

the

e

ner ve

anatomic

pigmented

tissue.

optic

RPE

the

choroid.

arrangement

crescent

may

from

not

oen

seen

extend

to

at

the

outer

the

Dierent

disc

to

edge

border

the

of

visible

the

disc,

deep

lar y

and

a

middle

capillar y

capillar y

and

plexus

plexus

deep

vascular

is

is

in

capillar y

in

plexus.

the

the

e

ner ve

ganglion

plexuses

lie

ber

cell

radial

layer,

layer,

along

the

the

and

peripapil-

supercial

the

inner

middle

and

outer

132,133

and

the

areas

are

of

darkly

pigmented

choroid

hypopigmentation

common

near

the

and

might

be

evident.

hyperpigmentation

Irregular

of

the

RPE

disc.

and

the

exit

site

for

cial

that

e optic disc ser ves as the site of entr y for the central retinal

arter y

edges

the

central

retinal

vein.

the

of

the

and

inner

peripapillar y

originate

deep

which

nuclear

at

the

capillar y

radiate

layer,

plexuses

superior

plexuses

toward

an

respectively.

are

and

are

organized

inferior

organized

epicenter

that

in

e

super-

long

vessels

arcades,

as

lobular

anastomoses

whereas

vortexes

with

the

130,132–134

supercial

vascular

peripapillar y CLINICAL

Papilledema

plexus

network

is

(see

Fig.

radially

8.22).

e

arranged

around

dense

the

optic

COMMENT: Papilledema

is

edema

of

the

optic

disc

secondary

to

an

increase

in

intracra-

ner ve

head

nial pressure. As intracranial pressure increases, pressure within the meningeal

vessels

sheaths

temporal

are

and

parallels

most

dense

the

in

ner ve

the

ber

superior

layer

(Fig.

temporal

8.31).

and

ese

inferior

135

causing

at

the

around

uid

disc

to

as

the

optic

nerve

accumulate

an

elevation

slows

within

of

the

the

axoplasmic

bers.

nerve

This

head

ow

in

the

ganglion

accumulation

with

blurring

of

of

the

uid

disc

bers,

is

seen

retina

sectors,

outer

to

where

the

the

outer

ner ve

ber

plexiform

layer

layer

is

is

thickest.

avascular,

e

and

the

margins

outer

plexiform

layer

is

thought

to

receive

its

nutrients

from

(Fig. 8.30). This condition is almost always bilateral. The central retinal vein may

both

be

compromised,

with

hemorrhages

becoming

evident

in

the

nerve

ber

layer

retinal

brane the

vicinity

of

the

and

choroidal

vessels.

e

middle

limiting

mem-

in

is

usually

regarded

as

the

disc.

and

retinal

vascular

supplies.

border

between

the

choroidal

CHAPTER

Fig.

8.30

Papilledema.

Note

the

elevation

of

the

A

CLINICAL

COMMENT: Retinal

Hemorrhages

from

the

retinal

Hemorrhages

vasculature

have

a

ner ve

head

in

capillar y-free

zone

extends

vessel,

characteristic

optic

and

of

the

arrangement

of

the

nerve

ber

layer,

blood

pools

in

a

pattern

called

a

ame-shaped

hemorrhage

(Fig.

8.32A).

avascular

eyes.

0.15

zone,

mm

as

around

This

is

each

mentioned,

is

retinal

approxi-

1,23,70,120–123

0.4

to

0.7

mm

in

diameter

(see

Fig.

8.22).

e

feath-

diameter ered

foveal

133

Retina

appearance.

mately

Because

the

both

8

of

the

indica-

retinal

vein

is

larger

(50

µm)

than

the

paired

136

arter y

(32

µm),

and

the

retinal

arteries

have

a

wider

capillar y-

tive of leakage from the radial peripapillary capillaries or supercial vascular 134

free plexus.

Hemorrhages

in

the

inner

nuclear

layer,

which

originate

from

zone

compared

or

deep

capillary

plexuses,

usually

appear

rounded

and

are

called

blot

hemorrhages

(Fig.

veins.

vessels

are

said

to

be

end

vessels

because

they

do

dot

not or

the

the

Retinal middle

with

anastomose

with

any

other

system

of

blood

vessels.

Retinal

8.32B).

vessels

terminate

in

delicate

capillar y

arcades

approximately

23

1

mm

up

of

by

a

from

a

the

single

ora

layer

basement

serrata.

of

e

retinal

unfenestrated

membrane

and

an

capillaries

endothelium

interrupted

are

made

surrounded

layer

of

peri-

23,47,137

cytes.

Peric ytes

facilitate

arteries.

retinal

A

Unlike

blood

Rather,

olites

blood

ow

and

is

is

ow.

the

in

the

artery

the

is

disc

a

contractile

muscle

which

autoregulated

of

with

Smooth

regulated

nutrients

edge

cells

choroid

not

cilioretinal

temporal

are

by

is

the

based

function

surrounds

autonomically

autonomic

on

the

that

retinal

inner vated,

ner vous

concentrations

system.

of

metab-

blood.

a

vessel

but

has

that

its

enters

origin

in

the

the

retina

from

choroidal

the

vascu-

lature. Such a vessel, which nourishes the macular area, is found in

138

approximately

15%

to

20%

of

the

population

(see

Fig.

8.28).

A

cilioretinal artery can maintain the viability of the macula if block-

age

of

the

central

retinal

artery

occurs.

Smaller,

less

signicant

138

cilioretinal vessels can be found in 25% of the population.

BLOOD-RETINAL

It

is

its

important

pathway

retinal

might

eral

Fig.

8.31

ence

Peripapillary

tomography

vasculature

angiography.

as

seen

with

optical

coher -

to

that

the

barrier

impede

factors

to

choroidal

light

entering

photoreceptor

prevents

light

from

consider

choriocapillaris

into

BARRIER

is

eye

outer

components

entering

in

the

fenestrated

tissue.

the

ese

of

retinal

function

allowing

molecules

have

few

segments.

blood

tissue.

of

this

large

can

obstacles

e

plasma

ere

are

barrier :

molecules

usually

pass

in

blood-

that

sev-

(1)

to

the

exit

through

CHAPTER

134

8

Retina

A

B

Fig.

8.32

tered

Fundus

ame

orrhages

photos

shaped

present

(A)

as

from

and

seen

two

dot

in

and

different

blot

(B)

patients

with

diabetic

hemorrhages. There

are

retinopathy

often

exhibiting

multiple

types

membrane

joining

retinal

and

the

RPE

tissue;

their

easily ;

cells

and

(2)

prevent

(3)

the

endothelium

the

zonula

such

retinal

contains

occludens

molecules

capillaries

zonula

scat-

hem-

B

124,143,144

Bruch

of

from

are

moving

not

occludens

junctions

into

fenestrated,

that

prevent

cones

be

with

caused

density

age;

by

with

145

others

the

age

position

lessens

in

do

not.

is

measured,

peripheral

as

conicting

the

portions

molecules

from

exiting

retinal

vessels.

Exosomes,

small

of

the

in

may

cone

fovea,

and

there is no dierence in cone density with age at 0.9 mm from the

143

large

data

reduction

central

fovea.

145

Rod

density

declines

with

age,

but

no

decrease

146

membrane

vesicles

blood-retinal

within

barrier.

In

the

RPE

addition

to

cells,

may

help

bypass

the

is

evident

in

along

cysto-

horizontal

induced

medi-

nuclear

transportation

scotopic

cell

sensitivity.

processes

Some

lengthen

and

bipolar

extend

dendrites

into

the

147

skeletal

tracts,

cations,

such

exosomes

may

anti-VEGF

help

agents,

intravitreally

reach

the

choroid

to

inhibit

layer.

148

e

number

of

astroglial

cells

is

reduced.

e

number of nerve bers in the optic nerve decreases, and the bers

149–151

139

choroidal

and

outer

are

neovascularization.

replaced

with

connective

tissue

as

they

degenerate.

e

nerve ber, ganglion cell, and inner plexiform layers thin with age,

117,142,152–155

whereas

CLINICAL

The

the

retinal

vessel

of

blood

of

the

artery

In

within

at

such

a

Normal

vessel.

and

the

This

the

aging

Because

will

is

the

is

an

are

the

vein.

end

with

is

arterial

wall

choroid

THE

It

and

33%

is

aging

seeing

the

blood

may

as

is

layers

may

thicken

with

age.

Because

the

column

oxygenated

slightly

and

some

thicken

its

vessels

attened

process

be

disease

50%

lifetime,

ganglion

retinal

and

blood

darker.

disease

The

pro-

constrict

the

are

visible

ribbons

(Fig.

through

8.33).

RETINA

may

to

outer

nicking.

and

appear

ophthalmoscopy.

actually

blood

With

continuous

a

with

clinician

arteriovenous

IN

during

decrease,

the

vessels

estimated

lost

to

changes.

changes

visible

the

Vessels

deoxygenated

pigmented

slow,

of

lighter-colored

called

choroidal

a

the

venous

CHANGES

aging

neurons

The

hypertension,

View

readily

supercial

pathological

normal

rons

as

individuals,

retina,

to

lies

are

transparent,

whereas

crossing.

AGING

one

vessels

are

the

generally

some

the

blood

walls

artery,

cesses,

vein

COMMENT: Fundus

may

of

central

number

loss

predispose

however,

processes

the

cell

that

unclear,

where

begin.

nervous

of

especially

system

retinal

noted

neu-

in

the

140

macula.

e

macular

thickness

decreases

with

age

in

all

but

Fig.

8.33

Peripheral

fundus. The

choroidal

vessels

are

141,142

the

central

subeld.

Some

studies

report

a

decrease

in

foveal

as

lightly

colored

bands

deeper

than

the

retinal

vessels.

evident

CHAPTER

e

retinal

153

nerve

ber

layer

decreases

by

about

0.1

to

5

µm

per

5.

156–159

6.

e

number

of

retinal

pigmented

2

from

Guymer

related

decade.

2

4000/mm

to

2

epithelial

cells

is

Hudspeth

retinal

Likewise,

the

Luthert

AJ,

P ,

Bird

with

Y ee

AG.

A.

age.

e

Changes

Prog

Ret

in

Eye

intercellular

135

Retina

Bruch’s

Res.

membrane

and

1999;18(1):59.

junctional

complexes

of

reduced

160

2000/mm

R,

structures

8

pigment

epithelia.

Invest

Ophthalmol

Vis

Sci.

1973;12:354.

RPE-Bruch 7.

Fatt

I,

Shantinath

K.

Flow

conductivity

of

retina

and

its

role

in

161

membrane

complex

on

OCT

thins

0.1

µm/year

with

age. retinal

Other

changes

in

the

RPE

layer

include

attenuation,

adhesion.

Exp

Eye

Res.

1971;12:218.

MF .

Systemic

pleomor8.

Kita

M,

Marmor

mannitol

increases

the

retinal

99

phism,

atrophy,

loss

of

melanin,

and

increase

in

lipofuscin. adhesive

Lipofuscin

accumulates

linked

decrease

throughout

life

in

the

RPE

and

may

a

in

the

2

metabolically

active

Peripapillar y

temporal

lysosomal

160

162

of

enzymes

in

the

is

an

age-related

usually

evident

degeneration

as

of

a

pale,

RPE

Marmor

11.

Kita

With

and

the

age,

there

vertical

is

optic

a

decrease

cup

in

diameter

of

the

optic

cup

both

increase.

ese

factors

when

assessing

the

optic

ner ve

head

for

need

to

cells

become

hypertrophic

with

Vis

Foulds

processes,

such

as

Sci.

reticular

degeneration,

become

narrower,

which

may

on

in

Sci.

of

uid

1980;19:893.

retinal

the

eect

subretinal

adhesive

subretinal

force

space.

in

vivo

Invest

of

Ophthal-

e

vitreous

in

retinal

detachment.

Trans

Ophthalmol

glaucoma. DeGuillebon

H,

Zanberman

H.

Experimental

retinal

detach-

150

stone

biophysical

peripheral

diminish

aspects

of

retinal

peeling

and

stretching.

Arch

degeneration,

cystoid

degen-

14.

eration, are probably linked to a decrease in blood supply. Retinal

vessels

Eects

agents

Vis

e

and

age.

paving

and

MF .

active

DS.

1975;95:412.

Ophthalmol.

peripheral

Ophthalmol

Cohen

adhesion

1992;33:1883.

WS.

UK.

ment:

Degenerative

Marmor

AS,

retinal

be

13. 149

Müller

Invest

on

the

Soc

considered

1991;109:1449.

neuro-

and

12.

area

M,

Abdul-Rahim

inhibitors

resorption.

and

mol

tissue,

FM,

metabolically

circulation.

rim

Ophthalmol.

Y ao XY , Moore KT , Marmor MF . Systemic mannitol increases retinal

metabolic

164

retinal

Arch

adhesiveness measured in vitro. Arch Ophthalmol. 1991;109:275.

10.

atrophy,

Bruch membrane, and may be caused by attenuation of the peri-

papillar y

vivo.

163

RPE.

chorioretinal

crescent,

activity

in

be 9.

to

force

blood

ow.

Hollyeld

to

15.

the

JG,

Varner

pigment

Hageman

tor

1972;87:545.

GS,

matrix

HH,

Rayborn

epithelium.

Marmor

mediates

Retina.

MF ,

Y ao

primate

ME,

etal.

Retinal

attachment

1989;9:59.

XY ,

retinal

etal.

e

interphotorecep-

adhesion.

Arch

Ophthalmol.

1995;113(5):655. CLINICAL

COMMENT: Visible

Retinal

Changes

16. Aging

changes

in

the

retina

may

be

clinically

observable.

The

foveal

Hollyeld

within dims

because

the

internal

limiting

membrane

thickens.

The

fundus

color

JG,

the

RPE

vessels

melanin

more

and

choroidal

prominent

and

pigmentation

giving

the

are

fundus

a

lost,

tigroid

making

the

(striped)

appearance.

of

the

The

accumulation

choroid

but

are

of

debris

observed

as

in

drusen

pinpoint

are

located

deposits

in

in

the

Eye.

Marmor

variation

to

the

retinal

MF ,

Y ao

XY ,

Hageman

human

eyes.

GS.

Retinal

Retina.

adhesiveness

in

surgi-

1994;14(2):181.

Bruch

Lazarus

HS,

Hageman

GS.

Xyloside-induced

disruption

of

inter-

retina.

Invest

19. COMMENT: Alzheimer

fovea

1990;4:333.

enucleated

photoreceptor

CLINICAL

Regional

from

tessel-

18. membrane

ME.

matrix

choroi-

or

cally lated

Rayborn

fades

17. dal

HH,

interphotoreceptor

peripher y. because

Varner

reex

matrix

Ophthalmol

proteoglycans

Vis

Sci.

results

in

retinal

detachment.

1992;33:364.

Picaud S. Retinal Biochemistry. In: Kaufman PL, Alm A, eds. Adler’ s

Disease

Physiology of the Eye. 10th ed. St Louis: Mosby; 2003:382e–408. Early

changes

in

the

retina

might

be

diagnostic

in

patients

with

Alzheimer

20. disease.

Because

the

nerve

ber

layer

is

a

tract

of

the

brain,

loss

of

brain

Sigleman

J.

Ozanics.

because

of

neurodegenerative

disease

may

result

in

thinning

of

the

layer.

Alzheimer

disease

is

correlated

165

and

macular

nerve

ber

layer

with

a

reduction

in

nerve

ber

layer

and

the

Some

level

of

have

found

cognitive

a

atrophy.

plaques

may

be

seen

in

the

outer

human

retinal

layers

An

cells

extensive

loss

of

neurons

throughout

the

retina,

particularly

glial

cells,

has

been

histologically

documented

patients

with

Alzheimer

disease.

increased

in

rim

tissue

have

also

been

observed

in

these

Anatomy,

Row ;

ME,

Landers

RA,

etal.

Insoluble

1982:441.

interpho-

matrix

domains

Exp

Eye

surround

Res.

rod

photoreceptors

in

the

1990;51:107.

Mieziewska

K.

Res

e

interphotoreceptor

Tech.

matrix,

a

space

in

sight.

1996;35(6):463.

Fine

BS,

Y ano.

e

retina.

In:

Fine

BS,

Y ano

M,

eds.

Ocular

specimens

cup-to-disc

ratio

2nd

ed.

Hagerstown,

MD:

Harper

&

Row ;

1979:59.

and

24.

171

decreased

Rayborn

retina.

Histolog y. An

&

gan-

23. and

170

from

JG,

Microscop

glion

ed. Ocular

Harper

on

169

OCT.

FA,

and

22. Amyloid

Jakobiec

Philadelphia:

correlation

impairment

168

cortical

Hollyeld

toreceptor

166

thickness.

loss

In:

T eratology.

peripapillary

167

between

and

nerve

21. ber

Retina.

tis-

Embryology, sue

Fine

BS,

Zimmerman

LE.

Obser vations

of

the

rod

and

cone

layer

patients.

of

the

retina.

thalmol

25.

Cohen

Vis

AI:

A

light

Sci.

e

and

electron

microscopic

study.

Invest

Oph-

1963;2:446.

Retina.

In:

Hart

MJ

Jr,

ed.

Adler’s

Physiolog y

of

the

REFERENCES Eye.

26. 1.

Hogan

MJ,

Alvarado

JA.

Retina.

In:

Hogan

MJ,

Alvarado

Laties

JE,

eds.

Histolog y

of

the

Human

Eye.

A,

Sharma

RK,

Ehinger

BEJ.

Development

and

structure

of

In:

ed.

Laties

A,

Kaufman

St

Louis:

PL,

Alm

Mosby ;

eye.

Campbell

Nature.

C.

Photoreceptor

orientation

in

1968;218:172.

Enoch

J.

An

A,

eds.

Adler’s

Physiolog y

Feeney-Burns

L,

relationship

analysis

of

of

retinal

neighboring

receptor

orientation.

photoreceptors.

Invest

I.

Oph-

of

the

Vis

Sci.

1971;10:69.

Eye.

Y oung

RW ,

B ok

D.

Participation

of

the

retinal

pigment

epi-

2003:319.

thelium 3.

1992:579.

the

28. 10th

P ,

Mosby ;

1971:393–522.

thalmol retina.

Louis:

Liebman

primate

Angular 2.

St

Philadelphia:

27. Saunders;

ed.

JA,

the Weddell

9th

Hilderbrand

ES,

Eldridge

S.

Aging

human

in

the

rod

outer

segment

renewal

process.

J

Cell

Biol.

RPE:

1969;42:392. morphometric

analysis

of

macular,

equatorial,

and

peripheral

29. cells.

Invest

Ophthalmol

Vis

Sci.

Y oung

RW .

monkey. 4.

Weiter

JJ,

Delori

FC,

Wing

GL,

etal.

Retinal

pigment

and

melanin

and

choroidal

melanin

in

human

Ophthalmol

Vis

Sci.

1986;27:145.

Cell

renewal

Biol.

of

rod

and

cone

outer

segments

in

rhesus

1971;49:303.

Y oung

RW .

e

renewal

eyes.

J Invest

J

epithelial

30. lipofuscin

e

1984;25:195.

Cell

Biol.

1967;33:61.

of

the

photoreceptor

cell

outer

segments.

CHAPTER

136

31.

Bok

D.

Invest

32.

33.

Retinal

Y oung

RW .

rhesus

monkey.

LaVail

MM.

Y oung

and

to

cone

e

Anderson

Sci.

of

outer

discs

DH,

Sci.

rod

Res.

interactions.

55.

of

outer

segments

shedding

in

the

56.

in

and

the

in

rat

retina:

rela-

Fisher

SK,

57.

degradation

chick

retina.

of

rod

Invest

58.

RH.

renewal.

Mammalian

Invest

cones:

Ophthalmol

Vis

disc

59.

Sci.

37.

Steinberg

R.

38.

cones.

O’Day

WT,

Raviola

ized

39.

E,

Nature.

Y oung

by

in

study

Euler

Haverkamp

T,

in

of

human

60.

in

the

daily

S,

and

T,

blocks

J

Cell

of

of

Biol.

Nat

segment

1978;76:593.

of

Quinn

of

N,

a

H,

t he

Golgi

42.

Park

of

of

43.

L,

F ly n n

E,

p e r iph e r a l

1975;65:192.

the

46.

In:

SL.

e t  a l.

re t i n a .

The

P ro g

P .

bipolar

Rev

63.

Neurosci.

cl i n i c a l

re l e v an c e

R et

R es .

Ey e

R.

Eye

H,

human

and

retina:

a

Majander

glion

cell

inferred

Invest

50.

A,

J

João

loss

in

from

C,

Timucin

OB,

assessment

phrenia

temporal,

Vis

Mutlu

of

EA,

healthy

biolog y

Foundations

Lippincott;

and

cone

the

of

67.

1994.

processing

68.

synapses

retina.

Clinical

In:

Press;

in

etal.

W ol ’s

Saunders;

cells

of

the

Anatomy

1976:99–180.

parafovea

and

serial

of

e

pattern

of

71.

the

section

chromatic

optic

sensitivity

D,

pathway

controls.

etal.

in

Katz

BJ,

Digre

photophobia.

52.

Benarroch

Res:

with

Surv

projections,

e

Diagnosis,

pathophysiolog y,

72.

gan-

73.

atrophy

losses.

Ophthalmol.

melanopsin

74.

schizo-

75.

functions,

and

clinical

of

76.

Obara

EA,

expressing

patients.

54.

retinal

Invest

Hannibal

pressing

Hannibal

J,

ganglion

Ophthalmol

Christiansen

human

intraretinal

Heegaard

retinal

cells

Vis

AT,

J

in

Sci.

etal.

Loss

severely

Neurolog y.

77.

of

melanopsin-

staged

cells:

Comparat

S,

etal.

glaucoma

Melanopsin

subtypes,

Neurol.

in

the

circadian

ONE.

WM

Jr,

rhythm

2013;8:e62841.

ed.

Adler’s

Physiolog y

1992:523.

e

organization

of

the

verte-

2011Webvision.med.utah.edu/.

etal.

in

the

Chromatic

human

connectivity

retina.

Invest

of

the

Ophthalmol

Ripps.

of

Eye.

JH.

the

Intrinsic

cell.

Vis

Structural

Müller

E,

Kuwabara

Trend

T,

Structure

Press;

A.

D.

retina:

neurocircuitr y

and

functional

circuitr y

2012;29:51–60.

of

and

retinal

glia.

Function.

In:

New

Sarthy

V ,

Y ork:

2001.

e

Neurosc.

Cogan

properties

Neurosci.

organization

cell:

Reichenback

retina.

mammalian

1997;11:904.

Müller

cell:

a

functional

element

1996;19(8):307.

Retinal

glycogen.

Arch

Ophthalmol.

Newman

EA.

Neurosci.

1985;5:2225.

Reichenbach

Membrane

A,

Müller

Stolzenburg

(glial)

Neuroanat.

Kumar

A,

Pandey

a

cells

JU,

do

of

retina

Eberhardt

for

their

glial

W ,

(Müller)

etal.

neuronal

What

“small

cell.

J

do

siblings” .

J

1993;6(4):201.

RK,

Miller

perspective

Immunol.

Br ingmann

physiolog y

on

LJ,

etal.

their

Muller

roles

in

glia

in

retinal

endophthalmitis.

innate

Crit

2013;33:119–135.

A,

Syrb e

f unc tion

S,

G ör ner

and

K,

etal.

de velopment.

e

Prog

pr imate

Ret

Eye

fove a:

Res.

2018;

Kirschfeld

Ogden

K.

Invest

TE.

Do

Müller

cells

Ophthalmol

Ner ve

contents.

Vis

ber

Res.

Vis

layer

act

Sci.

of

as

optical

bers

in

the

primate

2019;60:345–348.

the

primate

retina:

thickness

and

1983;23:581.

LaCour M. e retinal pigment epithelium. In: Kaufman PL, Alm A,

Panda-Jonas

eyes.

Zinn

S,

cell

KM,

Hoon

Am

of

J

JB,

Jakobczyk-Zmija

distribution,

Ophthalmol.

ed.

Ocular

Harper

Okawa

the

H,

retina:

&

and

J.

Retinal

Anatomy,

Row ;

Della

M.

Retinal

correlations

in

pigment

normal

hu-

1996;121:181.

Benjamin-Henkind

FA,

M,

Jonas

count,

pigment

Embryolog y,

epithelium.

and

In:

Teratolog y.

1982:533.

Santina

development

L,

and

etal.

Functional

disease.

Prog

Ret

architec-

Eye

Res.

Usui

S,

Kamiyama

78.

la

Cour

the

ex-

distribution,

cell

Y ,

Ishii

responses

H,

by

etal.

the

Reconstruction

ionic

current

of

model.

retinal

Vis

Res.

1996;36(12):1711(Abstract).

2016;57:4661–4667.

Heegaard

ganglion

connectivity.

S,

cells

amacrine

horizontal

J,

with

2014;42:44–84.

2011;76:1422–1427.

53.

the

ture

phototransduction,

implications.

SK,

types

Academic/Plenum

Jakobiec

2016;61:466–477.

system:

R.

(website)

of

patients

2011.

roles.

Retinal

Newman

man

treatment

Nelson

in

2012;29:911–919.

PLoS

Hart

Mosby ;

Alterations

eds. Adler’ s Physiology of the Eye. 10th ed. St Louis: Mosby; 2003:348.

Neuroimaging.

and

In:

etal.

Glaucoma

2008;3:e3931.

parameters

Changes

glaucoma.

Fisher

cell

Singer

Philadelphia:

KB.

EE.

V .

e

epithelial

patients

22,

P ,

Amacrine

JB,

retina.

Psychophysical

Psychiatr y

etal.

Intl.

etal.

1989;30(suppl):348.

AII

Sarthy

glial

retinal

dominant

E,

H,

sleep

C,

ONE.

66:49–84.

2017;58:502–516.

Timucin

the

Rev

70.

1991;303(4):617.

autosomal

and

March

immunity :

W ,

Ophthalmolog y,

ed. Eugene

J,

Louis:

Webvision

Ahuelt

str uc ture,

R,

St

Fernandez

H.

Chem

1941.

Tasman

and

Adaptation.

ed.

functional

retinal

69.

University

Fontana

Chronobiol

Ding

PLoS

1961;66:680.

2001;20(3):351.

microscopy

Neurol.

spatial,

Sci.

cell

and

Sci.

Demb

of

1994.

electron

koniocellular

versus

of

ganglion

AT,

A

1991;7(1-2):49.

Philadelphia:

Rider

Duane’s

cells

ed.

by

retina:

9th

N,

rhythm

primar y

horizontal

Kluwer

2017;266:27–34.

51.

Visual

retina.

H,

Kolb

ed.

66.

and

pathways

Res.

W arwick

OPA1-related

Ophthalmol

eds.

In:

Comparat

human

anatomy

Chicago

anatomy

Midget

study

reconstructions.

49.

7th

L.

Eye

Foundations

Lippincott;

Orbit.

EA,

bipolar

Neurosci.

eyeball.

Dekor ver

e

vision:

Ret

Cone

the

Philadelphia:

Rod

Chicago:

Duane’s

e

1.

Prog

of

Y ,

with

Chiquet

Grimes WN. Amacrine cell-mediated input to bipolar cells: varia-

of

1992;318(2):147.

ES.

Jaeger

vol

RF .

JM.

Functional

Philadelphia:

the

W ,

retina.

Vis

Neurons

Neurol.

Dacheux

Retina.

eds.

EA,

SK.

Gragoudas

Tasman

retina.

e

Witkorsky

Kolb

J,

Hopkins

Jaeger

of

48.

Comparat

SA,

BB,

W arwick

Fisher

Ophthalmolog y,

primate

Polyak

1.

KA,

mammalian

Boycott

vol

47.

J

retina.

the

Zhang

Eye.

H,

Kolb

and

65.

Sigelman

Clinical

the

45.

study.

SS,

Bloomeld

in

44.

Linberg

62.

64.

Csincsi k

v i su a l i s i ng

Kolb

Kolb

Zavalía

activity

O,

system.

tions on a common mechanistic theme. Vis Neurosci. 2012;29:41–49.

freeze-

2019;68:83–109.

41.

M.

the

Vis

61.

special-

retina:

Retinal

vision.

outer

Biol.

the

Cell

etal.

of

J

organization

layer

rabbits.

Schubert

building

shedding

goldsh.

2014;15:507–519.

40.

Hart

three

plexiform

monkey

elementar y

epithelium

Intramembrane

outer

fracture

pigment

Rhythmic

cells

NB.

the

by

1974;25:305.

RW .

visual

Gilula

contacts

cells:

H,

de

timing

glaucoma.

Accessed

Phagocytosis

retinal

membranes

MF ,

patients

brate

1978;17:117.

36.

Wang

in

of

Steinberg

and

Lanzani

Dkhissi-Benyahya

circadian

advanced

1976;17:105.

phagocytosis,

E,

the

locomotor

1976;194:1071.

shedding

membranes

Drouyer

alters

1971;34:190.

disk

Science.

rhythm

segment

Vis

from

segment

lighting.

daily

epithelium

1985;26:1659.

Ultrastructure

cyclic

outer

shedding,

J

Rod

Ophthalmol

35.

Vis

Shedding

RW .

Retina

photoreceptor-pigment

Ophthalmol

tionship

34.

8

and

2017;525:1934–1961.

79.

Eye.

M,

Dow ling

ina:

Ehinger

B.

Amsterdam,

JE,

elec tron

1966;166:80.

e

e

B oycott

retina.

In:

Fischbarg

Netherlands:

BB.

Organization

micros copy.

Proc

Royal

J,

Elsevier;

of

S oc

t he

ed.

e

Biology

2006:195–252.

pr imate

London

Biol

ret-

S ci.

of

CHAPTER

80.

Jonnal

of

the

ages.

81.

Litts

RS,

Kocaoglu

outer

Invest

KM,

raphy

retinal

Ophthalmol

Zhang

and

Farber

of

DB,

Invest

Curcio

CA,

Wells-Gray

cone

human

copy.

85.

Oppel

EM,

Stuttgart,

86.

Jonas

JB,

retinal

Invest

87.

la

la

In:

M,

Cour

J,

M,

ed.

Strauss

O.

Physiol

Rev.

mol.

91.

RW .

D.

J

Martini

I,

JL.

Y ano

M,

Marks

single

Kolb

Puller

rod

in

laser

retinaganglien

of

GO.

the

and

disc,

correlations

of

E,

pigment

the

Eye:

und

Eye,

etal.

in

rods

and

and

S-cones.

Twig

G,

the

K,

Parish

CA.

cones.

light-induced

P ,

of

damage

Ophthalmol

pigment

Ann

Vis

Sci.

epithelium:

a

retinal

P ,

etal.

retinal

R,

Sci.

Ogden

TE,

Development,

etal.

Modulation

of

JS,

Dobelle

eds.

Cultures

of

extracellular

matrix.

present,

ocular

Patholog y

architecture

N,

(e-book).

St

an

Haverkamp

118.

and

blue

Levy

103.

Arshavsky

J,

Jr.

Visual

Louis:

pigments

functional

etal.

Sci.

Age-related

circuits

in

immunohistochemical

study.

S,

in

J

cone

H,

How

retina.

retina

Like

etal.

I.

are

PLoS

Ret

works.

and

enriched

Eye

day :

Res.

Sci.

for

121.

R app

cones

2002;36:1–3.

mini

122.

A,

eds.

LM,

T,

of

etal.

e

feedback

e

feedback

review

with

a

the

mamma-

involvement

from

of

horizontal

pathway

look

neurocircuitr y

A,

Gouras

New

P ,

from

ahead.

of

eds.

Y ork:

of

dopamine

eld

hori-

Vis

Res.

amacrine

cells

Neurocircuitry

Elsevier

and

properties

Press;

its

of

agonists

ganglion

and

cells

in

1986;17:837–855.

Ultrastructure

Invest

JJ,

yellow

R,

in

SS,

of

the

Ophthalmol

Y-H,

in

etal.

interplexiform

Vis

Retina

natural

responses

In:

Sci.

is

scenes.

10th

E,

and

Kaufman

ed.

Alm

St

PL,

Louis:

A.

1983;24

structured

Proc

of

synaptic

Alm

A,

Mosby ;

Ocular

Physiolog y

retina.

Pruett

Mathew

inner

Choi

JH.

segment

pigment.

Natl

to

Acad

organization

eds.

circulation.

the

Eye.

Adler’s

2003:422–438.

10th

In:

ed.

Kaufman

St

Louis:

R,

and

Invest

RC,

rst

Pearce

E,

FC.

200

zeaxanthin

from

Age,

and

coherence

Sci.

and

Mac-

1981;1(14):296.

and

choroidal

pe-

2000;41:1200.

perspectives.

Retina.

sex,

concentra-

perifoveal

Vis

Historic

years.

etal.

retinal

optical

and

Ophthalmol

Delori

e

outer

Lutein

membranes

ethnic

thickness

tomography.

Am

J

varia-

on

Ophthal-

2015;160:1034–1043.e1.

Chen

Y ,

Lan

to

Res.

W ,

the

Schaeel

shape

PK.

e

M,

F .

the

Size

of

foveal

photoreceptor

Falavarjani

comparison

the

pit

foveal

but

not

blue

to

scotoma

macular

pigment.

in

of

KG,

mosaic.

Tepelus

swept-source

healthy

eyes.

and

Eye.

TC,

1998;12:531.

etal.

Quantita-

spectral-domain

Ophthalmic

Surg

Lasers

OCT

Imag

2017;48:385–391.

Fujiwara

A,

Morizane

avascular

zone

optical

Y ,

in

Hosokawa

healthy

coherence

M,

eyes:

etal.

an

Factors

aecting

examination

tomography

using

angiography.

PLoS

2017;12:e0188572.

Schwartz

Wang

of

2015;106:81–89.

R,

Q,

Bagchi

zone

Y uodelis

analysis

C,

of

A,

Dubis

dimensions

Surg

Chan

angiography.

124.

light

Adler’s

human

Nussbaum

Baq

Kao

darkness

Eye.

outer

Lasers

S,

choriocapillaris

cells

BG,

of

Maple

rod

Ophthalmic

123.

dierent

SK.

retina.

retina.

the

swept-source

primate

have

mammalian

2003:747–784.

in

foveal

2003;22:31–68.

and

Neuron.

Fisher

excess

GA,

Alm

avascular

2003;91:28–35.

rods

the

2005;147:219–229.

H.

Neuroscience.

Grandtam

tive

cho-

horizontal

Res.

Eects

Gio

Retina.

2014;9:e88963.

in

Res.

2010;107:17368–17373.

Al-Sheikh

horizontal

beneath

in

architecture

negative

Memorial.

Intracellular

Ahnelt

Histochem

elements

HII

opponency

Am

pathways.

Synaptic

between

ONE.

Color

Prog

night

regeneration

cells

ed.

Perlman

the

VY .

bipolar

SCF ,

M,

signaling

in

receptive

Borghuis

an

120.

the

the

NW .

the

vertebrate

ONE.

Neitz

novel

Eye

1999;40:1313–1327.

Sjoerdsma

Gallego

Cajal

human

119.

of

1994;35(5):2385.

changes

A

on

angiography

neural

Vis

Sci.

Functional

In:

of

Vis

In:

1964;43:1181.

Ophthalmol

feed-for ward

Neuhauss

Kolb

pigment

Arora

of

EF

R.

spectral-domain

Invest

disorders.

A

Physiolog y

tions

retinal

2017;65:567–577.

vertebrate

H.

Invest

junction:

MacNichol

Science.

the

related

selected

J,

Brain

cones.

retina.

CP ,

SM.

ular

Eye.

human

to

KA,

USA.

Wu

mol.

past,

A

Exp

1991;71:447–480.

Spekreijse

Daw

the

Ratli

tions

116.

repair

epithelium.

barriers:

Ocular

WH,

cones.

retina.

115.

in

1997;93:149.

of

of

Mosby ;

pigmented

1992;33(3):516.

blood-ocular

genetics

Linberg

PL,

uorophore

117.

e

Saini

102.

113.

Ophthal-

partner

RJ,

ripheral

pigment

etal.

retina.

processing

Vis

channels

Prog

M,

Retina.

process

Invest

2000;41:1981–1989.

versatile

AL,

(suppl):259.

112.

in

function.

lipofuscin

to

Hatch

Functional

Rev.

Klooster

retina.

rabbit

cell

1993;17:189.

Hogg

the

e

I,

Nelson

cat

the

the

eyes.

2006:253–271.

visual

Parallel

BB.

Physiol

cells

Jensen

of

in

Boycott

antagonists

In:

epithelium.

H.

Ophthalmol

cones.

H,

the

Sci

epithelium

ET,

cone-dominated

1985:215–232.

neuro-

normal

transport

pigment

H,

to

Kolb

of

2.

111.

Lactate

retinal

pigment

Ophthalmol.

e

C,

109.

op-

vol

and

epithelium.

Elsevier ;

the

1999;39:2449–2468.

healthy

ophthalmos-

cup,

in

in

Wässle

Kamermans

zontal

110.

Optic

B,

Fahrenfort

in

Structure

cycle

retina.

cells

and

1988;29:1151.

fetal

Supple.

Duker

GABAergic

cells

Vis

primate

T,

107.

114.

Molecular

WB,

H.

Gupta

of

Sci

JG.

Cytochem.

101.

in

2008.

rioretinal

100.

human

1965:97.

systems

Invest

Pandey

vertebrate

99.

the

108.

mid-peripher y

die

e

Villazana-Espinoza

Invest

Wässle

lian

1994;35:434–442.

epithelium.

Wiggs

Mosby ;

98.

blue

Hiscott

Doc

106.

patterns

2):255.

B,

Cunha-Va

future.

97.

Sci.

retinal

Ophthalmol

96.

über

retinal

Kenyon

human

regeneration

pigment

95.

Sci.

Nakanishi

Cell

1994;8(pt

94.

in

Boycott

retina.

photoreceptor

Variation

scanning

A,

visual

glutamate-gated

Human

etal.

optics

ed.

Biolog y

retinal

cells.

e

Grierson

and

JW ,

e

Renewal

mediates

vision.

93.

2018;38:445–461.

Distribution

105.

support

2005;85:845–881.

JR,

epithelial

Bok

tomog-

1973:843–854.

Sparrow

A2E

92.

H,

Vis

e

etal.

A,

Naumann

Vis

T.

e

Lin

coherence

nucleotides

Muniz

cone

137

Retina

2007;83:175–184.

1990;292:497.

the

conguration

Tezel

isolated

Y oung

adaptive

Verlag;

GC,

Ophthalmol

Cour

to

104.

im-

2016;30:1135–1143.

Rohen

size,

Ophthalmol

90.

using

fovea

origins

1985;26:1558.

RE,

Bries

cellular

tomography

degeneration

Retina.

etal.

cyclic

Sci.

Neurol.

SS,

e

Optical

macular

RN,

and

Kalina

the

Germany :

rim

freshly

89.

from

Gusek

Fischbarg

88.

KR,

etal.

sources.

Vis

etal.

coherence

2014;55:7904–7918.

Lolley

Untersuchungen

tikusfasern.

Sci.

KB,

protein,

RJ,

optical

age-related

JG,

Choi

(Lond).

O.

of

Comparat

retinas

Eye

Vis

Ophthalmol

J

density

in

reectivity

Sloan

topography.

84.

as

Zawadzki

Freund

Flanner y

photoreceptors,

retina.

83.

Y ,

histology

mitochondria

82.

OP ,

bands

8

Y ang

as

Am

J

Imag

JY ,

human

1986;26:847–855.

by

fovea

A

Normative

macular

Retina.

Ophthalmol.

A.

etal.

four

etal.

measured

Hendrickson

the

A,

in

data

vascular

on

foveal

layers.

2018;49:580–586.

Vascular

optical

density

in

coherence

retina

2016;168:95–109.

qualitative

during

and

quantitative

development.

and

tomography

Vis

Res.

CHAPTER

138

125.

Scheibe

P ,

Zocher

acteristics

Eye

126.

Res.

Mori

MT,

their

Retina

Francke

M,

asymmetries

etal.

in

Analysis

the

normal

of

foveal

char-

population.

144.

Exp

Kanno

described

by

J,

wide-eld

PL.

Retinochoroidal

montage

tomography.

imaging

Retina

of

morpholog y

spectral

145.

domain

(Philadelphia,

Pei

TF ,

Smelser

serrata

region

Some

primate

ne

structural

eyes.

Invest

features

Ophthalmol

Pa).

of

the

Vis

146.

ora

147.

Sci.

O’Malley

retina.

Jonas

Allen

Incidence

JB,

ner ve

RA.

and

Peripheral

distribution

cystoid

in

degeneration

1,000

autopsy

of

eyes.

the

148.

Arch

Nesper

count

PL,

anatomy

AM,

and

Fawzi

and

tomography

Müller-B ergh

optic

disc

size.

JA,

etal.

Invest

Human

optic

Ophthalmol

Vis

149.

Sci.

AA.

Human

connectivity

angiography.

parafoveal

revealed

Invest

by

capillar y

optical

Ophthalmol

vascular

150.

coherence

Spaide

RF ,

Vis

Sci.

Campbell

anatomy

of

133.

Muraoka

layered

ence

134.

Zhang

the

Y ,

human

Uji

retinal

A,

B onnin

S,

ence

Waheed

retina

V ,

Sci.

M,

etal.

Eye

TS,

by

Optical

Res.

etal.

coherence

etal.

Sci

Rep.

the

optical

Mansoori

radial

using

of

the

optical

four-

coher-

microcirculation

An

T,

A,

etal.

New

imaged

angiography.

peripapillar y

raphy

J,

by

Retina

Gamalapati

capillar y

density

insight

optical

JS,

etal.

the

into

the

155.

coher-

Pa).

normal

human

J

of

between

matched

Heisler

optical

M,

etal.

coherence

histolog y

in

the

retina

Cogan

DG,

Ophthalmol.

138.

Hayreh

supply

139.

Aboul

SS.

of

Res.

140.

Gao

tial

e

tomography

eye.

Exp

angiog-

H,

of

Hashemi

SH,

H,

Vis

cell

in

of

Brit

M,

of

etal.

J

Eye

perspective.

the

retina:

Its

Ophthalmol.

Chitadze

G,

Res.

role

in

Arch

in

the

blood

159.

Epidemiol.

Normative

H,

ceptor

M,

using

Sci.

human

retina.

epithelial

Cordle

normal

EP ,

in

etal.

LM.

ageing

Aging

Cellular

aging.

M,

Y ekta

A,

etal.

in

a

cell.

e

Exp

Eye

160.

161.

Invest

for

separate

domain

PLoS

Zhong

Z,

with

optical

distribution

of

ONE.

etal.

and

age-related

and

scotopic

Invest

reorganization

Ophthalmol

in

Vis

the

Sci.

inner

retinal

layers

164.

tomography

eccentricity

2011;52:7376–7384.

cone

and

eects

Ophthal

of

A,

of

etal.

Res.

B,

etal.

aging

Changes

of

astrocytes

degeneration.

Exp

Eye

Mitochondria

and

of

of

retina

application

of

free

2000;32:229.

Schnurbusch

calcium

Alasil

M,

and

Z,

U,

etal.

Age-

channel-mediated

and

currents

in

H,

Vis

Eye

Res.

L,

SM.

N.

Eects

structures

Aging

of

the

optic

of

on

sex

and

optical

age

on

the

coherence

2015;40:213–225.

etal.

Study

Y ,

Drance

etal.

Retinal

2011.

PLoS

Age-related

microcirculation,

Sci.

SE,

and

choroidal

Eye

Shi

AQ,

1980;98:2053.

Y oshimura

Zhao

Beijing

T,

ner ve

ber

ONE.

alterations

and

layer

thick-

2013;8:e66763.

in

the

microstructure.

retinal

Invest

2017;58:3804–3817.

Park

Y-H.

volume

Wang

ner ve

Chen

Invest

ber

K,

in

Eect

normal

Keane

layer

domain

C-Y ,

age,

PA,

of

age

eyes.

etal.

thickness

optical

Huang

axial

normal

Taiwan.

Khawaja

by

and

sex

Medicine

Analysis

age,

coherence

Y oo

PLoS

retinal

ner ve

KP ,

on

retinal

layer

(Baltimore).

sex,

of

normal

and

race

tomography.

J

reti-

using

Glaucoma.

SH,

Africans.

Adamis

AP .

Ko

PJ,

Foster

UK

e

relationship

ber

Taiwan:

e

layer

be-

thickness

Chiayi

eye

in

study

measures

Vis

OA.

Sci.

African

Retinal

etal.

the

Associations

EPIC-Norfolk

Eye

2013;54:5028–5034.

Retinal

with

DF ,

in

ner ve

ocular

Health

bre

and

Sci.

layer

systemic

thickness

val-

parameters

in

2016;16:1188–1194.

manifestations

of

aging.

Intl

1998;38(1):95.

Strouthidis

epithelium

the

in

etal.

ner ve

Gar way-Heath

layer

associations

Clin.

F ,

ber

Oduntan

Ophthalmol

C-N,

retinal

2018;13:e0194116.

MPY ,

Ophthalmol

their

South

Kuo

and

population

ONE.

Chan

Invest

and

EJ-C,

length

elderly

AP ,

Mashige

NG,

thickness

biobank.

etal.

Associations

measures

Ophthalmolog y.

in

a

large

with

retinal

cohort:

results

2017;124:105–117.

Boulton M, Dayhaw-Barker P . e role of the retinal pigment epithe-

Sparrow

JR,

Curcio

CA,

rioretinal

tor

photore-

age.

McCormick

Curr

Boulton

pathobiolog y.

2017;12:e0180450.

of

JJ,

macular

lium: topographical variation and ageing changes. Eye. 2001;15:384.

163.

Variation

retinal

162.

population.

Cifuentes-Canorea

coherence

Salazar

Germer

changes

Pan

Kim

pigment

2017;24:323–331.

JM,

U,

the

Ophthalmol.

Jiang

JY ,

Black

Dieren-

cells.

healthy

AI,

age-related

Biedermann

Hangai

YX,

Y ,

from

determinants

database

density

Vis

the

pigment

Martínez-de-la-Casa

spectral

T YP ,

packing

Ophthalmol

its

population.

Chui

of

CL,

retinal

e

Won

ues

1992;33:1–17.

and

Wei

with

Intracellular

RPE

cells:

A,

Arch

S,

Wang

in

1963;47:651.

etal.

bevacizumab

retinal

Khabazkhoob

Caucasian

Song

Aging

and

Ooto

Study.

uptake

JG.

Sci.

thickness

thickness

in

Dithmer

neurons

Nieves-Moreno

P ,

mural

arter y

ner ve.

following

Ophthalmol

143.

central

optic

Hollyeld

loss

macular

142.

e

Dohlman

the

2015;131:29–41.

Ophthalmol

141.

T.

Bringmann

tween

1967;78:133.

the

Naga

pathways

topography

2013;22:532–541.

158.

Kuwabara

Gärtner

scavengers.

spectral

Quantitative

human

G,

radical

nal

Glaucoma.

2018;170:13–19.

137.

imag-

adaptive

2016;95:e5441.

Measurement

angiography.

and

(glial)

thickness

157.

C,

Paasche

Ophthalmol

(Philadelphia,

in

tomography

Balaratnasingam

and

an

2018;32:1723–1730.

Chalupa

Ramírez

microvasculature,

156.

coherence

comparisons

154.

2018;59:5847–5853.

plexus

Sivaswamy

optical

D,

C,

LC,

Müller

ness:

unit.

2017;26:241–246.

136.

using

1998;38:3655.

during

ageing

tomography.

153.

2015;35:2347–2352.

135.

High-resolution

eyes

2001;73:601.

normal

2017;7:42201.

high-resolution

reveals

152.

vascular

Segmentation

JM,

retinal

ner ve.

2018;64:1–55.

Detailed

projection-resolved

using

C outurier

vascular

tomography

Ret

angiography

Vis

NK,

angiography.

vasculature

Mané

deep

Prog

Hwang

Ishikura

Ophthalmol

macular

M,

tomography

tomography

Invest

JG,

angiography.

JP ,

coherence

Res.

Liets

etal.

human Müller glial cells. Invest Ophthalmol Vis Sci. 2000;41:2791.

151.

Fujimoto

tomography

132.

K,

Eye.

M,

human

2001;15(3):376.

Owsley

Vis

disease-related

2018;59:3858–3867.

131.

Eye.

retina

Ramírez

Res.

2012;33(6):1992.

130.

camera.

Meillat

healthy

Photoreceptor

GR,

Eliasieh

in

1967;77:769–776.

Schmidt

ber

Jackson

C,

in

2007;48:2824–2830.

PF ,

Ophthalmol.

129.

CA.

human

1968;7:672.

128.

Moureaux

retinal

Curcio

sensitivity.

GK.

in

P ,

photoreceptors

maculopathy.

2016;36:375–384.

127.

of

optics

Gehlbach

coherence

Tumahai

ing

2016;148:1–11.

K,

optical

and

8

165.

loss.

Exp

M.

Eye

Saunders

atrophy :

PL,

G,

Di

tomography

in

Renzo

A,

PW ,

membrane

and

its

role

in

retinal

etal.

Peripapillar y

changes

and

cho-

photorecep-

2000;107:334.

Ziccardi

Alzheimer’s

2015;10:e0134750.

lipofuscin

2005;80:595–606.

Y ounger

Bruch’s

Ophthalmolog y.

Coppola

RPE

Res.

L,

disease:

etal.

a

Optical

coherence

meta-analysis.

PLoS

ONE.

CHAPTER

166.

den

Haan

J,

Alzheimer’s

Alzheimers

167.

Cunha

of

optical

Retina

168.

LP ,

den

ness

Verbraak

disease:

Dementia

Almeida

J,

Alzheimer’s

with

disease

2018;10:49–55.

Visser

PJ,

systematic

(Amst).

etal.

review

Retinal

and

thickness

in

169.

meta-analysis.

2017;6:162–170.

Costa-Cunha

tomography

in

LVF ,

SF ,

van

parietal

and

Doustar

diseases.

etal.

Alzheimer’s

e

role

disease.

Intl

170.

J

Blanks

Kreeke

cortical

control.

JA,

etal.

atrophy

Alzheimers

in

Retinal

thick-

early-onset

Dementia

(Amst).

Torbati

in

171.

Tsai

ner ve

Y ,

disease.

Ritch

ber

Black

Neurol.

Torigoe

Neurobiol

CS,

T,

Alzheimer’s

Front

JC,

Alzheimer’s

retina.

de

J,

mography

2016;2:24.

Janssen

correlates

FD,

ALM,

coherence

Vitreous.

Haan

a

R,

layer

1991;109:199.

I.

etal.

Optical

and

139

Retina

other

coherence

to-

neurodegenerative

2017;8:701.

Hinton

DR,

Ganglion

Aging.

etal.

cell

Retinal

loss

in

patholog y

B,

etal.

Alzheimer’s

Optic

disease.

in

foveal/parafoveal

1996;17(3):377.

Schwartz

in

KL,

disease

8

ner ve

Arch

head

and

Ophthalmol.

9

Ocular

Embr yology

is chapter follows the chapters describing the globe because the

surface

study of embryology can be dicult if the adult structure, organi-

cells

zation, and function of the eye are not known. Although studying

the

development

of

a

structure

aer

studying

the

structure

itself

ectoderm

of

neural

Neural

might seem backward, teaching experience has proven this to be a

the

globe

useful

tive

tissue

sequence

for

the

student.

In

this

chapter,

the

development

of each structure is described separately, but the reader must keep

structure

in

dicult

mind

that

these

events

are

occurring

simultaneously.

crest

periocular

then

crest

gradually

origin

cells

and

mesenchyme,

and

is

is

orbit

because

mesoderm

from

from

neural

becomes

collectively

which

the

Although

neural

crest

or

separated

crest,

cells

and

make

connective

most

orbital

determining

mesodermal

mesodermal

from

it

by

mesoderm.

develop.

derived

of

and

origin

neural

is

crest

up

the

tissue

of

connec-

whether

a

sometimes

cells

appear

4

e

human

greatly

trol

have

to

expanded

cellular

cesses

genome

are

the

basis

of

identied

control

normal

migration,

and

and

advanced

understanding

development,

at

been

our

study

structure,

anatomic

that

of

bind

and

function.

receptor

by

have

similar

that

con-

cited

ese

pro-

processes

development.

to

development

the

technolog y

Growth

sites

on

modulating

factors

target

cells

proliferation,

dierentiation.

cytologically.

as

the

e

neural

cells

ated,

tube

origin

is

uncertain,

mesenchyme

is

layer.

constricts,

lining

and

the

the

inner

outer

forming

surface

surface

is

of

the

this

covered

optic

stalk

entire

by

a

(see Fig.

formation

thin

basal

9.2).

are

cili-

lamina.

e

cavity of the optic stalk, as well as that of the optic vesicle, is con-

with

While

OF

the

As the optic vesicle evaginates, the tissue joining the vesicle to

the

tinuous

DEVELOPMENT

germ

If

OCULAR

the

the

space

wall

of

that

the

will

optic

become

vesicle

is

the

in

third

ventricle.

contact

with

surface

STRUCTURES ectoderm,

the

optic

vesicle

thickens

and

attens

to

form

the

4

By the third week of embr yonic development, the three primar y

germ

layers—ectoderm,

formed

the

mesoderm

A

embr yonic

will

take

thickening

in

part

the

mesoderm,

plate.

in

Of

the

these

and

three,

developing

ectoderm,

visible

ectoderm

the

and

nervous

down

the

system,

center

of

including

this

plate

ocular

dorsal

at

structures.

approximately

A

day

BOX

e

lower

wall

of

the

Embryological

9.1

structures.

optic

vesicle

and

optic

stalk

surface

groove

18

of

Derivation

of

Ocular

Structures

of

the embryo, forms the neural plate, which will give rise to the cen-

tral

disc.

endoderm—have

only

ocular

on

retinal

Surface

ectoderm

gives

rise

to

•

Lens

•

Corneal

•

Conjunctival

•

Epithelium of eyelids and cilia, meibomian glands, and glands of Zeis and Moll

•

Epithelium

forms

epithelium

gestation, epithelium

and the ridges bordering the groove grow into neural folds. As the

groove

form

expands,

the

before

neural

fusing,

these

folds

tube

an

along

area

of

grow

the

cells

toward

dorsal

on

the

one

another

aspect

crest

of

of

the

each

and

fuse

embryo.

of

the

to lining

nasolacrimal

neural

Neural

ectoderm

gives

folds separates from the ectoderm; these are neural crest cells. e

•

Retinal

neural crest cells form islands of cells within the mesoderm which

•

Neural

•

Optic

•

Neuroglia

•

Epithelium

of

ciliary

•

Epithelium

of

iris

•

Iris

now

surrounds

the

neural

tube.

e

neural

tube

is

formed

on

or

1

near

day

22.

ectoderm

Neural

e

and

and

tissue

the

of

surface

surface

the

neural

layer

ectoderm

is

tube

now

dier

in

is

now

called

called

surface

anatomic

system

Just

pigment

rise

to

epithelium

retina

nerve

bers

neural

body

ectoderm.

location

and

in sphincter

and

dilator

muscles

dierentiation potentials (Box 9.1). Fig. 9.1 illustrates these events.

Neural

Optic

Indentations

on

both

form

sides

completely

grooves).

closed,

the

closed.

On

the

of

along

the

forebrain

ese

the

vesicle

surface

140

is

of

optic

pits

expand

vesicles

continuous

each

(Fig.

with

vesicle

surface

region

indentations

approximately

optic

inner

day

25,

9.2).

the

are

neural

before

the

optic

the

lateral

the

the

pits

neural

tube

tube

(optic

tube

sac-shaped

is

gives

e

until

cavity

of

it

the

within

neural

comes

in

•

Corneal

stroma

rise

•

Corneal

endothelium

•

Most

•

Trabecular

•

Uveal

pigment

•

Uveal

connective

•

Ciliary

•

Meninges

•

Vascular

(or

all)

of

(which

to

gives

(which

sclera

structures

cells

has

tissue

exten-

3

lumen

expands

of

even

aer

forming

2

sions,

crest

Pits

the

tube.

contact

muscle

optic of

optic

e

with

pericytes

nerve

rise

to

gives

Bowman

rise

to

layer)

Descemet

membrane)

CHAPTER

Cut

edge

of

begins

to

buckle

and

9

move

Ocular

Embryology

inward

toward

the

141

upper

and

pos-

amnion

terior Level

in Neural

is

invagination

forms

a

cle,

variously

called

the

seen

section

fetal

B

ssure,

embr yonic

ssure,

or

optic

ssure.

e

inferior

fold

wall Neural

walls.

continues

to

move

inward,

pulling

the

anterior

wall

of

the

groove

optic

vesicle

with

it

and

placing

the

retinal

disc

in

the

approxi-

Somite

mate

Primitive

node

at Primitive

location

toward

the

one

of

the

future

another

midpoint

of

and

the

retina.

begin

to

ssure

e

edges

fuse

and

at

5

of

the

weeks.

proceeds

ssure

grow

Fusion

anteriorly

starts

toward

streak

the

rim

of

the

optic

cup

and

posteriorly

at

weeks,

along

the

optic

stalk.

A

Closure

is

complete

7

forming

Ectoderm

the

two

layers

of

the

5

optic

Mesoderm

sure

cup

and

and

optic

moves

stalk

into

the

(Fig.

9.3).

cavity

of

Mesenchyme

the

developing

enters

optic

the

s-

cup.

Endoderm

B

Optic

Cup

e optic cup at this stage of development is composed of two lay-

ers

of

with

cells

each

outer

layers

separated

C

two

tial

Neural

folds

(both

other

by

layers

space.

pigment

ciliary

of

neuroectodermal

at

the

the

the

optic

of

cup

approach

each

epithelium

and

of

(RPE),

anterior

origin)

e

(see

nally

optic

outer

iris

will

are

of

apex

Fig.

cup

that

cells

positioned

the

the

in

cup.

space

other,

layer

the

the

are

intraretinal

e outer

body,

rim

to

9.2F),

epithelium.

only

become

pigmented

inner

apex

as

a

are

the

poten-

the

retinal

epithelium

e inner

and

and

which,

become

will

continuous

the

of

layer

the

will

become the neural retina, the inner nonpigmented ciliary body epi-

thelium,

D

iris

and

the

epithelium

wall

of

the

posterior

evolves

optic

cup,

iris

from

the

epithelium.

tissue

inner

Although

located

and

outer

in

the

the

area

epithelial

of

posterior

the

layers

of

inner

tissue

are continuous at the tip of the cup, and transcription factors found

in

the

outer

optic

cup

have

been

shown

to

curl

inward

around

the

6

anterior rim and are present in the posterior iris epithelium.

CLINICAL

COMMENT: Coloboma

E

Incomplete

stalk

and

nasal

the

defect

coloboma

Surface

crest

F

neural

coloboma

the

can

optic

optic

vary

disc,

from

a

ssure

of

may

these

retina,

slight

affect

the

structures.

ciliary

notch

body,

to

a

or

large

developing

This

iris.

results

This

optic

in

an

defect

wedgelike

is

cup

or

inferior

called

defect.

A

a

large

produces

a

keyhole-shaped

pupil,

although

the

remainder

of

the

7

iris

tube

of

may

have

affecting

the

denser

sensory

pigmentation

retina

and

than

RPE

the

also

opposite

involve

the

normal

iris.

choroid

Colobomas

because

its

dif-

ectoderm

ferentiation

nasal

Optic

of

and

the

derivations

iris develops normally (Fig. 9.4A). When the coloboma is unilateral, the affected

Mesoderm

Neural

of

adult

ectoderm

iris

Neural

closure

area,

depends

with

on

retinal

an

intact

vessels

RPE

layer.

passing

over

Bare

the

sclera

defect

is

seen

(Fig.

in

the

inferior

9.4B).

pit

Mesenchyme

and

once

the

proliferates

cells

reach

their

and

migrates

destination,

around

they

the

optic

proliferate

cup,

and

dif-

ferentiate, contributing to the connective tissue of the eye and orbit.

Neural

uveal

crest

cells

stroma

and

will

form

the

melanocytes,

corneal

ciliary

stroma

muscle,

and

endothelium,

much

of

the

sclera,

G

connective Fig.

9.1

Formation of neural tube.

A,

Dorsal

view

of

an

tissue

and

meningeal

sheaths

of

the

optic

nerve,

and

embr yo.

connective tissue of the lids, conjunctiva, and orbit. V ascular endoB,

A

horizontal

section

through

the

three-layered

embr yonic 8

disc

at

neural

nates

the

level

plate

and

shown

area

neural

of

the

folds

in

A.

C,

The

ectoderm.

are

formed.

neural

D,

The

E, The

groove

neural

neural

forms

groove

folds

in

the

thelium and striated muscle cells are formed from mesoderm.

invagi-

continue

DEVELOPMENT to

grow

the

toward

ectoderm

each

of

the

other.

neural

F,

Neural

folds

as

crest

the

cells

folds

separate

fuse.

The

OF

THE

GLOBE

from

neural

Lens tube

(of

neural

ectoderm)

is

formed,

and

the

surface

ectoderm

During becomes

continuous.

G,

Evaginations

in

the

area

of

the

embr yological

structures brain

form

the

optic

development,

formation

and

growth

of

fore-

depend

on

tissue

dierentiation

and

interactions

pits.

among

these

tissues.

Some

structures

will

not

develop

unless

CHAPTER

142

9

Ocular

Embryology

Optic

groove

Level

seen

in

section

Neural

fold

Neural

groove

B

Optic

Neural

groove

fold

Mesenchyme

Surface

A

ectoder m

B

Neural

tube

Notochord

Optic

stalk

Lens

placode

Lens

pit

Forebrain

Mesenchyme

Lens

Optic

placode

vesicle

Surface

C

ectoder m

Mesenchyme

Early

D

stage

of

optic

cup

Midbrain

Surface

ectoder m

Hyaloid

Outer

layer

of

optic

ar ter y

cup

Inner

layer Lens

of

optic

Wall

Lens

vesicle

cup

of

brain

vesicle

Intraretinal

Optic

E

space

fissure

F

Hyaloid

ar ter y

Hyaloid

vein

Fig.

9.2

rst

indication

Early

fold

showing

ectoderm

trating

We

they

are

some

In

near

cases

others,

the

two

the

from

Born:

development.

eye

stages

developing

structures

must

groove.

be

in

of

area

must

just

C, The

approximately

Essentials

structures

A, A

dorsal

development. B, A

optic

an

successive

Are

another

the

eye

of

in

forebrain

28-day-old

development

Embr yology

at

a

specic

actually

come

proximity

to

view

transverse

of

and

the

In

other,

the

its

cranial

at

end

the

covering

D,

optic

Birth

contact.

each

and

embr yo.

time.

in

of

section

E,

cup

and

and

Defects,

ed

a

22-day

shown

layers

F,

of

embryo

in A

showing

through

mesenchyme

Sections

lens

5.

of

level

of

vesicle.

a

and

developing

(From

Philadelphia:

the

Moore

Saunders;

the

neural

surface

eye,

KL.

illus-

Before

1998.)

day 27), and the surface ectoderm adjacent to the vesicle begins

to

thicken,

9.6A).

forming

is

the

thickening

lens

is

placode

caused

by

(lens

an

plate)

(Figs.

elongation

of

9.5

the

and

ecto-

4

allowing

ence

biochemical

that

one

induction.

It

signals

developing

is

likely

that

to

pass

structure

the

between

has

on

mechanism

them.

e

another

of

is

induction

inu-

termed

is

not

a

dermal

area

is

of

less

cells

and

contact

than

by

a

regional

between

normal,

a

the

increase

optic

perfectly

in

vesicle

formed

cell

and

but

division.

surface

If

the

ectoderm

microphthalmic

eye

12

single

event

but

a

series

of

separate

steps

that

presumably

occur

can

result.

In

some

species,

transformation

of

the

lens

plac-

9,10

on

a

biochemical

Induction

level.

occurs

ode

between

the

developing

optic

cup

and

tact

into

with

the

the

lens

vesicle

optic

might

vesicle,

but

be

independent

the

optic

of

vesicle

direct

does

con-

play

an

13

the

developing

lens,

apparently

through

a

reciprocal

relation-

important

role

in

lens

maturation.

In

addition

to

signals

from

9,11

ship.

vesicle,

As the surface ectoderm comes in contact with the optic

invagination

of

the

optic

cup

begins

(approximately

the

developing

optic

vesicle,

several

signaling

molecules

may

be involved, and complete lens dierentiation might depend on

CHAPTER

9

Ocular

143

Embryology

Lens

Lumen

Hyaloid

of

optic

layer

of

ganglion

Optic

seen

optic

stalk

fissure (containing

Level

stalk

vessels Inner

in

optic

in

section

axons

of

cells)

Mesenchyme

B

stalk

Walls

with

the

of

the

optic

wall

layers

of

stalk

of

the

the

are

continuous

brain

optic

and

cup

Lens

Optic

fissure

closed

Axons

Hyaloid

Level

seen

in

section

Optic

optic

cells

vessels

fissure

closing

cell

vessels layer

in

ganglion

D

Ganglion Hyaloid

of

of

the

retina

fissure

Axons

of

ganglion

cells

Sheath

with

of

the

choroid

C

the

optic

meninges

and

ner ve

of

the

(continuous

brain

and

the

sclera)

1 Optic

stalk

Central Lens ar ter y

vein

Axons

Optic

seen

of

the

retina

ganglion

cells

ner ve

Optic Level

and

of

in

section

fissure

closed

F

E

F

Central

Fig.

9.3

ferior

A

vein

and

Closure

surface

of

longitudinal

ar ter y

of

the

the

of

optic

section

the

optic

of

retina

ssure

cup

a

and

and

stalk

portion

of

formation

showing

the

optic

of

the

optic

progressive

cup

and

nerve. A,

st ages

optic

in

st alk

C,

and

closure

(C

)

E, Views

of

the

showing

of

optic

axons

the

in-

ssure.

of

retinal

1

ganglion

through

the

of

factors

that

inhibit

the

optic

cells

cells

growing

optic

ner ve.

accumulate

Embr yology

lens

stalk

Note

in

and

formation

through

showing

that

the

inner

Birth

in

the

the

the

optic

st alk

successive

lumen

layer

Defects,

of

ed

ectoderm

of

the

the

5.

toward

stages

optic

st alk.

in

to

brain.

closure

stalk

is

(From

Philadelphia:

adjacent

the

of

B,

the

obliterated

Moore

KL.

Saunders;

Cell

D,

and

optic

F, T ransverse

ssure

gradually

Before

We

as

and

formation

axons

Are

sections

of

Born:

of

ganglion

Essentials

1998.)

division

ceases

in

the

center

of

the

lens

placode,

form-

13,14

the

lens

placode.

One

of

the

factors

directing

the

develop-

ing

a

pit,

and

cell

division

accelerates

in

the

peripher y

such

that

15

ment

of

the

is

PAX6

lens

placode

and

the

later

development

of

the

lens

the

lens

placode

invaginates

rapidly.

As

invagination

contin-

9

the

gene.

ues,

the

lens

vesicle

is

formed.

is

separates

from

the

surface

CHAPTER

144

9

Ocular

Embryology

A

B

Fig.

9.4

retina

across

(A

A,

and

the

from

Mosby;

Iris

coloboma

optic

ner ve.

intact

Kanski

1999;

sclera. The

JJ,

B

in

both

Retinal

Nischal

courtesy

eyes. The

tissue

inferior

KK.

and

disc

lens

at

vesicle

cells.

e

aspect

is

approximately

is

a

apical

hollow

surface

covered

extracellular

by

a

proteins

day

sphere

of

the

thin

33

(Fig.

Pacic

9.6B

composed

cell

basal

deposited

lines

the

lamina.

by

cells

of

University

and

a

With

the

and

the

16

a

keyhole

tissue

signicant

Clinical

Family

are

cupping

Signs

Vision

appearance.

absent,

and

Center,

and

and

B,

Coloboma

retinal

vessels

malformed

Differential

Forest

blood

Diagnosis.

Grove,

of

the

course

vessels.

St

Louis:

Ore.)

e

layer

the

the

of

basal

addition

lens,

has

17

C).

single

lumen,

of

shows

Ophthalmology;

9

ectoderm

pupil

choroidal

of

basal A

lamina

will

become

the

lens

Presumptive

capsule.

fibers

Once

cells

the

adjacent

lens

to

vesicle

the

future

is

formed,

vitreous

the

cavity

posterior

elongate

to

epithelial

ll

in

the

B

Neural

ectoder m

Retinal

disc

Surface

Mesenchyme

ectoder m

Lens

placode

C

Elongating

posterior

epithelium

D

Primar y

lens

fibers

E

Fig.

ing

9.6

the

A,

nucleus.

Posterior

Fig.

9.5

Light

thickening

of

micrograph

the

lens

of

a

placode.

6-mm

pig

embryo

showing

mar y

The

Formation

lens

C,

vesicle.

The

cells

lens

hollow

ll

the

epithelium

the

to

lens

E,

lens

elongate

bers

anterior

of

C

placode.

vesicle

becoming

lumen

B,

Development

is

lined

in

the

place.

the

with

primar y

forming

remains

Invagination

of

lens

form-

embr yonic

epithelium.

bers.

embr yonic

E,

D,

Pri-

nucleus.

CHAPTER

Surface

Inner

of

the

ectoder m

layer

cup

9.7

Light

lens

micrograph

vesicle

lling

of

with

a

15-mm

primary

pig

lens

embryo

showing

ber s.

Fig.

9.8

the

Light

hyaloid

Vessels

are

attached

optic

lumen

within

the

lens

vesicle

(Fig.

9.6D

and

E

and

Fig.

9.7).

embr yos,

if

the

lens

is

experimentally

turned

180

to

cup,

of

epithelium

that

was

once

at

the

anterior

lens

vesicle

is

to

the

developing

optic

cup

and

will

elongate

the

extending

posterior

which

a

will

lens.

form

25-mm

lling

pig

the

through

the

retinal

is

stalk

seen

pigment

showing

vitreal

optic

Pigment ation

the

embryo

future

in

cavity.

and

the

are

outer

the

corneal

epithelium,

stroma,

epithelium.

and

Early

endothelium

to

Evidence

of

the

developing

eyelids

is

also

visible.

are

The

now lens

adjacent

evident

of

system

degrees, present.

the

micrograph

arterial

In

layers

chick

145

Embryology

cup

optic

Fig.

Ocular

layer

optic

Outer

of

9

ll

bow

is

evident

as

a

cur ved

line

formed

by

cell

nuclei.

in

18

the

lumen.

factors

in

e

the

entiation.

In

orientation

developing

addition,

the

19

maintenance

e

and

and

posterior

form

the

of

the

lens

is

inuenced

vitreous

which

promote

aqueous

environment

by

growth

cell

dier-

enhances

cell

The

epithelial

embr yonic

CLINICAL

cells

become

nucleus

at

the

the

primar y

center

of

lens

the

bers

lens.

is

spectrum

development

signicant

has

no

sutures.

e

fact

that

the

posterior

used

to

form

the

embr yonic

nucleus

accounts

for

the

an

an

epithelial

formed

layer

beneath

the

posterior

lens

e

capsule

in

primary

anter ior

anter iorly

epit helial

cells

remain

in

place,

and

t he

cells

A

fails

way,

bers.

(Fig.

viral

pinpoint

causing

to

extensive

induce

result

densities

the

loss

lens

from

having

of

bers

problems

no

vision.

to

effect

If

the

elongate

during

on

tissue

and

lens

vision

near

pack

to

the

the

lens

bers

will

be

misaligned,

forming

a

together

cataract

Interference

with

secondary

lens

bers

can

lead

to

of

sutural

9.9).

and

p oster iorly,

for ming

s econdar y

lens

laid

down

around

t he

embr yonic

nucleus.

infection

congenital

to

affecting

malformations,

the

rubella

virus

the

mother

including

(German

a

during

the

cataract.

measles)

rst

The

trimester

developing

between

the

often

lens

fourth

is

and

causes

vulner-

seventh

b ers

week

are

Cataract

can

the

able

t hat

from

that

lens.

ne ar t he equator b eg in to undergo mitosis. E ach ne w cell elon-

gates

lens

orderly

cataracts

fully

range

opacities

lack the

of

lens

epithelium

in

was

of

opacities

developing

nucleus

COMMENT: Congenital

20

growth.

e

of

development,

when

the

primary

bers

are

forming.

After

this

period,

rst the

virus

cannot

penetrate

the

lens

capsule

and

thus

will

not

affect

the

lens.

17

layer

of

s econdar y

b ers

is

completed

by

week

7.

S econdar y The cataract usually is present at birth but may develop weeks to months later

lens

b ers

continue

to

for m

and

e ach

layer

sur rounds

t he

prebecause the virus can persist within the lens for up to 3 years. The opacity may

vious

layer.

e

ends

of

t he

b ers

meet

in

an

upr ig ht

Y-suture be

immediately

p oster ior

to

t he

anter ior

epit helium

and

in

dense

nucleus,

inver ted

sule

Y-suture

(s ee

Fig.

immediately

7.9).

es e

anter ior

sutures

are

to

t he

visible

p oster ior

dur ing

t he

and

opaque

or

it

may

be

diffuse.

The

cataract

may

affect

only

the

an or

it

may

involve

most

of

the

lens.

cap-

t hird

21

mont h.

b ers

t he

e

for med

cellular

would

(Fig.

be

nuclei

bir t h.

wit hin

is

a

cont ains

If

a

line

lens

t he

were

b er

Y-sutures

drawn

layer,

conguration

is

an

to

and

arc uate

called

t he

all

connec t

shap e

lens

b ow

cell

compressed

5

elongation,

development

bers.

at

A

Arterial

branch

through

ing

spherical

tional

Hyaloid

of

the

the

System

internal

fetal

ssure

carotid

to

arter y

become

enters

the

the

hyaloid

optic

arter y

cup

dur-

22

9.8).

throughout

dent

nu cl eus

b efore

re ve aled.

Mitosis,

tially

fetal

in

Secondar y

by

lens

becomes

lose

outer

from

ectoderm

ber

throughout

bers

evolving

surface

and

but

successive

weeks,

invaginating

shape

and

and

life.

more

their

bers.

the

formation

ellipsoid

organelles

e

lens

basement

from

e

continue

lens

with

as

capsule

of

ini-

addi-

they

membrane

secretions

is

is

evi-

of

the

are

the

lens

week

5.

e

network

that

vascular

tunic

is

lls

vascular

of

hyaloid

the

the

arter y

vitreous

lens

network

produces

cavity

(posterior

covers

the

and

a

highly

forms

tunica

posterior

branching

the

posterior

vasculosa

lens

(see

lentis).

Fig.

9.8).

22

By

the

end

Branches

vessel

loops

at

of

week

near

the

the

12,

lens

margin

for ward

the

onto

of

the

hyaloid

equator

the

optic

anterior

vasculature

anastomose

cup.

e

surface

of

is

fully

with

the

annular

the

formed.

lens

annular

vessel

to

sends

form

the

21

epithelium.

anterior

vascular

tunic

of

the

lens

(anterior

tunica

vasculosa

CHAPTER

146

9

Ocular

Embryology

3

become

cannot

the

be

ciliar y

body.

identied

as

e

vessels

arterial

or

of

the

venous

on

hyaloid

the

system

basis

of

their

23

histological

Glial

mass

cells

of

12

the

surface

around

forming

hyaloid

week

on

tissue

proliferate,

e

makeup.

the

a

glial

vasculature

and

begins

to

of

base

the

of

mantle

reaches

atrophy

optic

the

cup

hyaloid

around

its

peak

during

the

the

month,

which

retinal

no

vasculature

blood

normally

extent

of

the

ow

should

is

is

in

13,

degeneration

24

at

of

the

the

during

same

the

hyaloid

reabsorbed

glial

cells

system.

time

25

By

the

completely

conelike

arterial

developing.

present

be

a

ese

development

week

22

that

form

arter y.

tissue

seventh

vasculature,

by

mass

birth.

e

denes

the

26

extent

of

the

CLINICAL

of

a

artery

the

of

on

the

a

9.9

Sutural

cataract.

8

lentis)

during

networks

tion

of

the

carr y

the

seventh

nutrients

aqueous

and

week

to

the

(Fig.

vitreous

vitreous

humor

are

seen

the

lens

as

from

papilla

of

its

often

Glial

(Fig.

surface

the

of

entire

remnants

brown,

are

tissue

9.11A),

Papilla,

the

at

of

lens

the

the

seen

that

and

hyaloid

attachment

are

small,

system

health.

posterior

stars

(Fig.

cup.

Mittendorf

Dot,

a

is

pinpoint

called

artery

disc

to

during

on

the

the

be

seen

posterior

tunica

opacities

on

examination

nerve

remnant

Mittendorf

will

anterior

stellate-shaped

clinically

persists

of

dot

( Fig.

coursing

lens

the

vessels

35

inner

drain

retina

into

before

a

retinal

ese

lens

occurs.

network

Cor neal

days

vascular

located

in

9.11B).

9.11C).

lentis.

anterior

is

hyaloid

through

( Fig.

vasculosa

the

head

the

They

surface

of

9.11D).

vascular

until

ey

Retinal

produc-

also

sup-

Pigment

Apposition

of

the

Epithelium

two

layers

of

the

optic

cup

is

essential

22

ply

and

23

9.10).

developing

hyaloid

ocular

remnant

Epicapsular

Fig.

the

Bergmeister

Rarely,

optic

Stars

patient’s

called

physiologic

COMMENT: Bergmeister

Epicapsular

Remnants

adult

the

region

epithelium

2

for

devel-

26

formation.

ese

that

opment of the RPE, the rst retinal layer to dierentiate.

will

structures

and

melanosomes

3-4

months

begin

to

appear

in

the

Cellular

outer

layer

months Eyelid

Cor nea

Anterior Anterior

chamber chamber

Lens

Annular

Cor nea

vessel Annular

T er tiar y

vessel

Lens

vitreous

Lens

vesicle

Eyelid

epithelium

Lens

Primar y

Primar y

vitreous

vitreous Secondar y Secondar y vitreous vitreous

Vor tex

vein Muscle

Vitreous

space Choroidal Hyaloid vessel ar ter y

Retina

Optic

A

B Hyaloid

Long

system,

occupy

brillar

and

Hyaloid

the

retina.

bers

mology,

its

vol

space

C,

forms

During

(tertiar y

into

main

reaches

the

narrow

the

Philadelphia:

the

(From

An

the

CS,

development

A,

the

weeks,

the

the

ner ve

V ,

editors.

B,

hyaloid

connect

Duane

s

By

ciliar y

with

FA.

of

of

the

hyaloid

Prenat al

Foundations

branches

the

more

vascular

nely

-

system

progressively.

toward

vessels

the

and

development

of

ar ter y

hyaloid

hyaloid

atrophy

region

the

and

months,

vitreous

system

of

vessels

2

branches

growing

Jakobiec

regression

hyaloid

secondar y

peripheral

of

from

Ozanics

1994.)

5

and

ectoderm.

avascular

optic

EA,

At

neural

vessels

stretch

Jaeger

Lippincott;

and

between

to

Cook

W,

sections.

lens

month,

of

Retinal

vitreous

extent.

begin

center

Tasman

in

zone

fourth

ar ter y

ar ter y

sagittal

greatest

the

retina.

In:

of

between

its

a

features

vitreous)

through

adnexa.

1 .

the

drawings

the

Vessels

loops

and

of

in

of

vitreous

capsule.

eye

shown

composition

Zonular

small

Schema

much

primar y

C

system ciliar y

Fig. 9.10

ner ve

posterior

Clinical

lens

send

of

the

Ophthal-

and

vein

of

CHAPTER

A

9

Ocular

147

Embryology

B

Extension

posterior

to

lens

Persistent

hyaloid

artery

C

D

Fig.

9.11

Remnants

retroillumination.

lens.

D,

Epicapsular

sonville,

the

optic

cup,

and

C,

of

the

hyaloid

Persistent

stars.

vasculature.

hyaloid

(Image

A

arter y

A,

seen

courtesy

of

Bergmeister

extending

Stephanie

papilla.

from

the

B,

Mittendorf

optic

Rettenmeier,

disc

Eye

to

to

dot

the

Eye

seen

in

posterior

Clinic,

W ill-

Ore.)

pigmentation

of

the

retinal

the

earliest

epithelium

occurs

neural

retinal

cells

b egins

in

the

central

retina

and

pro ceeds

8

at

approximately

week

3

or

4;

this

is

pigmentation

evi-

to

the

p eripher y.

27,28

dent

in

the

embryo

(see Fig.

9.8).

Aer

week

6,

the

RPE

is

one

Ganglion

cells

and

amacrine

cells

dierentiate

in

the

vit-

30

cell thick. e cells are cuboidal to columnar in shape. e base of

read

each cell is external toward the developing choroid, and the apex is

cells

internal toward the inner layer of the optic cup.

and

portion

of

migrate,

almost

the

inner

forming

a

neuroblastic

layer

immediately

close

send

out

to

layer.

the

their

e

basement

axonal

ganglion

membrane,

processes,

which

21

become

evident

by

week

8.

Biomolecular

agents

guide

axonal

31,32

Neural

B etween

Retina

weeks

growth

4

to

6,

the

cells

of

the

inner

layer

b ecome

the

neural

of

the

optic

e

toward

bodies

of

termination

the

Müller

in

and

the

lateral

amacrine

geniculate

cells

remain

nucleus.

in

the

inner

30

c up

(in

the

area

that

will

retina)

prolifer-

neuroblastic

layer

but

move

slightly

sclerad.

29

ate,

and

outer

two

zones

region,

the

are

e vident.

prolifer ative

e

cells

z one

or

acc umulate

in

germinating

the

z one.

Bipolar

settle

cells

near

the

migrate

Müller

from

and

the

outer

amacrine

neuroblastic

cells;

the

layer

horizontal

and

cells

8

e

inner

marg inal

z one

(of

His)

is

anuclear

(Fig.

9.12A).

follow.

e

ber

layer

of

Chievitz

is

gradually

obliterated

by

21

A

of

thin

the

lamina,

optic

membrane,

ity.

the

the

At

the

c up

bas ement

and

s eparates

approximately

inner

and

tr ansient

outer

b er

the

the

membrane

prec urs or

marginal

week

7,

cell

neuroblastic

layer

of

of

zone

of

the

layers,

the

layer

limiting

vitreal

o cc urs,

b etween

a

inner

internal

f rom

migration

C hie v itz,

the

cav-

forming

w hich

nucleus-f ree

lies

this

move

is

9.12B).

complete

the

photoreceptor

week

the

12

the

inner

between

them.

nal

limiting

layers

the

h

prospective

cells

remain

of

the

ese

optic

bipolar

in

photoreceptors

layer

area

29

(Fig.

of

the

are

cup

junctions

membrane.

and

horizontal

outer

aligned

and

neuroblastic

along

adhering

form

the

Photoreceptor

cells.

the

layer.

outer

junctions

precursor

cells

of

e

side

of

appear

the

dierentiate

By

exter-

during

8,9

e

formation

during

the

of

third

thes e

two

month.

neuroblastic

Dierentiation

of

the

month.

ferentiate

during

Cones

the

dierentiate

seventh

rst

month.

and

e

rods

early

begin

inner

to

dif-

segment

CHAPTER

148

9

Ocular

Embryology

A B

Fig. 9.12

the

B,

inner

Developing

layer

Human

IN,

Inner

retina;

O,

of

the

photoreceptor

distal

cell

the

embr yo

retina. A,

optic

at

outer

cup.

week

neuroblastic

epithelium.

the

of

neuroblastic

(From

portion

a

the

lens;

layer;

optic

embr yo

at

accumulate

in

postconception. The

L,

Peces-Peña

of

produces

7

layer;

Human

Cells

PE,

MD,

cup

the

that

the

6

inner

becomes

region

and

of

and

outer

of

the

6

of

zones

inner

the

ciliar y

ciliar y

Cells, Tissues,

month

the

the

neuroblastic

epithelium

epithelium

Development

human.

postconception. T wo

outer

nonpigmented

pigmented

etal.

in

protuberance

NPE,

week

body:

Organs

there

layers

ciliar y

body;

are

region

dened.

NR:

retinal

morphological

in

anuclear.

are

body;

RPE,

evident

is

neural

pigment

changes

in

2013;198(2),149-159.)

is

no

further

mitosis,

and

retinal

growth

con-

39

embedded

in

the

RPE

and

continues

to

grow,

forming

the

cil-

tinues

because

of

cell

dierentiation,

growth,

and

maturation.

21,33

ium

and

e

outer

segment

horizontal,

developing

in

the

by

week

bipolar,

inner

24

or

25.

amacrine,

nuclear

layer,

Foveal

and

and

Müller

the

inner

cells

and

are

outer

of

inner

tion

of

development

retinal

consists

components

photoreceptors

of

to

toward

three

form

the

stages:

the

(1)

displacement

depression;

center,

which

(2)

migra-

increases

cone

40

plexiform

of

the

layers

Müller

forming

the

are

cells

lling

with

appear

primitive

neuronal

and

internal

extend

limiting

processes.

to

the

e

basal

membrane,

bers

lamina,

and

exter-

packing;

sixth

tion

and

month

of

(3)

maturation

cones

nuclei

in

begin

the

to

of

the

photoreceptors.

dierentiate,

macular

area

makes

and

this

a

During

dense

region

the

accumula-

thicker

than

26,38

nal

processes

cell

provides

extend

a

between

scaolding

for

the

cell

rods

and

cones.

development

e

and

Müller

appears

to

the

the

rest

of

the

ganglion

retina.

cell

In

layer

is

addition,

thicker

in

throughout

the

the

macular

sixth

area

month

compared

34

be involved with guiding the direction of axonal ber growth.

with

Fig.

evident.

the

peripheral

retina,

with

up

to

nine

rows

of

ganglion

cells

37,41,42

the

9.13

shows

neural

a

summar y

of

the

steps

in

the

development

of

retina.

Synaptic

During

the

seventh

month

the

ganglion

cells

and

the cells of the inner nuclear layer begin to move to the periphery

complexes

begin

to

appear

at

about

the

same

time

of

the

macula

and

the

beginning

of

the

foveal

depression

can

be

35,38,42

as the plexiform layers, with the inner plexiform layer preceding

seen.

By birth, there still is a single layer of ganglion cells and

35

the

outer

ules,

and

layer.

Cone

pedicles

photoreceptor

develop

synapses

with

earlier

than

bipolar

cells

rod

are

spher-

estab-

a

thin

(Fig.

inner

9.14).

nuclear

layer

Between

9

and

across

45

the

now-depressed

months

postpartum,

foveal

both

of

area

these

36

lished

before

the

outer

segments

are

completed.

layers

are

completely

displaced

to

the

sloping

walls

of

the

fovea,

37

By

month

5

the

ganglion

cell

layer

is

well

established.

leaving

the

cones

of

the

outer

nuclear

layer

as

the

only

neural

cell

38

Because

retinal

peripherally,

development

the

ganglion

is

more

axons

advanced

from

the

centrally

peripher y

than

must

take

bodies

in

continues

the

to

center

widen

of

and

the

depression.

deepen

until

e

about

foveal

age

15

to

depression

24

months

41,42

an

the

arched

ner ve

route

head.

above

is

and

line

of

below

the

deviation

macular

at

the

area

to

horizontal

reach

tempo-

as

cells

e

continue

foveola,

to

move

the

toward

retinal

area

the

of

macular

sharpest

periphery.

visual

acuity,

is

the

40

ral

meridian

is

termed

the

horizontal

raphe.

During

the

h

last

to

reach

maturity.

B efore

birth

the

rod-free

area

is

large

38

month,

a

reduction

of

retinal

cells

by

apoptosis

begins.

By

compared

with

that

in

the

adult.

e

cones

migrate

centrally,

CHAPTER

Developmental

Basal

lamina

of

marginal

structures

Retinal

9

cells

Ocular

Adult

zone

retina

Internal

Nerve

Marginal

zone

149

Embryology

limiting

fiber

membrane

layer

Ganglion

Ganglion

Inner

neuroblastic

layer

cell

layer

Amacrine

Inner

plexiform

Inner

nuclear

layer

Müller

Proliferative

zone

Transient

layer

of

Chievitz

layer

Bipolar

Outer

neuroblastic

layer

Outer

plexiform

Outer

nuclear

layer

Horizontal

layer

Photoreceptor

Photoreceptor

RPE

Retinal

Fig.

9.13

Flow

chart

of

retinal

cone

density.

At

birth,

41

cone

nuclei

layer

is

thick

by

2

to

in

4

the

foveal

nuclei

is

only

a

single

layer

41

208,200/mm

of

epithelium

at

age

37

years.

e

cone

inner

bers

elongate

42

pit.

thick

there

pigment

development.

2

increasing

layer

In

at

15

contrast,

months

the

aer

outer

birth,

and

nuclear

8

to

nuclei

adopt

synapse

an

oblique

with

the

orientation

cells

of

the

(forming

inner

Henle

nuclear

ber

layer,

layer)

which

have

41

4

years,

and

12

nuclei

thick

by

13

years.

Cone

2

increases from 18,472/mm

been

density

displaced

to

the

sloping

walls.

During

years,

the

photoreceptor

outer

segment

continues

41

2

at 15 months, 108,400/mm

and

at 4 years, and

A

the

inner

ber

lengthens.

B

Fig.

9.14

Human

tom). The

inner

single

layer

within

500

pit

deep.

ner

is

cones

µm

the

D, Vajzovic,

inner

outer

S:

to

over

2

B,

thin

cone

ELM:

Fovea

The

layer;

layer;

2012;154(5),

of

at

inner

inner

contact; TC:

Histologic

One

day

deep.

center

and

external

plexiform

plexiform

A,

cells

the

shallow.

synaptic

etal.

Ophthalmol.

long

1

center.

and

choroid;

IPL:

rod;

L,

foveal

of

are

present

wide

OPL:

R:

development.

layers

is

CH:

layer;

layer;

epithelium;

J

of

more

axon;

nuclear

Am

foveal

retinal

composed

(Ax:

nuclear

sin

of

becomes

center

the

rst

few

2

at 22 week gestation to 36,294/mm

2

at birth, 52,787/mm

foveal

the

3.8

OS:

development

of

pit.

(top)

the

of

13

have

and

P:

fovea

days

are

2

day

years

cone

foveal

3

deep,

one,

rods

bodies

ber

pit;

cell

layer;

layer;

PE:

The

are

foveal

8

to

12

INL:

in-

to

outer

pigment

Hendrickson

midgest ation

a

are

foveal

ONL:

retinal

(bot-

and

(R)

(bottom). The

cell

(From

from

postnat al

to

displaced.

ganglion

ner ve

Chievitz.).

human

8

been

GCL:

NFL:

segment;

and

slope

postnat al

and

segments,

layer

pit

At

neurons

segment;

outer

(top)

the

membrane;

inner

transient

767-778.e2.

years

outer

on

foveal

retinal

limiting

IS:

postnat al

Cones

A,

Pos-

maturit y.

to

develop

CHAPTER

150

9

Ocular

Fig.

9.15

Embryology

Absence

of

fovea

depression

in

a

patient

with

ocular

albinism.

38

CLINICAL

COMMENT: Ocular

Albinism

the

foveal

pit

may

be

absent

(Fig.

9.15).

The

overall

number

of

rods

may

be

43

Melanocytes

in

the

that

choroid,

derive

skin,

and

their

hair)

pigment

show

a

from

neural

variance

crest

(i.e.,

that

is

(i.e.,

retinal

related

those

to

located

race.

Mela-

decreased.

Abnormal

occurs,

more

with

optic

crossed

nerve

bers

projection

than

to

normal,

the

lateral

often

geniculate

resulting

in

nucleus

binocular

vi-

43

nocytes

that

are

neuroectodermal

in

derivation

pigment,

iris,

and

sion

anomalies.

37

ciliary

body

epithelia)

tion

gene

regulated,

of

is

melanocytes

retina

is

can

inuenced

are

be

by

densely

and

in

an

affected.

a

pigmented

individual

Because

melanin-related

in

with

normal

agent

all

races.

albinism,

Melanin

either

development

produced

in

the

or

of

the

RPE,

produc-

both

types

sensory

when

Retinal

Vessels

pig-

e

fetal

ssure

along

the

optic

stalk

closes

around

the

hyaloid

ment is absent from this layer, as occurs in ocular albinism, a number of retinal

arter y, abnormalities

are

present

at

birth

in

addition

to

the

absence

of

and

the

portions

of

the

vessel

A

branch

within

the

stalk

become

pigmentation. 9

the The

macula

is

underdeveloped,

there

is

no

rod

free

or

avascular

zone,

central

retinal

arter y.

of

the

primitive

maxil-

and

lar y

vein

located

within

the

optic

stalk

is

the

likely

precursor

CHAPTER

9

Ocular

151

Embryology

28

of

the

central

retinal

vein

Early

in

the

fourth

month

of

as

well

as

that

giving

rise

to

the

sclera,

are

of

neural

crest

origin

29,48

development,

loid

arter y

near

9

ber

primitive

22

24

the

retinal

optic

disc

vessels

and

emerge

enter

the

from

the

developing

hya-

(see

ner ve

Box

At

3

9.1).

months

all

layers

of

the

cornea

are

present

(Fig.

9.16)

25

layer.

Outer

retinal

capillaries

that

form

the

deep

ner ve

ber

except

Bowman

layer,

which

appears

during

the

fourth

49

capillar y

network

sprout

from

the

22

layer

around

the

sixth

vessels

in

the

month

and

is

presumably

formed

by

broblasts

24

of

the

anterior

56,57

month.

e

fovea

remains

avascu-

stroma

and

secretions

of

the

epithelial

cells.

Whatever

the

53

lar

throughout

guide

the

development.

growth

and

Signals

pathway

of

growth

of

these

the

vascularized

retinal

tissue

biomolecular

neurons

22

the

from

likely

also

guide

Astroc ytes

vascular

at

the

edge

endothelial

of

growth

24

factor,

which

promotes

and

stage,

Bowman

ment

and

layer

is

subsequent

always

acellular.

production

of

Fibroblast

collagen

brils

arrange-

begins

in

44

vessels.

synthesize

and

agents

directs

growth

of

the

posterior

of

the

corneal

corneal

stroma

stroma

45

vessels.

and

causes

proceeds

an

anteriorly.

increase

in

Rapid

cur vature

growth

relative

to

4

the

rest

(55

D);

of

the

globe.

At

birth

the

cornea

is

circular

and

steep

8

Müller

cells

may

play

a

role

in

creating

extracellular

spaces

the

cur vature

decreases

to

44

D

at

6

months

aer

birth.

22

in

which

develop

blood

from

gradually

Vessels

vessels

the

forming

reach

the

can

posterior

the

by

40

peripher y

25

e

vessels

toward

arterioles,

nasal

24

peripher y

grow.

pole

the

venules,

by

36

of

the

retina

peripheral

and

weeks

retina,

capillar y

and

the

beds.

temporal

Sclera

e

sclera

rst

mesenchyme

develops

near

the

anteriorly

limbus.

from

condensations

Growth

continues

in

the

posteriorly

46

weeks.

until

the

third

sclera

month,

reaches

the

the

sclera

optic

has

ner ve,

and

surrounded

by

the

the

end

of

developing

the

cho-

28

CLINICAL

Infants

zone

can

born

COMMENT: Retinopathy

prematurely

peripherally.

develop

If

have

they

retinopathy

are

of

incomplete

exposed

to

prematurity

of

a

vasculature

high

(also

roid.

Prematurity

retinal

with

concentration

called

retrolental

an

of

avascular

oxygen

they

broplasia).

The

the

During

posterior

bers

and

the

fourth

scleral

month,

foramen,

producing

the

connective

running

rst

connective

cause

tion

the

vessels

occurs;

to

reduced

stop

however,

the

vascular

developing.

new

vessel

endothelial

On

removal

growth

is

growth

of

the

factor

oxygen,

composed

of

levels

tissue

optic

strands

cross

ner ve

cribrosa.

By

the

h

month,

the

sclera

of

the

(including

the

27

scleral

and

bers

the

3

lamina

immature retinal blood vessels respond to the high concentration of oxygen with

vasoconstriction

tissue

through

spur)

is

well

dierentiated.

which

vasoprolifera-

leaky

vessels

with

Uvea

poorly formed endothelial tight junctions. Potential serious complications include

Choroid neovascular invasion of the vitreous and development of vitreoretinal adhesions,

e which

may

be

followed

by

hemorrhage

and

retinal

mesenchyme

that

forms

the

choriocapillaris

must

be

in

detachment.

contact

with

the

developing

pigment

epithelium

to

dierenti-

5,27

ate.

Cornea

At

e

choriocapillaris

development

about

the

time

the

lens

vesicle

separates

from

the

surface

vessels

of

appear

the

larger

during

forms

from

choroidal

week

7,

and

progenitor

vessels.

the

e

cells

before

choriocapillaris

diaphragm-covered

fenes-

22,58

ectoderm

(day

33),

induction

by

the

PAX6

gene

initiates

the

trations are evident by week 12.

Outer choroidal vessels begin

9,47,48

multiple

of

step

epithelial

development

cells

from

of

the

surface

cornea.

One

ectoderm

or

become

two

layers

aligned

and

to

form

and

by

from

the

buds

end

of

the

of

the

within

the

outer

h

choriocapillaris

month,

three

during

layers

of

week

blood

12,

vessels

22,58

will

form

the

corneal

epithelium.

During

the

sixth

week,

zonula

are

evident

posterior

pole.

By

the

sixth

month,

the

8

occludens

are

evident.

e

rst

component

of

the

anchoring

choriocapillaris

has

open

lumens,

contiguous

fenestrations,

and

22,58

system

is

the

basal

lamina,

which

is

evident

by

week

9,

and

mature

pericytes.

e

short

posterior

ciliar y

arteries

also

49

hemidesmosomes

month,

all

the

are

cellular

present

layers

by

of

week

the

13.

corneal

are

3

By

the

h

epithelium

or

sixth

are

pres-

evident

and

Bruch

begin

to

anastomose

membrane

develops

to

form

during

the

circle

month

4.

of

At

Zinn.

midterm

in

50

ent.

Corneal

mesenchyme

endothelium,

that

migrates

formed

into

the

from

space

the

rst

between

wave

the

of

corneal

fetal

ent,

development,

the

basement

the

elastic

sheet

membrane

of

of

the

Bruch

RPE

is

membrane

is

developing,

pres-

and

the

47

epithelium

and

the

lens,

is

one

to

two

cells

thick

by

week

8.

At

collagenous

layers

are

thickening.

e

basement

membrane

of

3

3

months

the

endothelium

is

a

single

row

of

attened

cells

with

the

choriocapillaris

is

the

last

component

3,51

a

basal

By

in

the

the

lamina,

middle

the

of

rst

the

endothelium,

evidence

fourth

of

month,

coinciding

Descemet

tight

with

membrane.

junctions

the

are

to

appear.

By

term,

59

the

choroidal

stroma

is

pigmented.

apparent

beginning

of

Descemet

membrane

aqueous

Ciliary

Body

47,52

formation.

before

e

birth

has

material

a

comprising

banded

appearance,

whereas

the

tissue

e

region

the

outer

of

the

outer

pigmented

layer

of

the

optic

epithelium

of

cup,

the

which

ciliar y

will

become

body,

begins

29

secreted

by

the

endothelium

aer

birth

(which

has

a

more

pos-

to

form

ridges

in

the

ninth

week.

e

inner

nonpigmented

53,54

terior

By

position)

week

migrates

has

8,

a

a

homogeneous,

second

between

the

wave

of

developing

unbanded

appearance.

mesenchyme

epithelium

and

epithelium,

proliferates,

endothelium,

ese

folds,

Zonula

from

the

almost

occludens

70

are

inner

in

optic

cup,

number,

evident

in

grows

become

the

the

inner

and

folds

ciliar y

with

it.

processes.

nonpigmented

epi-

8

and

gives

rise

to

the

broblasts,

collagen,

and

ground

substance

thelium

during

the

third

month.

Neural

crest

cells

dierenti-

55

of

the

stroma.

A

third

wave

of

mesenchyme

migrates

into

the

ate

into

stromal

elements.

e

fenestrations

in

the

capillaries

3,60

area

to

between

the

the

pupillar y

developing

membrane.

endothelium

ese

three

and

waves

lens,

of

giving

rise

mesenchyme,

of

the

processes

are

visible

in

the

fourth

month.

During

the

fourth month, the major arterial circle of the iris is formed by the

152

CHAPTER

9

Ocular

A

39

Embryology

D

days

3

months

Epithelium

Basal

lamina

Endothelium

B

7

weeks

Stroma

1

C

7

weeks

/ 2

Descemet

membrane

Endothelium

1

E

4

Epithelium

months

/ 2

F

7

months

Basal

lamina

Bowman

layer

Stroma

Descemet

membrane

Endothelium

Fig.

9.16

basal

B,

At

and

is

Developing

lamina.

7

weeks,

arranged

D,

in

By

proximately

posterior

the

above

basal

are

the

is

A

30

thin,

basal

lamina.

strewn

adult

randomly

In

in

a

are

in

the

bottom

of

CS,

Ozanics V ,

EA,

editors.

E

the

with

and

respect

FA.

the

and

is

to

only

that

Prenatal

Foundations

of

a

days,

7½

two

weeks,

or

three

midterm

indenite,

anterior

Clinical

a

of

few

in

of

of

are

the

regularly

most

some

matrix

developed.

lack

eye

and

vol

is

its

1 .

collagen

not

F,

in

adnexa.

are

7

months,

still

rest

of

Breaks

(From

In: Tasman W,

Philadelphia:

the

keratoblasts

the

brils.

its

forming

beneath

At

represented.

ap-

in

keratoblasts

keratoblasts

lamellae

among

has

arranged

stroma,

a

epithelium

appear

cells

on

space.

(broblasts)

stroma

emerges

supercial

stroma

Ophthalmology,

wing

layer

well

the

posterior

multilayered

is

the

brils

more

Collagenous

of

bet ween

and

rest

cellular

Mesenchyme

collagen

Bowman

the

epithelium

narrow

cells,

the

mostly

the

portion

few

layers

C,

of

by

space

months),

surface.

development

and

membrane

A

the

bet ween

(4.5

layers

stroma.

which

portion

spaces

central

into

acellular

Descemet

corneal

is

two

endothelium

corneal

membrane

few

the

39

peripher y

future

est ablished.

the

At

(keratoblasts),

By

an

formation.

indicate

Jakobiec

Duane’s

of

cornea

array,

F

E,

and

one-third

disorganized

parallel

Descemet

the

by

has

A,

three-layered

the

layers

endothelium.

of

of

broblasts

cells,

to

from

epithelium

uneven

almost

oriented

migrates

of

region.

t wo-

incomplete

epithelial

structure

a

precursor

the

layers

monolayered

the

stroma

to

the

ve

months,

25

half.

or

is

central

from

mesenchyme

four

3

cornea,

separated

endothelium. This

them.

and

It

Lippincott;

are

the

near

Cook

Jaeger

1994.)

CHAPTER

anastomosing

long

ciliar y

arteries

and

replaces

the

annular

9

Ocular

153

Embryology

ves-

61

sel.

of

Gap

the

junctions

two

and

epithelial

desmosomes

layers

during

appear,

the

joining

fourth

the

month.

apices

e

cili-

62

ar y muscle begins

to

develop

from

neural

crest

during

the

sev-

29

enth week.

3

However, the circular muscle remains incomplete at

27

birth.

Aqueous

humor

production

begins

at

4

to

6

months

of

60

gestation.

Iris

By

the

end

of

the

elongate

and

nea.

outer

e

epithelium

lium.

by

basal

the

layers

marginal

aspect

month,

between

layer

and

ese

the

third

grows

of

the

optic

layer

remain

sinus.

of

the

inner

the

the

lip

cup

the

and

cup

from

the

each

of

epithelium

begins

developing

iris

other

iris

epithe-

for

a

myolaments

adjoining

to

cor-

anterior

the posterior

proliferation

anterior

optic

the

becomes

forms

separated

e

of

lens

the

time

in

the

stroma

transforms the layer into myoepithelium. e group of cells that

will

become

zone

of

this

the

iris

sphincter

epithelial

layer

breaks

during

away

the

h

from

5

into

smooth

gestational

develop

pleted

ral

muscle

month,

within

by

from

the

the

birth.

ectoderm

within

bers

epithelial

at

is

the

the

unusual

mesenchyme.

iris

of

layer,

sphincter

because

and

most

Pigmentation

in

muscle

both

the

dilator

come

are

is

and

to

com-

from

tissue

anterior

sixth

continue

muscles

muscle

the

develops

During

dilator

and

pupillar y

and

63

stroma.

the

the

month

neu-

derived

posterior Fig. 9.17

epithelium

begins

to

appear

at

approximately

week

10

and

of

complete

during

the

seventh

month.

e

marginal

sinus

a

35-mm

and

the

intercellular

two

epithelial

layers

are

joined

at

their

human

apices

by

&

I.

The

Stratton;

Development

1994.

cells

line

up,

leaving

large

gaps

form

are

of

the

anterior

neural

crest

border

origin

layer.

and

8

the

second

collagen

Stromal

the

wave

bers

of

begins

of

the

iris

to

Human

1964,

British

Eye.

8

weeks).

New Y ork:

(From

Medical

Grune

Association.)

can

to

continue

said

stromal

to

compo-

migrate

f rom

brane

with

some

A

sparse

to

form

produce

to

stromal

As

occurs,

distribution

the

more

darken

for

iris

stroma.

pigment,

the

of

rst

6

collarette,

the

rior

with

reabsorption

loops

of

the

of

the

central

midregion

pupillar y

form

the

mem-

ridge

border

organization

not

other

components

incorporated

into

of

the

the

ante-

layer.

and

postCLINICAL

months,

65

disappeared.

64

accumulate

continue

e

are

mesenchyme.

melanoc ytes

color

natal

Copyright

the

between

5

nents

to

(approximately

of

junctions.

Mesenchymal

them,

embryo

disapMann

pears

Section through the eye and surrounding structures

is

COMMENT: Persistent

Pupillary

Membrane

complete Remnants

of

the

central

portion

of

the

pupillary

membrane

that

do

not

reab-

8

until

age

7

years. sorb

may

spider

Pupillary

be

web

seen

with

attached

to

a

biomicroscope

the

surface

of

and

the

appear

iris

(Fig.

similar

9.18).

A

to

strands

persistent

of

a

pupil-

Membrane lary

membrane

may

have

a

variety

of

presentations,

from

a

single

strand

of

As the lens thickens, its anterior vascular tunic disconnects from

connective

the

strands. Pigment cells also might be incorporated. A persistent pupillary mem-

annular

vessel,

and

its

constituents

are

incorporated

into

tissue

(anchored

at

one

or

both

ends)

to

several

interconnecting

65

the

iris

iris.

stroma.

During

between

replace

the

the

the

Remnants

third

lens

month,

epithelium

vascular

components

contribute

from

tunic.

the

the

and

is

third

the

major

circle

of

the

the

wave

minor

pupillar y

the

of

circle

membrane

corneal

transitor y

8

from

to

of

mesenchyme

and

is

present

in

17%

to

32%

of

the

population.

forms

endothelium

membrane

brane

the

to

contains

branches

Anterior

A

mass

of

Chamber

cells

of

Angle

neural

crest

origin

and

f rom

the

rst

wave

of

65

iris.

e

pupillar y

membrane

can

mesenchyme

accumulates

adjacent

to

the

ciliar y

body

and

the

54,66

be seen in Fig. 9.17 just anterior to the lens. ree or four arcades

iris

of

whereby

thin-walled

blood

vessels

separated

by

a

thin

mesodermal

root

in

the

this

anterior

mass

is

chamber

eliminated

to

are

completed

by

the

end

of

the

h

month.

e

vessels of the pupillar y membrane cannot be identied as arterial

controversial.

between

the

e

iris

mass

and

venous

on

the

basis

of

their

histological

expose

the

e

method

angle

remains

may

atrophy,

trabecular

the

structure

meshwork,

with

may

some

split

tissue

67

23

or

area.

27

65

membrane

angle

contributing

makeup.

to

each,

or

the

intercellular

spaces

may

enlarge

68

During

lar y

gestational

membrane

peripheral

month

atrophy

vessels

6,

and

contribute

the

central

become

to

the

vessels

of

bloodless.

minor

the

pupil-

e

more

and

e

the

iris,

of

fragmented

and

this

circle

of

the

cells

reorganize

trabecular

mesenchymal

into

the

meshwork

cells

during

is

the

surrounding

visible

fourth

as

a

tissue.

triangular

month;

at

least

mass

part

of

69–71

and

by

8.5

months

the

central

vessels

have

tissue

is

of

neural

crest

origin

(see

Box

9.1).

e

tissue

CHAPTER

154

9

Ocular

Embryology

e

secondar y

hyalocytes.

vitreous

bundle

in

of

vitreous

During

the

contains

the

third

anterior

Druault).

a

bril

month,

peripheral

is

forms

a

network

and

thickening

area

occurs

attachments

at

of

primitive

secondar y

(the

the

marginal

vitreous

base

8

and

at

the

e

tor

hyaloideocapsular

zonule

and

the

bers

ciliary

ligament.

develop

body.

in

ey

the

area

have

between

been

called

the

lens

tertiary

equa-

vitreous

because they do arise in the vitreous and were assumed to be collag-

8

enous, but now are believed to be noncollagenous.

the

zonules

pass

through

the

marginal

bundle

of

Fibers forming

Druault

at

right

angles. Early zonule bers appear to be a continuation of a thicken-

ing

by

of

the

the

internal

ciliary

limiting

epithelium.

membrane

e

bers

of

run

the

ciliary

from

a

body,

zone

formed

near

the

ora

serrata and from the valleys between the processes to the lens cap-

sule. e zonules are well formed during the seventh month.

Optic

e

Fig.

9.18

Persistent

Brunsvold,

Pacic

pupillary

University

membrane.

Family Vision

(Courtesy

Center,

Forest

Jade

Grove,

Nerve

optic

vesicle

stalk,

to

inferior

the

the

precursor

forebrain.

stalk

As

of

the

invagination,

a

the optic

optic

ner ve,

ssure

two-layered

joins

develops

optic

stalk

the

optic

along

is

the

created.

Ore.)

e

outer

layer

of

the

optic

stalk

becomes

the

neuroglial

sheath

that surrounds the optic ner ve; it also gives rise to the glial com-

progressively

becomes

more

organized,

and

by

9

months

the

tra-

becular beams and pores are well developed, with the intratrabec-

ular

spaces

and

pores

likely

formed

by

programmed

cell

the

canal

is

fourth

derived

month,

from

tight

the

deep

junctions

scleral

are

with

in

of

the

the

lamina

lumen

of

the

cribrosa.

optic

During

ner ve

the

becomes

ninth

gestational

progressively

ganglion

cell

axons.

Concurrently,

programmed

cell

lled

death

70

plexus.

evident

week

2

death.

69

Schlemm

During

ponents

the

occurs

in

avenue

for

the

cells

passage

of

of

the

the

inner

axons

optic

from

cup

layer,

ganglion

providing

cells

entering

an

the

68

canal’ s endothelial lining.

canal

is

month,

fully

giant

complete

Once

formed

vacuoles

circular

endothelium

the

that

some

are

canal

formed,

During the seventh month, Schlemm

in

is

seen

in

present

anterior

covers

quadrants.

the

the

During

endothelial

during

chamber

trabecular

the

is

lining,

ninth

lined

the

by

meshwork

eighth

and

the

month.

a

the

of

stalk.

the

Other

optic

increases

cells

ner ve.

from

of

e

1.9

the

inner

number

million

of

during

wall

become

axons

the

in

the

second

the

optic

glial

cells

ner ve

month

to

3.8

rst

mil-

lion in the fourth month and then decreases to 1.1 million in the

continuous

and

optic

irido-

2

seventh

glial

month.

and

is

connective

decrease

tissue

makes

processes

room

that

for

enter

the

the

increase

optic

in

ner ve.

72

corneal angle.

is membrane appears continuous at gestational

month

7

discontinuous

month

9.

but

68

is

in

the

region

of

the

meshwork

by

band

of

the

of

glial

inner

tissue

and

forms

outer

around

layers

of

the

the

optic

optic

disc,

cup,

at

the

thus

junc-

separat-

73

During

the

last

few

weeks

before

birth,

splits

occur

between cells in the membrane, and the size and number of these

splits

A

tion

increase

rapidly

because

of

the

increase

in

the

size

of

the

ing

the

potential

intraretinal

space

from

the

bers

of

the

optic

8

nerve;

this

Ganglion

tissue

cell

will

axons

become

ll

the

the

intermediary

lumen

of

the

optic

tissue

nerve

of

Kuhnt.

around

ges-

73

anterior

brane

ocular

over

the

structures.

trabecular

e

loss

meshwork

of

continuity

correlates

in

this

mem-

signicantly

with

tational

week

10

(Fig.

9.19)

and

grow

toward

their

termination

2

in

the

lateral

geniculate

nucleus.

Myelination

of

the

axon

begins

69

an

increase

in

the

facility

of

aqueous

outow.

Persistence

of

the

uninterrupted endothelial membrane over the meshwork (Barkan

73

membrane)

can

be

a

causative

factor

in

congenital

during

lateral

the

h

month

geniculate

of

nucleus.

gestation

once

Myelination

the

ber

reaches

the

reaches

chiasm

the

dur-

74

glaucoma.

ing

the

seventh

month,

the

optic

nerve

by

the

end

of

the

eighth

2

month, and the lamina cribrosa by one month aer birth.

Vitreous

e

In gen-

eral, no myelin continues into the retina past the lamina cribrosa.

presence

of

the

developing

lens

is

essential

for

vitreous

lls

normal

Myelination

of

the

75

accumulation

of

vitreous.

optic

nerve

bers

continues

to

increase

until

76

e

primar y

the

vit-

3

years

aer

birth.

e

optic

nerve,

from

globe

to

chiasm,

is

76

reous

space

early

mesenchymal

developing

in

and

lens

development

ectodermal

and

retina,

(see

origins.

as

well

Fig.

9.8)

Fibrils

as

and

derived

components

has

both

from

from

the

approximately 2.5 cm at birth and nearly doubles by age 15 years.

is

corresponds

to

the

increasing

size

of

the

skull.

the

68

degenerating

hyaloid

system,

will

form

the

primar y

vitreous.

CLINICAL

As

the

secondar y

vitreous

develops,

produced

by

retina

and

primar y

vessels,

hyalocytes

vitreous

thus

from

within

forming

the

the

the

primar y

region

of

vitreous,

The

the

funnel-shaped

it

encloses

atrophying

Cloquet

COMMENT: Emmetropization

neural

8

globe

continues

as

long

of

the

as

there

is

with

its

apex

at

the

optic

disc

and

its

base

at

canal.

the

refractive

is

well

formed

by

the

fourth

month.

It

persists

in

after

birth,

and

between

the

the

eye

length

will

of

become

the

eye

emmetropic

and

the

components.

Although

this

growth

is

under

the

genetic

power

control,

is

posterior

77

process.

lens,

grow

coordination

hyaloid

visual experience

zone,

to

the

adult.

that

provides

feedback

for

normal

growth

may

inuence

this

CHAPTER

Fig.

9.20

Light

embryo.

inner

of

Ocular

micrograph

Fused

layer

9

eyelids

the

optic

are

cup

of

an

seen.

is

an

155

Embryology

eye

The

of

a

2.5-month

human

mushroom-shape

of

the

artifact.

80

eyelids,

and

the

eyelashes

start

to

form

at

gestational

week

12

81

while

the

eyelids

are

still

fused.

Apoptosis

and

keratinization

78

of

the

Other

epithelial

cells

potential

may

theories

be

responsible

suggesting

for

causes

the

of

80

disjunction.

eyelid

separation

include lipid production from the meibomian glands or traction

78

Fig.

9.19

embryo

opment

Section through the eye and orbit of a 48-mm human

(approximately

of

Copyright

the

Human

1964,

British

9.5

weeks).

Eye.

New

Medical

(From

Y ork:

Mann

Grune

&

I.

The

by

the

eyelid

muscles.

Devel-

Stratton;

1994.

Orbit

Association.)

Orbital

fat

and

connective

tissue

are

derived

from

neural

crest

2

cells.

e

rst

evident

orbital

bone

is

the

maxilla

at

6

weeks.

e

frontal, zygomatic, and palatine bones are apparent at week 7. e

DEVELOPMENT

OF

OCULAR

lesser wing of the sphenoid bone and the optic canal are present at

ADNEXA

week

Eyelids

8,

the

greater

wing

of

the

sphenoid

2

10,

and

the

and

wings

Early in the second gestational month, folds of surface ectoderm

ossify

lled with mesenchyme begin to grow toward one another ante-

nective

tissue

fuse

rior

muscle

of

join

by

the

at

week

eighth

bone

is

evident

at

week

82

16.

Most

month;

of

the

however,

orbital

bones

nonossied

con-

2

lids.

to

the

Early

developing

formation

cornea.

of

these

ese

folds

folds

can

be

will

become

seen

in

Fig.

the

eye-

9.8.

e

remains

Müller,

present

which

in

covers

the

the

orbit

at

orbital

birth.

oor

e

while

orbital

the

infe-

rior orbital bones are forming, still covers nearly half of the oor at

2

upper

eyelid

fold

is

from

the

frontonasal

process,

and

the

lower

birth.

e angle between the orbits early in development is approx-

78

fold

is

from

the

maxillar y

process.

e

eyelid

margins

meet

imately 180 degrees, decreases to 105 degrees at 3 months, and is 71

2

and

fuse

during

ment

and

oped

(Fig.

the

remain

early

fused

78

part

until

of

the

the

third

eyelid

month

of

structures

develop-

have

devel-

degrees

at

a

at

faster

birth

rate

and

than

68

the

degrees

orbit,

in

adulthood.

accounting

79

for

e

globe

increased

enlarges

proptosis

at

2

9.20).

Two

layers

of

epithelium

cover

the

anterior

birth

compared

with

the

adult.

e

globe

reaches

its

adult

size

by

3

surface

to

become

epidermis

and

one

layer

lines

the

inner

sur-

age 3 years, but the orbit is not of adult size until age 16 years.

78

face

to

ture

become

evident

conjunctiva.

within

the

e

eyelids,

orbicularis

appearing

is

the

within

rst

a

struc-

week

of

Extraocular

Muscles

78

eyelid

folds

fusion.

grows

Surface

into

the

ectoderm

developing

78

tarsal

conjunctiva,

the

the

margins

plates

to

of

form

the

eyelid

meibomian

e extraocular muscles are

e

muscle

cells

are

derived

of

mesenchymal

from

mesoderm,

origin

(Fig.

whereas

9.21).

the

con-

80

glands late in the third month.

and

from

8

e epithelial layers of the skin

hair

follicles

and

glands

and

cilia,

and

the

meibomian

nective

tissue

Extraocular

components

muscles

once

originate

were

from

thought

neural

to

crest

develop

62

cells.

in

stages,

27

glands,

face

Zeis

glands,

ectoderm;

the

tarsal

plates,

of

Moll

all

orbicularis,

develop

levator,

78

muscle

eyelids

allows

of

Müller

isolates

develop

the

mechanical

from

developing

support

eye

from

the

ocular

and

sur-

tarsal

rst

but

posteriorly

recent

near

the

investigation

orbital

apex

suggests

80

mesenchyme.

while

from

and

that

then

muscle

grow

for ward,

origin,

belly,

and

83

Fusion

amniotic

structures

of

uid

are

the

and

form-

insertion

by

at

cranial

develop

ner ve

approximately

simultaneously.

III

are

day

derived

26.

e

e

from

lateral

the

muscles

rst

rectus

pair

muscle,

inner vated

of

somites

inner vated

78

ing.

Formation

of

meibomian

glands

requires

fusion

of

the

by

cranial

ner ve

VI,

develops

from

the

mesenchyme

of

the

CHAPTER

156

9

Ocular

Embryology

GENETIC

With

ing

the

current

interest

exponentially

tifying

by

IMPLICATIONS

genes

which

and

expressed

cellular

in

the

human

numerous

by

genome,

studies

ocular

characteristics

are

structures

and

the

eld

exploring

and

the

processes

are

is

grow-

and

iden-

mechanisms

governed

by

those genes. e PAX6 gene is considered the master control gene

9,87–91

and is necessary for normal development of ocular structures.

Mutations

of

PAX6

may

cause

anophthalmia,

microphthalmia,

aniridia, coloboma, optic nerve hypoplasia, foveal hypoplasia, and

87,89

cataracts.

ple

lens

An increase in PAX6 in mice is associated with multi-

defects,

including

abnormal

ber

shape

and

ber-to-ber

57

and

ber-to-cell

corneal

and

interactions.

conjunctival

e

PAX6

epithelium

and

gene

may

is

expressed

regulate

in

and

the

main-

48

tain cell structure.

It also has a role in the proliferation and main-

48,88

tenance

of

corneal

and

conjunctival

stem

cells

and

is

required

48,80

Fig.

9.21

neal

Light

layers

are

micrograph

present.

of

a

Pigment

45-mm

is

pig

evident

embryo.

in

the

The

outer

cor -

layer

for eyelid formation and retinal neurogenesis.

Other

of

genes

essential

in

eye

development

include

RAX,

48,87,89,92

the

are

optic

cup.

The

eyelids,

extraocular

muscle,

and

optic

ner ve

evident.

PAX2,

LHX2,

SIX3,

and

PIT X2.

e

gene

called

RAX

is

thought to be a major factor in the early stages of ocular develop-

ment, and mutations in RAX have been identied as causative in

87,89,92

maxillomandibular

muscle,

area

inner vated

by

at

about

cranial

day

27.

ner ve

e

IV ,

is

superior

derived

oblique

from

the

some

have

cases

been

of

anophthalmia.

implicated

in

Mutations

optic

ner ve

head

8

clearly

visible

by

week

8

the

PAX2

gene

because

87,93

second pair of somites at day 29.

are

in

colobomas

All extraocular muscles bellies

and

tendons

are

macroscopically

of

failure

result

in

of

the

optic

formation

2

ssure

of

an

to

close.

optic

LHX2

vesicle

that

mutations

does

not

may

transition

87

visible by the h month.

e common tendinous ring forms in

to

an

optic

cup.

Mutations

of

SIX3

can

cause

midline

decits

2

the

sixth

month.

e

tendinous

sheaths

at

the

scleral

insertions

that

include

cyclopia.

PIT X2

is

required

for

extraocular

muscle,

48,92

are

located

posterior

to

the

adult

insertion

points,

not

reach-

cornea,

and

iris

development.

2

ing

the

born

adult

location

exhibits

early

years,

poorly

indicating

developed

and

early

opment

normal

until

20

months

coordinated

that

the

visual

eye

aer

birth.

e

movements

extraocular

experience

muscles

can

new-

during

are

inuence

not

the

the

fully

devel-

A

myriad

of

speculation

surrounds

genes

and

the

tures

include:

ser ving

the

clusterin

might

nonkeratinized

be

state

the

of

factor

corneal

essential

epithelial

84

of

binocular

eye

e

may

main

lacrimal

also

age

gland

is

thought

thickening

at

to

the

develop

superior

from

epithe-

fornix

during

to

third

gestational

provide

may

some

provide

corneal

protection

some

epithelium;

atherosclerosis

degeneration

2

the

pre-

against

protection

apoptosis;

and

against

the

gene,

ultraviolet

dam-

94

System

lial-mesenchymal

for

cells

94

movements.

ALDH3,

Nasolacrimal

proteins

they encode. Some interesting theories concerning ocular struc-

and

there

drusen

through

the

may

be

formed

same

or

a

in

connection

age-related

similar

between

macular

extracellular

matrix

95

month.

S ome

investigators

question

this

genes;

and

genes

usually

associated

identied

in

the

aqueous

outow

tissues

are

85

origin

and

suggest

a

neural

crest

origin.

Despite

traditional

with

lymphatic

tissue,

perhaps

suggesting

95

thinking

more

that

than

80%

2

2

days

of

e

the

of

lacrimal

infants

have

a

is

not

normal

functional

basal

tear

at

ow

birth,

additional

within

In

function

addition

to

for

the

trabecular

providing

further

meshwork.

information

about

embryo-

86

life.

logical development, gene expression proling can further explain

nasolacrimal

surface

gland

ectodermal

drainage

cells

that

system

develops

becomes

buried

from

below

a

cord

the

of

maxil-

cellular

physiology,

structures.

as

well

Identifying

as

and

pathophysiology

understanding

aecting

the

genetic

ocular

regula-

78

lar y

mesenchyme

is

bifurcates

to

rst

form

seen

the

in

the

puncta

third

and

gestational

canaliculi.

e

month.

canaliculi

tion of normal cellular process brings us closer to understanding,

treating,

and

possibly

preventing

ocular

disease

and

dysfunction.

become patent in the fourth to h month, but the puncta remain

78

occluded

until

the

seventh

month,

aer

the

eyelids

separate.

REFERENCES

BLOOD

VESSEL

PERMEABILITY

AND

BARRIERS

1.

Moore

Birth

e

blood-retinal

and

blood-aqueous

barriers

are

with

the

development

of

the

tight

junctions

Before

5th

We

ed.

Are

Born:

Essentials

Philadelphia:

of

Embr yolog y

Saunders;

and

1998.

recognizable 2.

early

KL.

Defects.

formed

in

T awk HA, Dutton JJ. Embryologic and fetal development of the hu-

the man orbit. Ophthalmol Plast Reconstruct Surg. 2018;34(5):405–421.

RPE,

the

nonpigmented

ciliar y

epithelium,

and

the

capillaries 3.

of

the

ability

iris

in

capillaris

and

the

retina.

Fenestrations

capillaries

also

are

of

evident

the

that

ciliar y

early

in

the

establish

processes

vessel

and

gestational

the

perme-

chorio-

period.

Cook

eye

CS,

and

dations

Ozanics

its

of

Williams

V ,

adnexa.

Clinical

&

Jakobiec

In:

FA.

Tasman

W ,

Ophthalmolog y,

Wilkins;

2013.

Prenatal

Jaeger

vol

1.

development

EA,

eds.

of

Duane’s

Philadelphia:

the

Foun-

Lippincott

CHAPTER

4.

Barishak

ed.

YR.

Embr yolog y

Developments

5.

Barber

6.

Wang

A.

X,

K,

of

the

eye

and

Ophthalmolog y.

Embryolog y

Xiong

posterior

in

Lu

pigmented

of

L,

the

Human

etal.

its

New

Eye.

adnexae.

Y ork:

St

Louis:

Developmental

epithelium

of

iris.

Cell

In:

Karger ;

Mosby ;

origin

of

Biochem

30.

Straub,

31.

1995.

Morrison

iris

DA,

heterochromia:

a

DR,

Fleck

common

BW .

Iris

association.

coloboma

Arch

Barishak

Karger ;

9.

10.

33.

Embryolog y

of

the

Eye

and

its

Adnexae.

New

J

T.

genes

Ophthalmol.

Harrington

analysis

toxin

of

L,

involved

the

morphogenesis

of

the

34.

eye.

1993;37(3):215(Abstract).

Klintworth

ocular

transgenic

in

GK,

Seror

morphogenesis

mice

TE,

in

undergoing

etal.

alpha

35.

Developmental

of

the

lens.

Dev

36.

Biol.

1991;148(2):508.

12.

Coulombre

thalmol

13.

Gunhaga

viding

Philos

14.

AJ.

Vis

L.

new

Marshall

ment

UK.

16.

of

J,

CS,

its

Smelser

GK.

lens

Lovicu

22.

lens

V ,

Saha

Sci.

Invest

Oph-

37.

lens

M,

of

embryonic

etal.

early

Recent

formation.

Rother y

and

in

induction

38.

development.

S.

zonules.

progress

Eye.

e

1992;6(pt

anatomy

Transact

on

and

In:

T asman

Embr yolog y

Vis

JL,

Sci.

factors

in

R

Y ,

O’Rahilly

e

R.

AJ.

Science.

JW ,

de

Lond

Lovicu

eye

EA,

development

2):117.

eds. Duane’s

Philadelphia:

morpholog y

of

39.

of

the

the

lens.

FJ,

lens.

B

development:

RU.

development:

Biol

Sci.

McAvoy

insights

role

from

the

Planar

cell

polarity

in

of

the

human

lens.

43.

GA,

DS.

Development

vasculatures

in

the

fetal

of

the

human

hyaloid,

eye.

Prog

44.

the

Exp

Eye

45.

46.

choroidal

Ret

Eye

24.

Mutlu

F ,

tunica

vasculosa

Selvam

in

25.

S,

Sun

Y ,

Smith

diseases.

26.

W ar wick

the

27.

Eye

Mann

and

I.

LEH.

Rev

Prog

Retinal

Vision

7th

of

the

Ophthalmol.

M.

Ret

Retinal

Eye

Res.

vasculature

Sci.

ed.

of

of

hyaloid

system

and

the

eye.

Human

47.

Sharma

S,

Cook

ed.

Mosby ;

MD,

PG.

eye

to

the

guidance.

Photoreceptor

electron

Müller

A.

brain:

Brit

J

the

Ophthalmol.

morphogenesis

microscopic

study.

in

the

Anat

Louis:

Spira

Ehinger

PL,

Mosby ;

Br ingmann

AW .

A,

str uc ture,

EJ.

Alm

cells

vivo

of

their

in

retinal

possible

vitro.

layers

Histol

in

roles

Histo-

prenatal

human

Early

development

of

the

human

1972;7:472.

Development

A,

and

and

2016;161:29–35.e1.

Ophthalmol.

RK,

glia

in

Development

Ophthalmol.

Kaufman

O’Connor

eds.

Adler’s

and

structure

Physiolog y

of

of

the

the

Eye.

retina.

10th

ed.

2003:319.

Syrb e

S,

G ör ner

f unc t ion

AR,

Wilson

associated

Yuodelis

C,

of

and

with

K,

etal.

e

de velopment.

CM,

Fielder

preterm

Hendrickson

the

Hendrickson

of

the

Vajzovic

L,

human

A.

AR.

birth.

A

fovea

A,

Possin

human

D,

fovea

pr imate

Prog

Ret

fo-

Eye

Res.

Ophthalmological

Eye.

qualitative

during

prob-

2007;21:1254–1260.

and

quantitative

development.

Vision

Res.

Vajzovic

from

L,

etal.

Histologic

midgestation

to

develop-

maturity.

Am

J

2012;154(5):767–778.e2.

Hendrickson

human

fovea:

tomography

Jeer y

G.

Provis

e

of

JM.

Eye

AE,

correlation

ndings

retinal

the

O’Connell

of

with

pigment

neural

retina.

Development

Res.

Gariano

RV ,

etal.

spectral-domain

histolog y.

Am

J

Maturation

optical

of

coher-

Ophthalmol.

of

epithelium

Eye.

the

as

a

developmental

1998;12:499.

primate

retinal

vasculature.

Prog

2001;20(6):799.

RF .

Special

England).

features

of

human

retinal

angiogenesis.

Eye

2010;24(3):401–407.

Rivera JC, Sapieha P , Joyal J-S, etal. Understanding retinopathy of

vasculature

development

48.

development

In:

Wol ’s

Saunders;

Eye.

New

Anatomy

Grune

the

fetal

50.

&

Tisdale

of

of

1976:418–462.

Y ork:

o c u l ar

C.

Normal

System

of

and

abnormal

Ophthalmolog y,

development.

Embryolog y,

vol

In:

51.

la

opment

of

the

ciliar y

portion

of

the

optic

body :

cup

2013;198(2):149–159.

in

C,

Vicente

morphological

the

human.

A,

changes

Cells

Tissues

etal.

in

Devel-

the

distal

Organs.

development:

Mol

Brow n

Biol

NL.

de velopment.

52.

KM,

Wulle

Translat

Eye

dierent

Sci.

cells

Topic

from

a

common

2015;134:43–59.

org ano gene s is:

Cur r

the

fetal

Spurr-Michaud

KG.

structures

Invest

Ophthalmol

Electron

D e velop

Ruprecht

human

1974;13:923.

S.

Fine

Clin.

and

Ophthalmol

development

Rodrigues

the

a

h i e r arch ic a l

vie w

Biol.

2019;132:

of

corneal

the

Vis

Sci.

etal.

Development

in

rabbit

and

human

1988;29(5):727.

structure

of

the

Descemet’s

Vis

KW ,

M,

epithelium

of

the

developing

1975;15(1):19.

microscopy

endothelium

KG,

SJ,

of

Ophthalmol

Mockel-Pohl

Intl

Invest

Wulle

of

AS,

corneas.

Zinn

eye.

Cuadra-Blanco

JB,

anchoring

corneal

3.

1963.

de

Corneal

Prog

351–393.

and

49.

Eugene

PY .

Miesfeld

of

2018;63:1–19.

in

Lwigale

cornea.

S,

Peces-Peña

S.

dierentiation

MJ,

progenitor.

1964;71:102.

2018;4:101–122.

Philadelphia:

the

fetal

1964.

Duke-Elder

Louis:

Arch

Development

Orbit.

structure

Fruttiger

Duke-Elder

St

29.

T,

Development

Stratton;

28.

e

disease.

Ann

R.

IH.

lentis.

Kumar

and

the

axon

343–353.

Leopard

health

cell

prematurity: update on pathogenesis. Neonatology. 2011;100(4):

Res.

2018;62:58–76.

23.

J

Can

(London,

McLeod

retinal

Am

regulator

1975;2:93.

Lutty

Connecting

ganglion

scanning

Layer

J

Ret

eye.

of

regeneration.

2012;154(5):779–789.e2.

of

2011;7(3):191–201.

development

a

Hollenberg

the

2011;366(1568):1204–1218.

JW .

E,

Ophthalmol.

elongation

the

DW .

of

Wadhwa

retina.

ence

Understanding

determinants

and

2003;22(4):483.

1998;13(2):531.

ment

1963;142:1489.

Iongh

Organogenesis.

prenatal

41.

1994.

Invest

ber

development

1973;12:295.

1986;26(6):847.

eye

42.

Lens

K,

Hendrickson

lems

40.

Soc

Foundations

Lippincott;

Molecular

sur vival,

the

Sci.

2018;66:49–84.

the

1965;4:398.

embr yonic

Soc

Jaeger

1.

and

Coulombre

McAvoy

Trans

W ,

vol

Prenatal

A.

of

Vis

1998;252:133.

analysis

FA.

basis

study

Ophthalmol

Cellerino

157

Embryology

microscopic

Invest

development,

pathol.

ve a:

develop-

Ophthalmol

A,

retina

St

pro-

2011;366(1568):1193–1203.

MS,

Jakobiec

orientation.

FJ,

Sugiyama

and

JJ,

model

determination

Biol

embr yonic

mammalian

Res.

cell

B

Ophthalmology,

Coulombre

Philos

21.

of

adnexa.

growth

20.

into

Henr y

Ozanics

Clinical

and

19.

morphogenesis.

cells.

during

In:

classical

Lond

human

Ophthalmol

18.

a

Beaconseld

the

ocular

1982;102:423–440.

Cook

and

17.

of

Soc

RM,

mechanisms

15.

lens:

insights

R

of

1969;8:25.

e

Trans

Grainger

Regulation

Sci.

Res.

retina:

Willbold

retina.

A-cr ystallin/diphtheria

ablation

Electron

cell

Sretavan

Narayanan

Record.

e

Eye

SF ,

human

Y ork:

2001.

Matsuo

Kretz

Ocular

2003;87:639.

Ophthalmol.

Graw J. Eye development. Curr T opic Develop Biol. 2010;90:343–386.

Jap

11.

YR.

S,

ganglion

Ret

Oster

GK.

Müllerian

molecular

with

2000;118(11):1590.

8.

Smelser

Isenmann

Prog

Biophys.

32.

FitzPatrick

S,

retinal

retinal

the

2015;71(2):1067–1076.

7.

Uga

of

1992.

9

Sci.

development

of

the

of

the

human

1972;11:897.

Windrath

cell

fetal

membrane

LC.

junctions

endothelium.

Electron

in

Invest

the

microscopy

embr yonic

Ophthalmol

Vis

and

Sci.

CHAPTER

158

53.

Lesueur

L,

Arne

ultrastructural

premature

JL,

9

Embryology

Mignon-C onte

changes

infants’

Ocular

and

in

the

M,

etal.

Structural

developmental

children’s

corneas.

process

Cornea.

and

73.

of

1994;

Bahn

CF ,

dothelial

74.

Falls

HF ,

Varley

disorders

GA,

based

on

etal.

Classication

neural

crest

origin.

of

corneal

en-

Ophthalmolog y.

Ozanics

and

V ,

M,

Sagun

dierentiation

in

D.

the

Some

aspects

primate.

Exp

of

corneal

Eye

76.

Res.

Wulle

KG,

77.

Richter

development

Graefe’s

57.

of

Arch

D unc an

of

MK,

J.

the

Clin

PAX6(5a)

regu l at ion

Electron

human

Exp

of

lens

corneal

Ophthalmol.

Kozmi k

in

microscopy

Z,

c el ls

(a lpha) 5 ( b et a) 1

the

epithelium.

early

embr yonic

Albrecht

Von

K,

e t  a l.

resu lts

in

i nteg r i n

Lutty

GA,

choriocapillaris.

59.

ML,

scopic

obser vations

human

60.

Eye

Mund

Wulle

system

of

Am

e

the

J

Baba

T,

(London,

Rodrigues

eye.

KG.

T,

MM,

on

the

O verex pre ss i on

c at arac t

Development

BS.

and

J

78.

up-

pigmented

Ophthalmol.

C ell

S ci.

layers

of

the

electron

of

the

in

human

Loewenfeld

Applications.

62.

Gage

and

JE,

e

Pupil:

Boston:

Rhoades

mesoderm

in

Anatomy,

the

human

and

eye.

Physiolog y,

80.

developing

drainage

Adv

and

Butter worth-Heinemann;

W ,

Prucka

the

SK,

etal.

mammalian

Fate

eye.

64.

Tamura

Smelser

of

Carlson

BM.

Louis:

65.

T,

muscles

N,

GK.

iris.

81.

Ophthalmol.

membrane:

Ophthalmol.

Embryolog y

G.

the

stage

1999.

maps

Invest

of

of

83.

neural

Ophthalmol

crest

Vis

Sci.

the

sphincter

and

Electron

ne

84.

Edelhauser

Alm

A,

of

the

of

the

membrane.

Ubels

Adler’s

JL.

Cornea

Physiolog y

of

studies

white

Invest

and

the

Biolog y.

on

strands

the

of

Ophthalmol

sclera.

Eye.

St

Burian

ment

68.

69.

the

Braley

angle

1956;53:439.

GK,

Ozanics

work

primate

in

Rodrigues

MM,

BJ,

meshwork

J

pupil-

SI,

In:

10th

the

BJ,

Kupfer

eyes.

its

C,

eye.

St

Invest

RC.

the

J.

of

of

the

the

St

of

Vis

F ,

R,

Call

K.

for

origin

the

RC.

In:

R,

Mosby ;

e

Shields

Sci.

Mosby ;

the

develop-

eye.

88.

BS,

Sevel

D.

Porter

trabecular

mesh-

VIII

antigen,

of

human

of

90.

Li

Ophthalmol

Vis

the

MB,

91.

92.

G,

Sci.

etal.

defocus

of

of

visually

MH,

ocular

Postnatal

develop-

growth

of

the

hu-

2016;30(10):1378–1380.

A,

etal.

opposite

guided

Fouad

human

Y A,

eyelid.

Traboulsi

eyelid

Y ,

etal.

eyelid

anterior

Krupin

T,

trabecular

segment

eds.

outow

1971;10:513.

facility

in

Gene

signs

eye

expres-

reveals

growth.

PLoS

Biol.

etal.

Embr yologic

Ophthal

Plast

and

Reconstruct

EI.

Molecular

development.

biolog y

Ophthal

and

Genet.

Role

and

of

EGF

receptor

meibomian

glands.

signaling

Exp

Eye

on

Res.

Platt

R,

of

J

BE,

the

the

Biolog y

of

Dermatol.

et

al.

Eye.

Orbit.

St

origin

In:

Louis:

of

the

eyelash

hair

follicle:

2016;174(4):741–752.

Kaufman

Mosby ;

human

PL,

Alm

A,

2003.

extraocular

muscles.

1981;88:1330.

Andrade

Alm

Mosby ;

BJ,

of

etal.

Br

Cook

Reappraisal

PL,

CI,

sight.

FH,

A,

Baker

eds.

RS.

Adler’s

e

extraocular

Physiolog y

of

the

muscles.

Eye.

10th

In:

ed.

2003:787.

Tripathi

lacrimal

RC.

Evidence

gland.

Invest

of

neuroectodermal

Ophthalmol

Vis

Sci.

origin

of

1990;31:393.

W ,

Pevny

Xu

F ,

Zhu

J,

limbal

Chem.

JL,

eye

Transcription

cell

and

retinogenesis.

Cold

2012;4(12).

lineage

BM,

Zhang

GA,

Q,

in

Y ang

JM,

Vis

Daniels

What

development

interface

factor

PAX6

development

OH.

the

basic

Genetic

(paired

and

box

disease.

6)

J

regulation

of

2014;86(5):453–460.

e

corneal

PAX6

and

homeobox

conjunctival

gene

epithelia.

1997;38(1):108.

Corneal

Cell

DD.

Genet.

Res.

epithelial

stem

cells:

deciency

2008;4:159–168.

experimental

of

of

the

Sci.

JT.

Stem

Clin

Sundin

throughout

LK.

Eisenstat

development.

regulation.

the

development

Biol.

etal.

stem

Ophthalmol

McLoon

Eye

2015;290(33):20448–20454.

expressed

Secker

L.

Perspect

embr yolog y

extraocular

muscles

and

sciences.

clinical

can

in

teach

us

about

anophthalmia:

Arch

Ophthalmol.

2011;129(8):1077–1079.

93.

94.

e

human

I,

plain

Harbor

Koroma

the

Martinovic-Bouriel

Kinoshita

man

95.

of

J,

England).

B enavente-Perez

AC,

Physiolog y

Zagozewski

is

channels.

glaucoma.

in

human

and

drainage

pathogenesis

of

Xia

of

Gausas

JD,

Tripathi

Biol

89.

Arch

1989.

development

M,

hypodysplasia.

Embr yolog y

Ritch

D,

the

Weber

Burgoa

Adler’s

Spring

PL,

Louis:

human

factor

aqueous

crest

of

embr yonic

enigma

Sires

at

Neural

Zhuo

optical

of

Apt L, Cullen BF . Newborns do secrete tears. JAMA. 1964;189:951–953.

1971;71:366.

Collagen

human

Mechanisms

Heavner

the

Kaufman

ed.

concept

Ophthalmol.

Troilo

to

JL.

86.

1989;107:583.

Louis:

Ross

J

implications

Tripathi

human

new

chamber

development

Foidart

in

A

on

Invest

87.

1980;87:337.

Tripathi

and

Glaucomas.

72.

Katz

Ophthalmol.

Tripathi

of

Paus

Invest

e

Am

immunoglobulins

Tripathi

Am

V .

eyes.

L.

anterior

Smelser

Ophthalmolog y.

71.

Allen

the

Ophthalmol.

and

70.

AE,

of

M,

Abdulhafez

TJ,

of

vertebrate

HM,

of

Dong

the

2003:47.

67.

studies

eyes.

2016;32(6):407–414.

Rubinstein

controls

HF ,

eds.

HA,

StLouis:

85.

Developmental

microscopic

structure

human

1975;15(1):7.

(London,

mechanism

Ophthalmolog y.

dilator

1973;89:332.

and

TV ,

Eye

development

eds.

1971;10:108.

66.

Tawk

an

Clinical

1994:265.

Smelser

disappearing

Development

Arch

Clin.

Meister

ner ve.

response

Kaufman

Human

Mosby ;

Matsuo

lar y

the

microscopic

in

1971;10:252.

Coulombre

morphogenesis

2005;46:4200–4208.

63.

in

genetics

82.

IE.

angle

2016;37(3):252–259.

micro-

1972;26:296.

61.

electron

2017;163:58–63.

productive

the

SL,

optic

Surg.

1972;73:167.

of

humor

and

AJ,

Tkatchenko

fetal

2010;24(3):408–415.

Light

Sci.

Scanning

iridocorneal

2018;16(10):e2006021.

expre ss ion .

England).

Fine

development

aqueous

etal.

T.

the

Ophthalmol

bidirectional

79.

Hasegawa

Int

Bernstein

sion

1978;209(1):39.

Cvek l ov a

f ib er

of

2000;113:3173.

58.

Coulombre

man

1976;22:305.

56.

Vis

of

T rachimowicz RA. Review of embryology and its relation to ocular

ment.

Rayborn

scleral

Jerndal

disease in the pediatric population. Optom Vision Sci. 1994;71(3):154.

75.

1984;91:558.

55.

HA,

development

Ophthalmol

13(4):331.

54.

Hansson

the

Wistow

gene

S,

ocular

G.

Am

Adachi

surface

e

2006;25:43–77.

in

B enachi

Med

W ,

A.

Genet.

PAX2

Sotozono

Bank

human

project

and

mutations

in

fetal

renal

2010;152A:830–835.

C,

epithelium. Prog

NEI.

expression

J,

J

etal.

Ret

for

Characteristics

Eye

ocular

rodent

eye

Res.

of

the

hu-

2001;20(5):639.

genomics:

tissues. Prog

data-mining

Ret

Eye

Res.

10

Bones

e

skull

can

be

divided

into

two

parts:

the

cranium

and

the

face.

Each

e cranium consists of two parietal bones, the occipital bone, two

large,

temporal

shaped

bones,

the

sphenoid

bone,

and

the

ethmoid

bone.

e

face is made up of two maxillary bones, two nasal bones, the vomer,

the

two

and

inferior

zygomatic

conchae,

bones,

two

and

lacrimal

the

bones,

mandible.

two

e

palatine

single

bones,

frontal

bone

two

is

a

part of both the cranium and the face.

In

general,

immovable

dibular

the

bones

joints.

joint,

e

which

bones.

Air-lled

several

of

the

of

the

attaches

cavities

is

the

called

unite

the

at

sutures

movable

mandible

sinuses

are

that

form

temporoman-

to

the

temporal

contained

within

bones.

reader

a

is

more

detailed

advised

to

presentation

have

a

skull

of

the

available

orbital

for

bones.

reference

e

while

process,

and

and

articulations

between

bones

and

identifying

foramina

ssures.

aspect,

of

the

and

paired

cranium

other

bone

the

inferiorly

sphenoid

and

men

with

e

in

ebellum

at

the

bones,

is

inner

which

lie.

portion

internal

and

temporal

roof

and

suture,

with

and

e

bone

sides

articulate

midline,

suture.

forms

of

the

the

with

and

the

of

with

the

parietal

posterior

found

surface

10.3

on

of

are

or

cavity.

inion,

midline

the

the

(Fig.

inferior

bone

the

each

occipital

the

bone

greater

shows

the

inner

with

aspect

A

is

e

the

the

single

The

inion,

frontal

(Fig.

the

useful

landmark

just

in

the

portions:

to

processes

the

extends

inner

ear

zygo-

within

structures.

from

is

bone

zygomatic

form

project

forms

parietal

the

a

wedge-

portion

the

portion

and

the

of

At

the

top

of

the

infe-

stylomas-

skull,

for

of

superior

the

and

oor

frontal

it

the

10.3).

portion

and

Inferiorly,

bone,

the

anteriorly

entrance

anterior

the

on

and

(see Fig.

cavity,

bones.

ethmoid

an

cavity

the

cranial

parietal

bone

superiorly

provides

forms

the

occipital

cranial

the

bone,

the

runs

and

the

bone

oor

sphenoid

with

into

10.4).

with

bones,

cavity

fossa

aspect

the

where

on

e

of

of

skull

the

of

lobes

the

temporal

the

exter-

large

fora-

occipital

of

cranial

the

cranial

bones,

cer-

oor.

parietal

bone.

portion

e

the

outer

to

the

the

part

bone

articulates

placement

of

the

of

the

electrodes

occipital

used

to

cortex,

record

a

is

a

visual

the

e

the

bones

bones.

in

is

the

nasal

lacrimal

surface

forms

frontal

sinuses

are

bones,

bones.

the

the

cranial

anterior

cranial

lobes

located

of

maxillar y

of

the

within

cerebral

the

ante-

bone.

a

single

articulates

form

the

inner

bone

which

frontal

bone

to

e

frontal

frontal

and

with

the

bone,

with

base

of

the

the

the

body

occipital

cranium

of

which

bone

and

(see Fig.

lies

the

10.3).

e sphenoid bone joins the zygomatic bones to form the lateral

walls

of

the

articulates

orbits.

with

Anteriorly

the

and

maxillar y

inferiorly,

and

palatine

the

sphenoid

bones,

bone

superiorly,

it

articulates with the parietal bones, and anteriorly and superiorly,

it

articulates

sion

on

bone,

the

the

pituitar y

bone.

pole

lie.

of

sphenoid

temporal

articulates

10.3),

midline

hollow,

posterior

of

Fig.

rior

the

the

(see

it

zygomatic

hemispheres

wing

posterior

the

aspect

the

of

and

portion

frontal

COMMENT: Inion

located

bone

process

two

canal

portion

arter y

anterior

face

Two

CLINICAL

carotid

petrous

articu-

prominence,

found

10.2).

forms

depressions

articulates

sphenoid

posterior

cranial

protuberance,

bone

middle

these

with

projection,

petrous

styloid

articulates

e

carotid

cranium,

in

there

Fig.

occipital

the

bones

the

lambdoid

the

oor

magnum

fossa,

along

coronal

bone

occipital

bone.

the

the

form

parietal

bone.

posterior

surface

e

suture

at

at

occipital

external

e

sagittal

anteriorly

e

nal

the

bones

10.1).

posteriorly

bone

lates

at

the

and

two

thickened,

squamous

zygomatic

e

of

a

Orbit

CRANIUM

parietal

(Fig.

houses

e

and

articulates

anterior

the

10.1).

between

Inferoanteriorly,

e

with

process

skull.

through

with

THE

and

An

composed

portion;

portion.

and

bone.

Fig.

is

and

toid foramen, through which the facial ner ve exits the skull. e

of

OF

bones

petrous

cranium

(see

Skull

squamous

articulates

arch

articulates

BONES

the

mastoid

rior

the

the

cranium

e

reading this chapter, particularly for distinguishing the relation-

ships

of

the

temporal

sphenoid

petrous

Aer a brief description of the bones of the skull, this chapter

presents

the

the

the

plate,

area,

side

matic

skull

exception

of

at

of

body

(see

with

A

forming

pairs

e

Fig.

ethmoid

cranial

hypophyseal

gland.

and

the

superior

the

of

are

10.3).

e

lesser

the

(or

the

body

sinus

sella

the

from

and

of

of

e

the

turcica),

the

depres-

sphenoid

houses

sphenoid

are

body

the

smaller

wings

bones.

body

the

bone

is

cavity.

from

project

superior

frontal

of

the

project

wings

more

of

sphenoid

wings

lesser

fossa

portion

and

surface

of

anterior

than

the

attached

to

the

sphenoid

aspect

greater

the

of

the

wings

body

by

evoked potential. This electrodiagnostic test records responses from the visual

small

cortex.

Clinical

applications

include

the

determination

of

visual

acuity

in

a

roots

unable

conduction

to

in

respond

the

to

patient

the

with

typical

eye

suspected

chart

and

multiple

the

assessment

of

struts.

e

gap

between

the

lesser

wing

and

the

pa-

sphenoid tient

or

body

forms

the

optic

foramen

(canal)

through

which

impulse

the

optic

ner ve

the

frontal

exits

the

orbit.

e

lesser

wings

articulate

with

sclerosis.

and

ethmoid

bones.

159

160

CHAPTER

10

Bones

Squamous

of

the

suture

Skull

and

Orbit

Ver tex

Coronal

Parietal

suture

bone

Frontal

bone

Pterion

Glabella

Sphenoid

T emporal

bone

Nasal

bone,

greater

bone

Infraorbital

foramen

Zygomatic

bone

Occipital

Maxilla

bone Mastoid

process

Exter nal

auditor y

meatus

Styloid

process

Mental

foramen

Zygomatic Mandible arch

Fig.

10.1

Lateral

Principles.

Sagittal

St

view

Louis:

of

the

Mosby;

skull.

(From

Mathers

LH,

Chase

RA,

Dolph

J,

etal.

Clinical

Anatomy

1996.)

suture

Parietal

bone

Lambda

Lambdoidal

Occipital

T emporal

suture

bone

bone

Asterion

Exter nal Emissar y occipital

foramen

protuberance

(inion)

Styloid

Maxilla

process

Pter ygoid

hamulus

Mandible

(interior

Fig.

10.2

Posterior

Anatomy

Principles.

view

St

of

Louis:

the

skull.

Mosby;

(From

1996.)

Mathers

LH,

Chase

RA,

Dolph

J,

surface)

et al.

Clinical

wing

CHAPTER

Anterior

10

Bones

of

the

fossa

Skull

and

Cribrifor m

ethmoid

Sphenoid

lesser

Orbit

plate,

bone

bone,

wing

Middle

meningeal

a.

Anterior

clinoid

process

Foramen

lacerum

Foramen

rotundum

Foramen

ovale

Foramen

spinosum

Carotid

canal

Middle

fossa Inter nal

Petrous

Hypoglossal

ridge

canal

of

trigeminal

Jugular

ganglion

foramen

Sigmoid

Parietal

meatus

ridge,

temporal

Position

auditor y

sinus

Foramen

magnum

Posterior

fossa

bone

T ransverse

sinus

Occipital

Fig.

10.3

ciples.

bone

Floor

St

of

Louis:

the

skull.

Mosby;

(From

Mathers

LH,

Chase

RA,

Dolph

J,

etal.

Clinical

Anatomy

Prin-

1996.)

Coronal

Frontal

suture

bone

Nasion

Nasal

Supraorbital

bones

notch

T emporal

Superior

orbital

fossa

fissure

Zygomatic Infraorbital

bone

foramen

Maxilla

Ramus

Angle

of

Mental

Fig.

10.4

Anatomy

Anterior

Principles.

view

St

of

Louis:

the

skull.

Mosby;

(From

1996.)

Mathers

LH,

Chase

RA,

Dolph

J,

of

mandible

mandible

foramen

et al.

Clinical

161

CHAPTER

162

10

Bones

of

the

Skull

and

Orbit

Sphenoid

Optic

bone

canal

Anterior

Superior

clinoid

process

orbital

fissure

Pituitar y

Foramen

fossa

rotundum Posterior

Foramen

ovale

Foramen

spinosum

Groove

clinoid

for

process

middle

meningeal

a.

Inter nal

auditor y

Jugular

meatus

foramen

T emporal

bone,

squamous

Foramen

Hypoglossal

10.5

etal.

Disarticulated

Clinical

Anatomy

view

of

Principles.

the

St

base

Louis:

of

articulate

mous

e

with

portions

of

pter ygoid

the

and

articulates

each

contributes

ree

frontal

temporal

process

wing

fossa.

the

a

bones,

projects

with

to

bone,

the

parietal

and

from

vertical

shallow

important

the

the

the

of

depression,

foramina

are

zygomatic

base

stem

of

the

the

located

bones,

the

squa-

bones.

palatine

the

skull.

bone;

greater

wing

of

the

two

tal

bone

e

the

of

both

with

ner ve

ing

lar

ner ve

middle

e

of

rated

sides

single

a

the

for

of

midline

box,

the

the

the

box,

by

ethmoid

sphenoid

inferiorly.

lacrimal

of

are

air

and

e

foramen

through

bone

the

spinosum,

the

through

mandibu-

which

the

resembles

plate.

cribriform

olfactor y

parallel

frontal

e

the

rectangular

is

plate

plate,

ner ves

the

which

is

plate,

with

the

the

the

perfo-

e

are

the

with

vomer

maxillar y

It

THE

cheek

two

with

single

the

frontal

nasal

the

bone

named

RA,

Dolph

Fig.

bones.

the

walls

e

the

J,

with

the

the

nasal

of

the

the

bone

the

fron-

suture).

upper

and

the

jaw,

oor

articulates

sphenoid,

maxillar y

of

the

palatine,

bone

form-

sinus.

bridge

of

the

bone,

(see

Fig.

posterior

and

names

cavity,

maxillar y

frontal

palatine

form

ethmoid,

the

the

between

frontozygomatic

bones,

Each

bones

the

the

of

to

suture

the

portion

form

with

forms

the

maxillar y

maxillar y

that

is

lacrimal,

bones

other,

bone

10.4).

nasal,

according

(e.g.,

maxillar y

lateral

(see

nasal

of

or

contains

each

separate

e

the

face

and

bones

located

lacrimal

and

frontal

ere

nose

and

10.4).

part

of

and

with

e

the

maxillar y

articu-

the

frontal

vomer

nasal

bones

is

a

septum.

inferiorly

extends

stem

along

(one

articulates

two

from

e

bone

the

in

with

lateral

each

the

walls

orbit)

is

maxillar y

of

the

the

nasal

smallest

bone,

cavity.

bone

ethmoid

of

bone,

bone.

are

palatine

the

hard

horizontal

runs

along

bones.

palate

plate

the

is

Each

at

the

found

posterior

is

an

back

in

the

aspect

L-shaped

of

the

oral

of

cavity.

the

bone

mouth

nasal

e

that

to

the

verti-

cavity

and

FACE articulates

e

are

connected

zygomatic

frontal,

articulates

cal

OF

Chase

and with the ethmoid bone superiorly. e inferior conchae are

orbit.

BONES

the

orbits

with

single

are

palate,

processes

and

bones.

LH,

maxillae,

zygomatic

e

plate

articulates

and

with

that

10.3).

perpendicular

bone

superiorly

articulate

box

bisects

(see Fig.

perpendicular

from

ethmoid

bones

plates

a

generally

and

the

the

late

separated

cells.

orbital

which

passes.

horizontal

which

and

ovale,

perpendicular

passage

plates

the

the

arter y

ethmoid

orbital

the

and

meningeal

contains

top

passes;

foramen

Mathers

that

two

hard

and

the

face

bones

(Fig. 10.5): the foramen rotundum, through which the maxillar y

passes;

(From

bone

1996.)

greater

pter ygopalatine

in

the

Mosby;

e greater wings project from the lateral aspects of the body

and

magnum

canal

Occipital

Fig.

par t

bone

bones,

forms

maxillae,

the

and

forehead

zygomatic

and

bones

articulates

in

forma-

tion of the face (see Fig. 10.4). e sutures joining adjacent bones

small,

the

with

attened

orbital

maxilla.

oor

the

area

at

pter ygoid

at

the

the

top

process

of

posterior

the

edge

of

the

sphenoid

vertical

of

the

stem

is

orbital

bone.

located

plate

of

A

in

the

CHAPTER

e

paired

zygomatic

bones

form

the

lateral

part

of

and

articulate

with

the

zygomatic

process

Bones

of

the

Skull

and

163

Orbit

the

Orbital cheekbones

10

of

Walls

the

Roof temporal

e

bones

zygomatic

and

with

e

the

form

greater

mandible

shoe-shaped

two

to

bones

the

also

wings

forms

bone

zygomatic

articulate

of

the

the

perpendicular

of

processes,

the

sphenoid

movable

consisting

arches

with

a

the

Fig.

10.1).

bones

bone.

lower

cur ved

(see

maxillar y

e roof is triangular and composed primarily of the orbital plate

of the frontal bone in front (see Fig. 10.7). e lesser wing of the

jaw.

It

is

horizontal

a

horse-

body

and

rami.

sphenoid

the

anterior

may

tact

THE

orbits

of

are

the

bony

skull

extraocular

connective

e

which

orbit

is

at

below

the

margin

roof,

with

small

fossa.

leaving

the

on

either

cranium.

and

orbital

side

ey

of

the

midsagittal

contain

ner ves,

blood

the

globes,

vessels,

and

this

shaped

within

approximately

walls,

angle

parallel

with

as

four-sided

margin

skull.

medial

extended

described

a

orbital

the

and

eral

if

like

anterior

oor,

area

wall

posterior

portion.

e

orbital

plate

dural

only

In

the

covering

an

elderly

periosteal

of

the

adult,

bone

connective

frontal

lobe

of

in

this

tissue

the

in

area

con-

e

and

to

each

pear

each

other

shaped,

and

the

orbital

lateral

posteriorly,

pyramid,

other,

would

(Fig.

having

are

e

at

base

the

the

of

pos-

referred

medial

whereas

form

10.6).

its

apex

walls

walls.

the

to

walls

two

lat-

approximately

e

widest

orbit

has

portion

a

of

the

runs

lesser

slightly

wing

of

the

downward,

sphenoid

and

an

that

oval

is

brain.

e

involved

foramen,

in

the optic

canal, lies between it and the body of the sphenoid (see Fig. 10.7).

is

optic

e

run

90-degree

the

muscles,

is

as

the

cavities

tissue.

terior

been

a

ORBIT

plane

the

cranial

resorb,

small

e

contributes

of the frontal bone is thin in the area that separates the orbit from

gin.

the

Behind

frontal

piece

the

of

foramen

frontal

of

the

the

bone:

bone

the

muscle

roughly

the

aspect

fossa

ridge

of

for

the trochlea,

is

orbital

passes

the

the

apex

is

lacrimal

mm

the

an

to

the

A

mar-

plate

medial

of

in

U-shaped

orbital

the

tendon

pulleylike

orbit.

orbital

indentation

gland.

behind

e

this

of

superior

margin

attached

2

margin.

through

at

of

this

the

approximately

superior

oblique

located

forms

lateral

cartilage,

frontal

is

bone

the

of

aspect

superior

structure.

also

1.5

cm

Floor

1

inside

the

orbital

margin.

mately

two-thirds

extend

to

Each

illar y,

the

orbit

(Fig.

single

bone

depth

orbital

of

the

oor

orbit;

extends

the

to

other

approxi-

three

sides

apex.

is

10.7).

and

e

of

oor

the

is

also

triangular

maxillar y

bone

and

and

is

the

composed

orbital

of

plate

the orbital

of

the

plate

zygomatic

bone in front and the small orbital process of the palatine bone

composed

zygomatic,

bones

the

e

of

sphenoid,

e

take

frontal,

part

in

seven

bones—the

ethmoid,

palatine,

sphenoid,

and

the

formation

frontal,

and

ethmoid

of

both

max-

lacrimal

are

each

a

orbits.

behind

part

of

zygomatic

small,

at

Fig.

the

and

bone.

most

e

area

e

in

the

adult

of

palatine

oor

does

of

orbital

at

the

not

the

reach

bone

of

the

the

the

vertical

is

is

up

the

largest

provided

by

palatine

bone

arm

is

plate

between

maxilla

the

of

orbital

suture

all

makes

remainder

process

of

the

and

the

top

edge

skull,

bone

maxillar y

most

posterior

Oen

the

10.7).

oor,

attened

e Ethmoid

(see

the

and

of

the

the

the

is

a

located

maxilla.

orbital

process

indistinguishable.

way

to

the

apex

and

is

sepa-

bone

rated

sure

from

(see

across

canal,

canal

Fig.

the

bridged

the

a

10.8).

inferior

of

bone,

within

the

inferior

posteriorly

Fig.

the

plate

runs

on

wall

and

from

thin

which

the

10.7

oor

by

opens

below

lateral

facial

the

e

the inferior

infraorbital

orbital

thus

ssure

of

margin

bone

the

as

the

the

s-

runs

anteriorly

is

infraorbital

(Fig.

maxilla

orbital

groove

and

becoming

maxillary

surface

orbital

by

6.3

10.9).

to

infraorbital

8.8

is

mm

foramen

2–4

(see

Fig.

maxilla

10.7).

and

CLINICAL

e

the

inferior

maxillary

orbital

process

COMMENT: Blow-Out

of

margin

the

is

composed

zygomatic

Fracture

of

the

of

the

bone.

Orbit

The orbital rim is strong and can withstand considerable impact. However, a blow

to

the

orbital

orbital

rim

contents

can

cause

resulting

in

buckling

a

sudden

of

the

orbital

increase

in

walls

or

compression

intraorbital

pressure,

of

the

either

of

which can cause a fracture of one of the orbital walls. In the classic blow-out frac-

ture, the orbital rim remains intact. The oor of the orbit is particularly susceptible

Medial

orbital

walls

to such a fracture, which usually occurs in the thin region along the infraorbital ca-

5–8

nal (Fig. 10.10).

Clinical signs and symptoms accompanying this damage include

orbital swelling, ecchymosis, anesthesia of the area innervated by the infraorbital

nerve, Lateral

orbital

and

upward

Fig.

10.6

Angular

relationship

of

the

diplopia

caused

by

restriction

of

ocular

motility

(particularly

noted

in

walls

orbital

walls. The

gaze).

Limitations

in

ocular

motility

are

caused

either

by

bruising

or

he-

medial matoma of the extraocular muscles or by herniation and entrapment of the inferior

walls

are

approximately

were

extended,

parallel

to

each

other.

If

the

lateral

walls muscles, or adjoining fat and connective tissue, within the fracture.

an

approximate

right

angle

would

be

formed.

CHAPTER

164

10

Bones

of

the

Skull

and

Orbit

Supraorbital

notch

Strut

wing

Frontal

from

of

lesser

Body,

sphenoid

sphenoid

bone

Greater

wing,

Maxilla,

sphenoid

frontal

process

Optic

canal

Zygomaticoorbital

foramen

Ethmoid Superior bone orbital

fissure

Nasal

Inferior

orbital

bone

fissure

Zygomatic

Lacrimal

bone

bone

Infraorbital

foramen

Maxilla

Palatine

Fig.

10.7

Clinical

Anterior

Anatomy

view

of

Principles.

the

St

bones

Louis:

of

Mosby;

Lesser

Sphenoid

the

wing

bone

orbit.

(From

Mathers

LH,

Chase

RA,

Dolph

J,

etal.

1996.)

of

the

sphenoid

bone

sinus

Superior

orbital

fissure

Pterygopalatine

Greater

fossa

the

Maxillary

Fig.

10.8

Coronal

computed

tomography

sinus

scan

Inferior

through

orbital

the

fissure

orbital

wing

sphenoid

apex.

of

bone

CHAPTER

Crista

10

Bones

of

the

Skull

and

galli

Frontal Frontal

165

Orbit

sinus

bone

Lamina

papyracea

Zygomatic

bone

Infraorbital

Fig.

Medial

e

b one,

of

the

cess

by

t he

of

t he

t he

of

a

of

t he

t he

b one,

foss a

is

op ens

a

pro cess

of

the

(Fig.

t hat

a

toget her

t he

c anal and

wit hin

t he

wit h

is

t he

b one

t he

par t

on

t he

par t

fossa

bone

Maxillary

tomography

of

of

for

e

t he

t he

the

of

t he

plate

ina

is

b one,

for ming

b one

for ms

sup er iorly

t he

t he

wit h

p oster ior

p osteri or

t he

par t

of

t he

10.10

orbital

B,

In

Coronal

oor.

addition

complained

A,

to

of

computed

The

the

contents

fracture,

numbness

of

the

the

the

of

the

(Fig.

joined

t he

the

duc t

are

cavity.

the

right

patient

right

of

t he

margin

ethmoid

and

10.12).

sometimes

the

e

medial

small

is

said

wall

part

of

is

to

the

the

be

“paper

thinnest

sphenoid

thin”

of

the

bone

(lam-

orbital

present

adjacent to the wall of the optic canal (see Fig. 10.7). e oor is

tomography

of

me dial

orbit.

to

two

the

located

roof

medial

walls,

and

within

and

wall

the

the

medial

at

the

anterior

sutures

and

connecting

posterior

frontoethmoidal

suture

wall.

B

Fig.

lacrimal

prominence

max-

wit h

A

lacr imal

continuous

globe.

in this wall is part of the body and is located at the posterior end,

p or t ion

nas al

the

size

t he

t he

t he

is

papyracea),

walls

lacrima l

lower

t he

sinus

through

e ethmoid bone forms most of the medial wall. e orbital

pro-

medial

nas olacr imal

of

of

in

and

f ront al

b o dy

crest.

scan

r idge

crest

is

lacrimal

infer iorly

t he

me atus

it

f ront al

pro cess

foss a.

cont ains

infer ior

a

b ack,

approximately

f ront al

t his

to

lacrimal

continuous

w hich

t he

and

r idge

anter ior

of

t he

of

A

f ront

maxi l la,

anteri or

small

t hat

the

ethmoi d,

t he

wal l

gro ove

of

b order

b one,

From

10.11).

for ms

for ms

anter ior

for ms

nas olacrimal

w hich

plate

als o

lacr imal

t humbnail,

illar y

rec t angular.

b one

maxilla

margin

e

is

frontal

orbital

demarcates

sac.

Maxillary

computed

A

wall

sphenoi d

orbit al

canal

Coronal

Wall

medial

for med

10.9

has

cheek

scan

orbit

showing

are

ecchymosis

and

a

blow-out

protruding

double

and

a

vision.

into

the

fracture

right

subconjunctival

of

the

maxillar y

right

sinus.

hemorrhage.

He

the

bones

ethmoidal

at

the

of

canals

junction

of

CHAPTER

166

10

Bones

of

the

Skull

and

Orbit

Posterior

ethmoid

Lesser

&

anterior

foramina

wing,

sphenoid

bone

Frontal

bone

Ethmoid

Optic

canal

Groove Body

bone

for

of lacrimal

sphenoid

sac

bone

Foramen

Nasal

bone

rotundum

Lacrimal

bone

Palatine

canal Palatine Maxilla bone

Pter ygopalatine

foramen

Fig.

10.11

Anatomy

Lateral

Bones

of

Principles.

medial

St

orbital

Louis:

wall.

Mosby;

(From

Mathers

LH,

Chase

RA,

Dolph

J,

et al.

Clinical

1996.)

Wall

10

to the orbital rim on the frontal process of the zygomatic bone.

e

lateral

zygomatic

wall

is

bone

roughly

in

front

triangular

and

the

and

greater

is

composed

wing

of

the

of

the

sphenoid

is

is

the

palpebral

attachment

levator

site

muscle,

for

the

the

aponeurosis

lateral

canthal

of

the

tendon,

superior

the

lateral

10–12

bone

orbit

the

be

behind

from

(see

the

Fig.

temporal

zygomaticofacial

present

in

10.7).

the

e

fossa.

and

zygomatic

One

or

more

bone

foramina,

zygomaticotemporal

zygomatic

bone

as

a

separates

conduit

check

including

foramina,

for

the

may

ner ves

and

ligament,

and

the

suspensor y

ligament

of

Lockwood.

e greater wing of the sphenoid separates the orbit from the

middle

in

cranial

back

by

fossa.

the

e

superior

roof

is

separated

orbital

ssure

from

(see

the

Fig.

lateral

10.8)

wall

and

in

9

vessels

between

the

orbit

and

facial

areas.

e

lateral

or

mar-

front

by

ginal orbital tubercle (Whitnall tubercle), present in over 60% of

inferior

orbits,

from

is

a

small,

bony

prominence

located

2

to

3

mm

posterior

the

frontozygomatic

orbital

the

lateral

ssure

wall

and

separates

(Fig.

frontosphenoidal

the

Lamina Ethmoid

posterior

10.13).

papyracea

sinus (ethmoid

Maxillary

Fig.

10.12

Coronal

sinus

computed

Inferior

tomography

orbital

scan

fissure

posterior

to

the

globe.

bone)

sutures.

part

of

the

e

oor

CHAPTER

10

Bones

of

the

Skull

and

Zygomatic

Ethmoid

Sphenoid

sinus

Pterygopalatine

Greater

fossa

the

Fig.

zontal

38

Axial

computed

tomography

in

of

males,

scan

not

dimensions

diameter

mm

10.13

Margins

Although

of

the

and

bone

sinuses

Inferior

Orbital

167

Orbit

the

orbit

orbital

the

vary

margin

average

widely,

is

30

vertical

the

mm

average

in

diameter

hori-

females

is

34

and

mm

in

is

through

(Fig.

anterior

10.14).

cur ve

of

the

fissure

of

sphenoid

continuous.

the

wing

orbital

the

inferior

Starting

lacrimal

e

from

crest,

posterior

medial

orbit.

the

the

inferior

orbital

lacrimal

orbital

crest

nasal

margin

aspect,

forms

completes

the

which

a

spiral

superior

margin.

13

females

and

40

mm

in

males.

e

average

depth

of

the

medial

14

and

tal

of

lateral

bone

this

the

wall

forms

arch

is

superior

(see

rior

Fig.

42

the

mm

medial

is

47

corner

and

of

just

is

mm,

orbital

one-third

located

margin

and

superior

located

10.7)

orbital

is

the

the

the

respectively.

margin.

way

orbit.

medial

to

conduit

e

along

e

the

for

fron-

highest

the

point

margin

supraorbital

center

the

e

of

from

notch

the

supraorbital

supe-

Orbital

A

Foramina

number

the

middle

and

exit

of

structures.

of

and

foramina

and

cranial

fossa,

vessels

and

e

optic

Fissures

ssures

sinuses,

ner ves

that

foramen

or

exist

and

between

face

supply

the

to

the

optic

the

allow

globe

canal

orbit

the

and

(see

and

entrance

orbital

Fig.

10.7)

vessels

and nerves. Although a fascial band is generally present along the

oor of the notch, the notch can be palpated easily. In 27% to 52%

3,15

of

orbits,

At

the

the

the

supraorbital

superior

supratrochlear

vessels

notch

of

or

the

medial

notch,

same

groove

notch

the

enclosed

corner

is

through

name.

in

is

e

a

to

less

which

form

of

orbits,

the

orbital

foramen.

well-dened

passes

supratrochlear

majority

a

the

notch

becoming

groove,

ner ve

and

remains

a

a

foramen

16,17

in

less

than

e

to

18%

lateral

possible

margin.

frontal

bone

bone

e

It

margin

and

is

is

therefore

formed

superiorly

and

by

by

is

the

the

the

region

most

strongest

zygomatic

frontal

exposed

area

of

the

of

the

process

process

of

the

zygo-

inferiorly.

inferior

maxillary

skulls.

injur y

orbital

matic

of

orbital

orbital

bone

and

margin

the

usually

zygomatic

is

bone.

formed

e

equally

by

the

zygomaticomaxil-

lary suture can oen be easily palpated through the skin along the

inferior

orbital

edge.

e

infraorbital

foramen

(the

opening

from

the infraorbital canal) is found in the anterior surface of the max-

2–4

illary

bone,

e

the

frontal

frontal

margin.

bone

6.3

8.8

mm

process

bone

is

and

to

and

of

the

forms

process

anteriorly

below

the

maxillar y

part

of

articulates

with

the

inferior

the

orbital

bone

medial

posteriorly

nasal

bone.

e

margin.

articulates

rim

with

of

the

the

medial

with

orbital

lacrimal

margin

is

Fig.

that

and

10.14

the

The

medial

discontinuous

posterior

(blue

orbital

edges

arrow)

margin

are

crests

is

along

of

the

not

the

fossa

continuous.

anterior

for

the

(red

Note

arrow)

lacrimal

sac.

CHAPTER

168

10

Bones

of

the

Skull

Optic

and

Orbit

canal

Sphenoid

sinus

Anterior

clinoid

Optic

process

strut

Superior

orbital

Foramen fissure

rotundum

Fig.

is

formed

by

a

bridge

of

bone

10.15

called

Coronal

the

optic

computed

strut,

tomography

which

is

scan

located

at

the

anterior

optic

to

canal.

the

superior

orbital

ssure

and

the

optic

18

extends from the lesser wing to the sphenoid body (Fig. 10.15).

canal (Fig. 10.18). is ring is the origin for the four rectus mus-

e

cles. e optic ner ve and the ophthalmic arter y pass through the

canal

10.16).

the

lies

e

just

canal

sphenoid

lateral

oen

sinus

to

the

causes

and

the

body

an

of

the

sphenoid

indentation

bone

may

be

into

bone

the

dehiscent

(Fig.

bone

in

3%

of

optic

canal

and

the

tendinous

ring.

to

18

28%

of

cases.

It

provides

communication

between

the

orbital

CLINICAL

cavity

and

the

middle

cranial

fossa

and

is

separated

from

posterior

edge

of

the

superior

orbital

ssure

by

the

dura

e

optic

ner ve

exits

and

the

ophthalmic

arter y

enters

through

this

canal

(Fig.

10.17).

A

circular

band

of

tissue,

the

common

tendinous

ring

(or

annulus

the

optic

Nerve

canal

is

Damage

adherent

and

the

periosteum

of

the

canal.

This

to

close

of

the

even

bony

very

passage

small

predisposes

lesions

or

tumors

the

of

nerve

the

bony

to

sinus

fissure

canal

the

wing

of

sphenoid

Fig. 10.16

bone

dura

compression

canal.

Superior

Lesser

the

Zinn),

Ethmoid

Optic

both

connement

connecby

tive

lining

of

of

the

the

optic

nerve

the within

orbit

mater

optic nerve

strut.

COMMENT: Optic

the

The

medial

Sphenoid

sinus

Body

of

the

sphenoid

bone

Axial computed tomography scan through the optic canal.

orbital

and

damage

CHAPTER

10

Bones

of

the

Skull

and

Globe

Lens

Medial

rectus

Lateral

Optic

169

Orbit

rectus

nerve

Ophthalmic

artery

Optic

canal

Superior

orbital

fissure

Pituitary

Fig. 10.17

Axial,

Superior Lacrimal

soft

orbital

tissue

computed

fossa

tomography

scan

nerve

ingeal

Common

tendinous

vein

arter y

ssure

Optic

vein

the

optic

nerve.

before

may

exiting

enter

the

the

orbit

20

orbit.

e

through

the

middle

superior

men-

orbital

to

anastomose

with

the

recurrent

meningeal

branch

of

foramen

the

lacrimal

there

is

a

arter y ;

however,

cranioorbital

in

46%

foramen

to

55%

(also

of

called

the

the

population,

orbitomen-

ner ve

Optic Oculomotor

(superior

of

ring

Superior

T rochlear

length

19

ophthalmic

Frontal

the

fissure

ner ve

ophthalmic

along

ingeal

foramen)

ssure

in

located

superior

lateral

to

the

superior

orbital

ner ve 14

ner ve

which

this

anastomosis

19

22

occurs.

division) Ophthalmic

ar ter y

e inferior orbital ssure lies between the oor of the orbit

Nasociliar y

and

ner ve

and Oculomotor

ner ve

(inferior

the

10.18

orbital

fossae.

foramen

ner ve

Inferior

Fig.

orbital

fissure

within

and

above

the

common

tendinous

ring.

inferior

ing

the

vessels

e

lesser

superior

wing

and

orbital

the

ssure

greater

is

a

wing

7

of

to

8

the

mm

gap

between

sphenoid

bone

the

and

is

the

the

(see

the

Fig.

10.7).

orbit

ssure

and

ssure.

infraorbital

ner ve

It

the

maxillar y

and

into

allows

passage

of

pter ygopalatine

narrowest

the

division

of

of

the

(see

the

Fig.

its

trigeminal

maxillar y

ner ves,

inferior

continue

in

vessels

and

tem-

center.

pter ygopalatine

the

zygomatic

vessels

bone

is

Branches

through

and

oen

opens

maxillar y

orbital

passing

orbital

in

is

rotundum

transmits

Nerves and vessels that enter orbit through superior

ssure

wall

between

division)

poral

Abducens

lateral

ner ves

join

orbital

into

10.9).

the

A

fossa

ner ve

ner ve,

the

e

infraorbital

of

the

includ-

infraorbital

ssure.

branch

to

e

and

the

infra-

groove

inferior

19

located

between

the

roof

and

the

lateral

wall

(see Fig.

10.7).

As

with the optic canal, this ssure is a communication between the

orbital

cavity

widest

medially,

and

the

middle

becoming

cranial

fossa.

narrower

e

toward

ssure

the

usually

lateral

ophthalmic

ssure

vein

below

may

the

exit

the

common

orbit

through

tendinous

the

inferior

orbital

ring.

is

portion.

PARANASAL

SINUSES

Approximately midway on the lower aspect is a small sharp spur

(the

lateral

lateral

rectus

rectus

spine)

muscle.

that

Fig.

ser ves

10.18

as

shows

the

the

attachment

relationships

for

the

among

e paranasal sinuses are mucosa-lined, air-lled cavities located

in

four

of

the

orbital

bones.

ese

hollow

spaces

decrease

the

the superior orbital ssure, the common tendinous ring, and the

weight of the skull and help add resonance to the voice. e para-

various

nasal

tal

ner ves

ner ve,

ssure

will

and

above

either

passing

through

trochlear

the

pass

ner ve

circular

through

them.

pass

tendon.

or

e

above

e

lacrimal

through

the

superior

the

ner ve,

superior

fron-

orbital

ophthalmic

common

tendinous

vein

ring

20

before

exiting

the

orbit

through

the

superior

orbital

sinuses

communicate

with

the

nasal

cavity

through

small

apertures.

e orbit is surrounded on three sides by sinuses (Fig. 10.19):

the

frontal

sinus

above

(see

Fig.

10.9),

the

ethmoid

and

sphe-

21

ssure.

noid

sinus

cavities

medial

to

(see

Fig.

10.13),

and

the

maxil-

e superior and inferior divisions of the oculomotor ner ve, the

lar y sinus below the orbit (see Fig. 10.9). Of these, the maxillar y

nasociliar y

sinus is largest. e roof of the maxillar y sinus is the orbital plate

sure

and

ner ve,

the

and

common

the

abducens

tendinous

ner ve

ring.

pass

e

through

inferior

the

s-

ophthalmic

of

the

maxilla.

is

plate,

only

0.5

to

1

mm

thick,

separates

the

1

vein may pass through the superior orbital ssure, but more fre-

sinus

quently,

the

the

inferior

ophthalmic

vein

drains

into

the

superior

from

body

the

of

orbital

the

contents.

sphenoid

and,

e

in

sphenoid

some

sinus

individuals,

is

within

continues

CHAPTER

170

10

Bones

Frontal

into

the

moid

the

lesser

sinus

frontal

the

thin

wing

of

and

sometimes

process

bone

of

sinus

of

may

the

both

the

within

surround

into

maxilla.

Orbit

sinus

cavities

continues

and

sinus

Maxillary

Location

Skull

sinus

Sphenoid

10.19

the

sinus

Ethmoid

Fig.

of

In

the

the

a

optic

and

walls.

canal.

lacrimal

high

sphenoid

orbital

percentage

the

e

bone

of

ethmoid

contact

CLINICAL

with

the

dural

sheath

COMMENT: Orbital

of

the

optic

into

orbits,

sinuses

23

makes

eth-

or

24

ner ve.

Cellulitis

The thin walls of the sinus cavities are poor barriers to the passage of infection

from

the

air

cavities

into

the

orbit.

If

pathogens

from

a

sinusitis

penetrate

the

thin, bony barrier, a serious infection involving the orbital contents might ensue

(Fig.

10.20).

A

major

infection

that

involves

the

orbital

connective-tissue

6

tents

is

Signs

called

and

orbital

symptoms

cellulitis,

include

and

one

sudden

of

its

onset

major

causes

pain,

edema,

of

is

con-

7

25

Fig.

left

the

in

ocular

motility.

Orbital

cellulitis

is

a

serious

Coronal T1

cellulitis

maxillary,

fection

has

of

the

relatively

easy

access

to

the

brain

proptosis,

medical

through

and

situation

must

be

treated

aggressively;

orbital

hospitalization

and

left

resonance

fungal

frontal

frontal

sinus

imaging

infection

sinuses

bone

to

showing

involving

bilaterally. The

enter

the

orbit

in-

(asterisk).

a

optic

canal,

foramina

may

be

the

periorbita

splits

such

that

a

portion

becomes

be-

with

the

dura

of

the

optic

ner ve

and

another

por-

and

7

and

the

a

26

tion ssures

ethmoid,

eroded

continuous cause

magnetic

following

sinusitis.

the decrease

10.20

orbital

reects

for ward

to

take

part

in

the

formation

of

the

com-

25

required.

mon tendinous ring. At the inferior orbital ssure, the periorbita Orbital

cellulitis

also

is

a

possible

sequela

of

a

blow-out

fracture,

which

can

is

continuous

with

the

periosteum

of

the

skull.

At

the

lacrimal

(but rarely does) provide a pathological avenue between the sinus cavities and

crests

27

the

orbit

that

results

in

orbital

infection.

a

sheet

of

periorbita

covers

the

lacrimal

sac,

and

the

peri-

orbita is continuous with the tissue lining the nasolacrimal canal.

ORBITAL

CONNECTIVE

Another

portion

Orbital

Septum

At

that serves to line, cover, and separate orbital structures; to anchor

nective

so

the

tissue

structures

this

to

network

bone;

is

and

to

continuous,

compartmentalize

the

segments

are

areas.

described

here individually according to their position and function.

periorbita,

fascia,

covers

nective

cles,

also

the

tissue

called

bones

of

membrane

tendons,

and

the

the

ser ves

ligaments

orbital

orbit

as

and

periosteum

(Fig.

an

is

a

10.21).

is

attachment

support

or

orbital

dense

site

for

structure

the

con-

mus-

for

the

orbital

periorbita

margins,

tissue

sheet

palpebral

tive

the

Periorbita

e

the

covers

the

lacrimal

gland.

TISSUE

e connective tissue of the orbit is arranged in a complex network

Although

of

tissue

orbit

fascia

sheet

to

the

is

fascia

the

is

from

entering

Figs.

10.21

structures

and

or

as

orbit.

the

runs

aponeurosis

both

barrier

It

also

show

orbital

is

continuous

orbital

septum,

orbitale.

and

inferiorly,

10.22

the

septum

strong

the

and

periorbita

circular

levator

lopalpebral

eyelids.

the

known

of

which

At

the

con-

connec-

rim

the

fat

in

infections

in

its

between

lateral

of

capsu-

embedded

facial

orbital

relationships

a

termed

entire

and

are

prevent

maintains

septum.

dense

the

superiorly

helps

the

is

from

with

also

place.

orbital

margin,

the

orbital septum lies in front of the lateral canthal tendon and the

28

blood supply to the orbital bones. e periorbita is attached only

check

loosely

orbital

to

sutures,

the

and

underlying

the

edges

bone

of

except

ssures

at

and

the

orbital

foramina.

margins,

At

the

the

orbital

lea

margins it is continuous with the periosteal covering of the bones

the

of

the

the

canal,

the

face.

and

At

the

periosteal

the

edges

ethmoid

layer

of

of

the

canals,

the

dura

superior

the

orbital

periorbita

mater.

At

the

is

ssure,

the

continuous

anterior

optic

with

portion

of

for

ligament

and

margin

bridges

medial

the

the

rectus

septum

supraorbital

the

rectus

Horner

lateral

orbital

lacrimal

medial

tendon,

the

margin

posterior

the

for

orbital

crest,

muscle,

and

passes

and

it

in

the

At

front

which

front

lies

in

the

of

supratrochlear

septum,

lies

muscle;

muscle.

of

behind

lacrimal

the

check

At

behind

ligament

medial

(see

troch-

notches.

attaches

the

sac

superior

the

Fig.

canthal

10.22),

CHAPTER

Combined

Sheath

T endon

Sheath

of

of

superior

superior

of

sheaths

levator

oblique

rectus

of

levator

and

superior

10

Check

rectus

Bones

ligament

of

of

the

and

171

Orbit

levator

Levator

muscle

Skull

aponeurosis

muscle

muscle

Orbicularis

Periorbita

Orbital

Müller

muscle

septum

muscle

Orbito-palpebral

Cutaneous

of

T enon's

Capsule

plates

Palpebral

Bulbar of

rectus

conjunctiva

inferior

Orbital

Falcifor m

(of

of

Kronfeld

isolating

cavity)

the

from

lacrimal

the

orbit

sac

Fascial

the

PC.

system

eyeball.

The

(which

ligament

The

Human

Periorbita

of

oblique

the

eyeball

Eye.

orbit

is

in

muscle

shown

primar y

Rochester,

communicates

with

the

NY :

Check

in

a

Bausch

nasal

proper.

vertical

position

&

with

Lomb

in

the

to

the

space

COMMENT: Preseptal

cellulitis

is

an

inammatory

condition

that

affects

the

tissue

of

ner ve,

If

an

infection

of

an

eyelid

the

closed.

vertical

(Adapted

me-

from

area.

Although

1.5

mm

between

eye

Tenon

capsule

posterior

the

to

episclera

movements.

the

and

Tenon

is

rmly

limbus,

Tenon

capsule

is

a

attached

potential

capsule

which

pierced

by

gland

becomes

more

serious

and

vortex

veins,

ciliar y

vessels

and

ner ves,

and

the

extra-

the

ocular eyelid.

rectus

1943.)

about

present

inferior

through

eyelids

Press;

smooth

of

Cellulitis

optic

Preseptal

the

limbal

is

ligament

section

sclera

allows

CLINICAL

septum

Lockwood)

Inferior

10.21

muscle

fold

Suspensor y

ridian

conjunctiva

muscle

Orbicularis

Fig.

inser tions

levator

T arsal

Sheath

sulcus

muscles.

At

the

muscle

insertions,

Tenon

capsule

forms

involves 6,30

sleevelike

sheaths

that

cover

the

tendons.

Posteriorly,

Tenon

the tissue around the gland, preseptal cellulitis occurs. The disease can be lim-

capsule ited

by

the

location

of

the

orbital

septum,

which

provides

a

barrier

to

dense spread

into

the

orbit.

Spread

of

the

disease

could

result

in

the

orbital

T enon

dural

capsule

sheath

acts

as

of

a

the

optic

barrier

to

ner ve.

is

prevent

of

orbital

infections

into

the

the

globe.

cellulitis.

Capsule

capsule

tissue

that

in

anterior

the

the

tissue

development

Suspensory

Tenon

with

connective

spread of

merges

prevent

e

(bulbar

encases

the

portion

fascia)

globe.

of

is

a

sheet

Smooth

Tenon

of

dense

muscle

capsule,

bers

whereas

Ligament

suspensor y

ligament

connective

hammocklike

sheet

are

its

on

the

present

posterior

attachment

of

the

(of

Lockwood)

(of

dense

lacrimal

L ockwood)

connective

bone

at

(see

tissue

the

Fig.

that

medial

10.21)

runs

orbital

is

a

from

wall

to

the zygomatic bone at the lateral wall. Tissue from several struc-

29

portion

is

a

conjunctiva

brous

and

the

capsule

of

episclera

orbital

and

fat.

merges

It

lies

with

between

them

the

anteriorly

tures—Tenon

lar

muscles,

capsule,

and

the

the

sheaths

inferior

eyelid

of

the

two

inferior

extraocu-

aponeurosis—contributes

to

CHAPTER

172

10

Bones

of

the

Skull

and

Orbit

Orbicularis Medial

Anterior

canthal

limb

muscle

tendon

Posterior

limb Superior

tarsus

Palpebral

conjunctiva

Bulbar

Lacrimal

Hor ner

sac

muscle

Orbital

Check

Orbital

septum

Lateral

canthal

septum T enon’s

of

conjunctiva

capsule

ligament

medial

rectus

Sheath

of

medial Check

rectus

tendon

ligament

of

muscle lateral

rectus

Periorbita Sheath

rectus

of

lateral

muscle

Periorbita

Fig.

lies

10.22

with

the

Lomb

the

to

formation

support

the

orbital

Orbital

e

of

this

globe,

Muscle

of

muscle

smooth

inferior

but

it

eyelids

Press;

system

the

of

the

horizont al

closed.

orbit

shown

meridian

(Adapted

from

of

in

a

horizontal

eyeball,

Kronfeld

which

PC.

The

is

section. The

assumed

Human

Eye.

to

plane

be

in

Rochester,

ligament.

e

in

suspensor y

the

absence

ligament

of

the

helps

bones

of

of

the

muscles

nectivity

occur

Orbital

Fat

during

eye

of

may

the

Müller

of

muscle

orbital

the

play

orbital

Müller

role

a

embedded

ssure,

in

the

providing

sympathetically

periorbita

a

ceiling

and

over

inner-

A

contents

Septal

complex

nizes

the

web

covering

the

bony

function

regulating

in

humans

venous

blood

is

unknown,

during

embr yological

ow

or

isolat-

development.

System

of

orbital

partments.

spaces

four

not

adipose

cone

occupied

tissue

surrounding

extraocular

muscles

Bausch

&

the

orbit

V arying

(see Figs.

degrees

11.7 and

of

con-

11.8).

by

compartments

the

optic

connective

surrounding

Collagenous

strands

the

connect

globe

the

tissue

into

septa

radial

periorbita

to

and

intermuscular

membranes.

is

connective

structures,

connective

tis-

the

are

ner ve

located

and

within

separating

the

it

muscle

from

the

separates

the

34

muscles.

from

tissue

of

the

outward

interconnecting

space

ocular

A

walls

of

ring

the

of

adipose

orbit,

and

tissue

adipose

is

the

predomi-

33

nant

near

the

orbital

orbital

apex.

contents,

displacement

of

a

the

Because

of

the

space-occupying

close

lesion

associa-

will

cause

globe.

orga-

com-

T enon

CLINICAL

Protrusion

capsule

NY:

section

position

sue, ner ves, or vessels become lled with adipose tissue. Usually,

33

Its

in

small,

31

ssure.

a

e

is

tion

Orbital

the

movements.

throughout

31

ing

of

primar y

1943.)

particularly

10

margins

above

oor.

orbital

vated

the

the

Fascial

slightly

of

COMMENT: Exophthalmos

the

globe

is

termed

exophthalmos,

or

proptosis

(Fig.

10.23A).

It

tissue

can

be

caused

by

a

number

of

pathological

conditions,

including

inammation,

system of slings anchors and supports the extraocular muscles and edema, tumors, and injuries. The most common type is thyroid ophthalmopathy

32

blood vessels, attaching them to adjacent orbital walls.

e slings (dysthyroid

associated

with

each

of

the

muscles

maintain

correct

positioning

orbitopathy,

Graves

disease),

which

can

cause

hypertrophy

of

the

CHAPTER

A

Bones

of

the

Skull

and

173

Orbit

B

Fig.

10.23

showing

the

A,

Exophthalmos

enlargement

of

the

(proptosis)

extraocular

of

the

left

muscles

muscles

eye.

causing

B,

Axial

computed

proptosis

of

both

tomography

eyes,

but

scan

greater

on

right.

6. extraocular

10

(see

Fig.

10.23B).

In

some

patients,

the

muscles

Doxanas

MT,

Anderson

RL.

Clinical

Orbital

Anatomy.

Baltimore:

become

Williams

&

Wilkins;

1984:20,

25,

117.

7

enlarged

to

8

times

their

normal

size.

Thyroid

ophthalmopathy

also

causes

lymphoid

inltra-

7. proliferation

of

orbital

fat

and

connective

tissue,

as

well

as

Kanski

JJ.

Clinical

Heinemann;

Ophthalmolog y,

3rd

ed.

London:

Butter worth-

1994:33–52.

7

tion.

Because

the

orbital

tissue

is

encased

in

immovable

bony

walls,

this

8. increase

in

volume

of

the

orbital

contents

produces

protrusion

of

the

Forrest

LA,

blow-out and

simulates

eyelid

retraction.

At

the

rst

sign

of

proptosis,

investigation

to

determine

the

causative

fractures.

DE,

Am

Strauss

J

Sports

RH.

Management

Med.

of

orbital

1989;17(2):217–220.

is

9. necessary

Schuller

globe

Iwanaga

J,

Badaloni

F ,

Watanabe

K,

etal.

Anatomical

study

of

the

factor.

zygomaticofacial

foramen

and

its

related

canal.

J

Craniofac

Surg.

2018;29:1363–1365.

10.

AGING

CHANGES

IN

THE

Cornelius

Facial

In

elderly

in

the

nective

and

pass

adults,

medial

tissue

with

age

into

the

can

area,

occur.

these

the

orbital

inferior

e

walls

orbit.

septum

and

e

weakens,

herniation

walls

may

oen

of

the

actually

inferior

of

fat

rim

particularly

and

paranasal

contain

orbital

loose

con-

sinuses

thin,

perforations

recedes

with

11.

the

upper

face

becomes

more

concave.

FN,

suture:

Orbit.

that

age,

Fries

Plast

12.

Mayer

features

Surg.

P ,

in

Ehrenfeld

view

of

M,

etal.

innovative

e

Orbits—

surgical

methods.

2014;30:487–508.

Y oussef

Whitnall’s

P ,

Ir win

tubercles

application

and

to

PA,

their

etal.

Comparing

relation

symmetr y

to

the

following

the

le

and

right

frontozygomatic

lateral

orbital

surger y.

2016;35:305–308.

Gospe

SM,

Bhatti

MT.

Orbital

anatomy.

Int

Ophthalmol

Clin.

2018;58:5–23.

35,36

and

C-P ,

Anatomical

ORBIT

In

addition,

the

13.

Sinanoglu

A,

Orhan

K,

Kursun

S,

etal.

Evaluation

of

optic

canal

supraorbital rim recedes, which may contribute to the increased and

visibility

of

fat

along

the

upper

medial

surrounding

structures

using

cone

beam

computed

tomog-

eyelid. raphy :

considerations

for

maxillofacial

surger y.

J

Craniofac

Surg.

2016;27:1327–1330.

14.

Y oon

J,

Pather

N.

e

orbit:

a

re-appraisal

of

the

surgical

landmarks

REFERENCES of

1.

2.

W ar wick

R.

my

Eye

of

the

Aggar wal

fraorbital

Clin

3.

Kaur

of

men

N,

with

paranasal

H,

a

7th

ed.

Gupta

basis

BR,

Abreu

T,

for

sinuses.

In

Eugene

Philadelphia:

etal.

Wol ’s

Saunders;

Anatomical

successful

study

infraorbital

Anato-

15.

1976:1–29.

of

the

ner ve

Surg

Apaydin

Radiol

N,

reference

and

to

so

Custódio

infraorbital

Anat.

Kirici

of

16.

Y .

A

morphometric

relative

to

surgi-

of

the

landmarks.

Takahashi

the

of

orbital

Y ,

oor

in

predisposition

Exp

migraine

Janis

JE,

Radiolic

fora-

Anat.

Ophthalmol.

T,

Miyazaki

relation

to

orbital

to

the

oor

H,

etal.

An

infraorbital

fracture

2016;254:2049–2055.

site.

anatomical

study

of

groove:

implications

Graefe’s

Arch

Clin

JE,

DA,

Webster

Plast

RC,

K,

relevance.

the

JM,

notches

the

Plast

Reconstr

Acosta

to

for

RR.

clinical

Hagan

Gaunt

relevance.

Abhinav

walls. Clin

Hagan

notch:

implications

surgical

18.

lateral

headaches.

Hatef

approach

Nakano

Janis

supratrochlear

infraorbital

Surg

M,

and

supraorbital

headaches.

17.

2011;33:329–335.

Location

tissue

ALN.

foramina

2017;39:11–15.

5.

Fallucco

the

in-

block.

medial

ner ve:

MHNG,

supraorbital

landmarks.

Ercikti

and

Orbit.

2015;28:753–760.

Chrcanovic

cal

4.

A,

and

foramen:

Anat.

analysis

Orbit

the

R,

e

Reconstr

etal.

Y ,

Wang

canal:

Neurosurgery.

Surg.

the

morpholog y

surgical

of

treatment

2012;130:1227–1233.

of

treatment

the

of

supratrochlear

migraine

2013;131:743–750.

Hamdan

and

to

Anatomy

surgical

Surg.

2016;29:998–1010.

anatomical

relevance

US,

foramina:

Laryngoscope.

optic

Anat.

etal.

Supraorbital

anatomical

and

variations

and

1986;96(3):311–315.

W-H,

etal.

anatomic

Endoscopic

endonasal

considerations

2015;11(Suppl

3):431–445;

and

surgical

discussion

445-446.

19.

Regoli

ing

M,

the

Bertelli

orbit

with

E.

e

the

revised

cranial

anatomy

cavity.

Orbit.

of

the

canals

connect-

2017;36:110–117.

CHAPTER

174

20.

Cheung

N,

McNab

Ophthalmol

21.

22.

23.

Vis

Natori

Y ,

orbital

ssure.

Abed

SF ,

AA.

Sci.

Rhoton

AL.

P ,

Shen

foramen

Surg.

optic

ner ve

the

of

Skull

the

and

orbit.

Orbit

Invest

28.

S,

and

anatomy

of

the

superior

its

A

cadaveric

signicance

29.

study

in

of

the

orbital

30.

SG,

Forbes

paranasal

Otolaryngol

G.

Relationship

sinuses

Head

as

Neck

shown

Surg.

of

by

the

Cheung

scan

the

computed

31.

1987;96(4):

of

Attia

the

transnasal

EL,

Kirkpatrick

lateral

wall

transethmoid

of

DA,

the

etal.

sphenoid

endoscopic

An

anatomic

sinus

approach.

as

J

and

related

CT

32.

to

Otolaryngol.

R.

ed.

Mills

of

RP ,

e

33.

Merck

Manual.

14th

ed.

Rahway,

NJ:

Merck;

infection

from

JM.

the

Orbital

wall

paranasal

thickness

sinuses.

Clin

and

the

spread

Silver

as

a

HS,

Fucci

MJ,

complication

Surg.

A,

of

orbital

1992;118(8):845–848.

JC,

etal.

Otolaryngol.

fracture.

Severe

Arch

orbital

35.

infection

Otolaryngol

Head

Pogrel

Oral

JJ.

Jaeger

vol

MA.

Med

Nakano

Anatomy

Oral

Pathol

of

Oral

the

lateral

Radiol

J,

1.

Ann

Wöhler

of

and

A,

its

etal.

of

the

Duane’s

Philadelphia:

Anat.

Clinical

eds.

T,

Anatomy

of

Tenons

2012;40:611–616.

anatomy

EA,

features

etal.

extraocular

Foundations

Lippincott;

Anatomy

detailed

muscles.

of

Clinical

1994.

of

the

topography,

human

syntopy

orbital

and

2017;211:39–45.

surgical

orbital

anatomy.

Ophthalmol

Clin

1996;9(4):527.

L.

Orbital

Anatomy,

&

Y ,

Ophthalmol.

Functional

W ,

Feiser

Koornneef

Row ;

connective

Embryolog y,

tissue.

and

In:

Jakobiec

Teratolog y.

FA,

ed.

Philadelphia:

1982:835.

Wolfram-Gabel

Huang

fat

Flanagan

N,

Surg

R,

Kahn

JL.

Adipose

body

of

the

orbit.

Clin

Anat.

2002;15(3):186–192.

1985;10(4):209–216.

27.

Exp

(OM):

Am.

Harper

34.

Kartush

Dutton

Ocular

1982:1984.

26.

Wilden

North

Oral

Takahashi

morpholog y.

DK,

study

Berkow

HM.

Tasman

muscle

1993;22(2):63–68.

25.

H,

Clin

Ophthalmolog y,

331–335.

24.

Eggers

In:

Talebzadeh

2000;89(1):24–28.

Kakizaki

capsule.

surger y.

T,

tendon.

Endod.

1995;36:762–775.

etal.

Rosenstein

canthal

2012;129:307e–311e.

Harner

to

tomography.

the

anatomy

Microsurgical

Plast

SF ,

Venous

of

2003;44:988–995.

cranio-orbital

Bansberg

Bones

Neurosurgery.

Shams

Reconstr

10

Neck

R-L,

graing.

36.

Xie

Y ,

compartments

Aesthet

Ilankovan

V .

Wang

and

Surg

J.

Anatomy

2014;52:195–202.

W ,

its

etal.

clinical

Anatomical

application

study

for

of

temporal

temporal

fat

2017;37:855–862.

of

ageing

face.

Br

J

Oral

Maxillofac

Surg.

11

Extraocular

e

muscles

involuntar y

of

the

globe

intrinsic

can

muscles

be

divided

and

the

into

two

voluntar y

groups:

extrinsic

the

mus-

cles. e intrinsic muscles—the ciliar y muscle, the iris sphincter,

and

the

control

sic

iris

the

dilator—are

movement

muscles—the

and

control

is

and

six

and

muscle

are

Chapters

the

and

the

with

anatomy

the

ocular

eye.

ese

structures.

muscles—attach

to

extrin-

the

sclera

of

Smooth

brief

action

of

the

muscle.

actions

intrinsic

of

microscopic

en

each

muscles

are

eye

move-

extraocular

discussed

in

14

Myobrils

myobrils

subunit

other

OF

a

by

cell

two

composed

long,

arms

form

projecting

cytoplasm,

and

the

special

sarcoplasm,

muscle

con-

bers,

the

of

slender

at

the

outward

one

types,

lament

end.

backbone

in

a

thick

hundreds

spiral

thin.

two

laments

the

(Fig.

and

myosin

with

ese

of

of

globular

lie

myobril,

11.2A).

e

next

with

e

thick

subunits.

thin

Each

heads

to

the

each

heads

myobrils

are formed by the protein actin arranged in a double-helical la-

ment,

ated

STRIATED

e

structures

comprise

are

is

and

with

a

within

e

ANATOMY

cellular

myobrils.

lying

MICROSCOPIC

potential.

normal

attached

review

striated

and

an

tains

muscles

e

globe.

a

characteristics

discussed.

5

of

begins

macroscopic

ments

within

internal

extraocular

movement

chapter

located

of

to

Muscles

of

complex

grooves

alternating

muscle

types

molecular

the

are

light

of

and

produced

myobrils

are

the

of

dark

by

troponin

double

bands

the

arranged.

helix

tropomyosin

11.2B).

characteristic

manner

e

and

(Fig.

light

in

which

band

is

of

stri-

these

the

I

two

(isotro-

MUSCLE pic)

Striated

known

as

nective

muscle

within

muscle

the

the

enclosure,

sheaths

network,

divides

bundle

the

are

tudinally

surrounded

epimysium.

tissue

and

is

it

is

surrounded

endomysium

may

play

a

connective

with

perimysium,

bundles.

interconnected

and

a

Continuous

the

into

by

by

(Fig.

in

a

sheath

which

delicate

e

is

connective

connective

mechanical

a

muscle

circumferentially

the

sheath

con-

inltrates

individual

11.1).

both

role

e

this

tissue

and

the

the

ber

band,

names

two

e

to

each

tissue

(Fig.

tissue

band

longi-

properties

of

and

the

describe

dark

the

band

is

the

birefringence

A

to

(anisotropic)

polarized

light

band.

ese

exhibited

by

areas.

I

band

other

11.3).

contains

at

Only

contains

the

Z

actin

both

two

line,

a

sets

myobrils

myosin

of

dark

and

actin

stripe

are

laments

that

found

actin.

bisects

in

e

the

I

central

connected

the

I

band.

band

e

lighter

A

zone

of the A band—the H zone—contains only myosin. Overlapping

actin and myosin laments form the outer darker edges of the A

1

the

muscle.

however,

at

the

e

each

each

invaginations

which

ber

peripher y

rounding

allow

individual

of

is

ions

the

the

to

ber

multinucleated,

muscle

into

muscle

ber.

ber,

cell,

spread

e

the

the

is

comparable

with

the

plasma

cell

sarcolemma,

transverse

quickly

nuclei

the

a

cell

a

cell;

arranged

membrane

forms

tubules

through

to

band.

sur-

series

of

(T

tubules),

in

response

e

M

interconnect

A

line

the

sarcomere

tractile

unit

of

bisects

myosin

extends

striated

the

H

zone

and

contains

proteins

that

brils.

f rom

Z

line

muscle.

to

With

Z

line

and

muscle

is

the

con-

contraction,

a

Epimysium

A

Perimysium

B

Fig.

in

Fig.

11.1

Connective

11.2

Myosin

composed

Endomysium

tissue

network

of

striated

muscle.

a

spiral.

lament

to

of

B,

and

actin

two-headed

The

which

actin

myobrils.

laments,

myobril

is

A,

with

The

the

composed

troponin-tropomyosin

myosin

heads

of

a

complexes

bril

is

arranged

double-helix

are

att ached.

175

CHAPTER

176

A

band

H

zone

11

Extraocular

I

Muscles

band

Z

Myosin

line

++ Ca

ATP

A

A

band

Actin

Actin

M

Tropomyosin

Troponin

line

filaments

H

Myosin

zone

filaments

Z

line

Z

line

B

ADP

Fig.

11.3

mere.

A,

B,

indicated.

Histology.

change

as

the

causes

of

Photomicrograph

sarcomere

of

Arrangement

in

(B

Baltimore:

laments

the

lines

Z

to

of

from

thin

striated

&

o ccurs.

slide

come

and

H

the

closer

with

Cutts

W ilkins;

e

past

laments

muscle

Krause WJ,

Williams

conguration

actin

thick

JH.

in

a

+

P

sarco-

parts

of

the

Concise T ext

1981 .)

zone

width

myosin

together

decreas es

laments.

and

the

is

sarcomere

ATP

to

shor ten.

is

decreased.

remains

zone

is

along

length

of

as

Ratchet

of

explained

the

e

o ccurs

do es

the

the

the

A

muscle,

actin

and

band.

e

the

mus cle

myosin

I

band

length

laments

and

the

H

shor ten.

process

tion

this

constant

Sliding

e

As

of

a

by

the

muscle

release

of

Model

muscle

of

Contraction

contraction

sliding

ratchet

contraction

acetylcholine

occurs

into

and

model

the

when

sarcomere

shortening

(Fig.

e

initia-

impulse

causes

a

11.4).

nerve

neuromuscular

junction.

e ADP

sarcolemma

surface

and

depolarizes

is

carried

and

into

an

the

action

potential

muscle

ber

passes

through

along

the

+

P

the

system

2+

of

T-tubules.

Ionic

channels

are

opened

and

calcium

ions

(Ca

)

are released from the sarcoplasmic reticulum into the sarcoplasm.

2+

Ca

binds

to

the

troponin-tropomyosin

complex,

resulting

in

a Z-LINE

congurational change, allowing an active site on the actin protein Fig.

to

be

available

adenosine

broken

the

for

binding

triphosphate

down

active

and

actin

(ATP)

released,

site.

with

a

myosin

attached

allowing

Once

this

a

bond

head.

to

the

myosin

cross-bridge

is

11.4

formed,

to

head

bind

the

head

e

Myasthenia

a

junction

of

between

a

new

the

ATP

actin

and

molecule

myosin

to

the

is

broken

myosin

by

head.

the

e

head then rights itself, and the cross-bridge is ready to bind with

defect

formed

in

and

are

next

actin

site

along

the

chain.

is

ratchet

type

of

COMMENT: Myasthenia

gravis

is

a

chronic

transmission

that

muscular

either

junction.

block

is

ptosis

of

the

or

Muscle

particularly

symptom

the

of

muscle

contraction.

tilts

it.

attachment

model

is

CLINICAL

with

ratchet

with

toward the sha of the myosin lament, pulling the actin lament

along

Sliding

Simultaneously,

(Fig.

nerve

destroy

with

11.5).

neuromuscular

impulse

the

weakness

evident

Gravis

autoimmune

to

muscle

acetylcholine

and

fatigue

repetitive

Sometimes

a

at

the

throughout

Often

vision

caused

Antibodies

receptors

worsen

movements.

during

disease

bers.

the

rst

examination,

by

are

neuro-

the

day

clinical

the

up-

move-

per eyelid begins to droop, and becomes quite evident by the end of the exami-

ment

occurs

along

the

length

of

the

ber,

moving

the

laments nation.

past

one

another

with

the

overall

eect

of

shortening

the

Ocular

resulting

mere

and

the

entire

muscle.

myasthenia

gravis

sarcoin

diplopia

and

ptosis.

is

limited

to

extraocular

and

eyelid

muscles,

CHAPTER

A

11

Extraocular

177

Muscles

B

Fig.

30

11.5

Ptosis

seconds

of

associated

looking

up,

with

the

myasthenia

ptosis

has

gravis.

signicantly

A,

muscles

STRUCTURE

OF

THE

EXTRAOCULAR

Before

worsened

prolonged

in

both

a

range

have

upgaze.

B,

After

eyes.

of

ber

sizes,

with

the

bers

closer

to

the

MUSCLES surface generally having smaller diameters (5–15 μm) and those

e

extraocular

muscles

have

a

denser

blood

supply,

and

their

deeper

within

16

connective

tissue

sheaths

are

more

delicate

and

richer

in

elastic

(10–40

the

17

20

muscle

generally

having

larger

diameters

21

μm).

2

bers

compared

included

skeletal

in

an

with

skeletal

extraocular

muscle

elsewhere.

muscle.

muscle

Fewer

motor

Striated

muscle

unit

muscle

of

than

the

bers

are

leg

are

found

can

in

contain

Extraocular

one

end

with

of

muscle

the

bers

spectrum

gradations

in

to

range

typical

between.

from

slow

Singly

typical

bers

twitch

at

inner vated

the

bers

other

bers

at

end,

have

the

3

several

hundred

muscle

bers

per

motor

unit.

In

the

extraoc-

classic end plate (en plaque) seen in skeletal muscle. ese bers

4

ular

muscles,

each

axon

inner vates

3

to

10

bers.

is

dense

respond

to

electrical

stimulation

with

a

single

twitch.

Multiply

22

inner vation

muscles

allows

resulting

precise

in

the

ne

motor

control

high-velocity

ocular

of

the

extraocular

movements

neces-

inner vated

have

a

bers,

for

saccades

(up

to

1000

degrees

per

second),

as

well

as

ver y accurate pursuits (velocities of 100 degrees per second) and

(en

normally

neuromuscular

23

sar y

not

in

resembling

skeletal

a

muscle,

bunch

of

grapes

24

grappe).

traction.

junction

present

ese

Recently,

bers

respond

multiterminal

5

en

with

a

plaque

graded,

endings

tonic

were

con-

found

22

xation.

Extraocular

muscles

are

among

the

fastest

and

most

in

extraocular

muscle.

It

would

seem

that

the

fast-twitch

bers

6

fatigue-resistant

Muscle

ated

of

striated

spindles

muscle

have

and

been

muscle.

Golgi

tendon

identied

in

organs

human

of

typical

extraocular

stri-

mus-

should

produce

quick

should

produce

slower

tone.

However,

all

saccadic

pursuit

bers

are

movements

and

movements

active

at

all

and

times

although

useful

it

is

unclear

proprioceptive

whether

these

information

structures

relative

to

the

provide

any

level

extraocular

of

involvement

Among

the

in

global

all

ocular

muscle

slow

provide

and

16

cle,

the

19

21

bers

muscle

share

some

25

movements.

bers

that

are

singly

inner vated,

7–9

muscles.

Aerent

proprioception

is

information

thought

to

be

regarding

mediated

extraocular

by

a

muscle

receptor

that

is

the

fast

red

bers

twitch

(having

and

a

fatigue

high

amount

resistant.

e

of

myoglobulin)

white

bers

(with

may

a

be

lesser

6

unique

to

extraocular

muscle,

the

myotendinous

cylinder

(pali-

amount

of

myoglobulin)

are

fast

twitch

and

may

be

fatigable.

7,10

sade

ending).

e

bers

Global

of

the

extraocular

muscles

have

a

layered

organiza-

the

bers

that

are

myotendinous

multiply

cylinder

or

inner vated

palisade

are

associated

endings;

they

are

with

large

6

tion.

e

global

layer

is

adjacent

to

the

globe

and

consists

of

bers

myobrils

and

appear

to

be

slow

and

tonic.

Orbital

muscle

11

of

various

of

the

diameters.

muscle

and

is

is

group

attached

at

of

the

bers

extends

origin

and

the

full

insertion

length

through

bers

tendons.

a

inner vated

6

well-dened

with

high

have

number

small

of

mitochondria

myobrils,

allowing

and

for

that

are

rapid

singly

access

of

2+

e

global

layer

inserts

into

the

sclera

and

Ca

to

contractile

bers.

ese

are

generally

fast-twitch

and

12

causes

movement

of

the

globe.

e

outer

orbital

layer

is

adjacent

fatigue-resistant

bers,

resulting

in

rapid

contraction

and

sus-

6

to orbital bone, consists of smaller-diameter bers, and is more vas-

tained

tone.

Orbital

bers

that

are

multiply

inner vated

have

11,13

cularized than the global layer.

ese bers end before the mus-

several

ner ve

terminals

along

the

length

of

a

single

ber,

and

6

cle

tendon

and

have

insertions

into

the

muscle

sheath.

e

orbital

they

include

both

fast

twitch

and

slowly

contracting

bers.

6,11,14

layer

of

orbital

the

oblique

layer

inserts

muscles

into

may

encircle

the

connective

tissue

axis

muscle

global

muscle

layer.

pulleys

e

that

can

ORBITAL inuence

distance

the

rotational

between

the

pulley

of

and

the

the

muscle

and

assure

insertion

a

on

CONNECTIVE

TISSUE

STRUCTURES

constant

the

globe

Connective tissue sleeves or pulleys can be identied using mag-

6,12

despite

changes

in

gaze.

e

orbital

layer

bers

make

up

40%

to

netic

resonance

imaging

(Fig.

11.6).

Although

not

as

prominent

15

60% of the bers within an extraocular muscle.

as the pulley of the superior oblique muscle, and only consisting

12

Muscle

istics,

bers

such

as

can

be

location,

divided

size,

into

groups

morpholog y,

based

on

character-

neuromuscular

junc-

of

a

so

tissue,

sleeve

and

the

can

pulleys

aect

encircle

the

each

mechanisms

extraocular

of

muscle

muscle

like

positioning.

2,16–19

tion

type,

or

various

biochemical

properties.

Extraocular

Smooth muscle-connective tissue struts attach the pulleys to the

CHAPTER

178

11

Extraocular

Muscles

Dense

cle

a

connective

sheaths

highly

and

organized

supporting

muscles

the

are

tissue

between

septa

the

network

globe

that

within

anchored

to

between

sheaths

the

the

orbit.

extraocular

orbital

contributes

the

the

and

to

e

periorbita

at

bones

the

form

framework

horizontal

the

mus-

rectus

anterior

orbital

walls through the medial and lateral check ligaments. e medial

check ligament is attached to the bones of the medial orbital wall,

and

on

the

the

lateral

check

zygomatic

posterior

to

the

ligament

bone

of

orbital

is

the

attached

lateral

septum.

e

to

wall.

the

lateral

Both

medial

tubercle

ligaments

check

are

ligament

is

31

better

were

the Fig.

11.6

Inection

of

lateral

rectus

at

muscle

pully

developed

described

globe;

the

slight

bend

in

the

lateral

rectus

muscle

as

is,

the

lateral.

brakes

in

that

Traditionally,

limit

abduction,

the

the

extent

medial

these

of

check

ligaments

movement

ligament

of

stops

(arrow).

lateral Note

that

than

when

the

movement

of

the

globe

when

extension

of

the

medial

rec-

eye

tus muscle starts to exert pull on the relatively inelastic ligament. is

adducted.

In

addition,

the

check

ligaments

support

the

extraocular

muscle

32,33

pully

periorbita

of

the

orbital

wall

and

may

12

tion

the

of

binocular

pulley

is

eye

richly

help

by

rene

coordina-

e

and

help

connective

maintain

tissue

septa

the

globe

that

within

connect

the

orbit.

muscle

to

muscle

26–28

movements.

inner vated

to

system

e

smooth

sympathetic

and

muscle

of

parasympa-

and

periodically

along

a

connect

signicant

individual

portion

of

muscles

the

muscle

to

the

orbital

length

walls

have

been

intermuscular

septa

34–36

thetic ner ves, suggesting both excitator y and inhibitor y capabil-

6

identied

in

dissection

studies.

ese

28

ities.

e

connective

smooth

tissue

or

muscle

moves

either

the

regulates

pulleys

to

the

alter

stiness

the

of

pulling

the

direc-

include

medial

those

joining

rectus;

(2)

the:

(1)

medial

lateral

rectus

rectus,

and

inferior

superior

rectus,

rectus;

and

(3)

lat-

12

tion.

e

sideslip

of

pulleys

the

maintain

extraocular

stability

muscles

of

the

muscle

during

globe

path,

reduce

rotation,

eral

rectus

and

and

rior

oblique

dis-

to

superior

and

to

the

rectus;

orbital

(4)

roof

medial

and

rectus

oor ;

(5)

to

the

medial

supe-

rectus

29

help

to

determine

placement

can

the

eective

clinically

mimic

direction

muscle

of

pull.

Pulley

dysfunction,

and

orbital

imaging may be needed to distinguish it accurately from a palsy.

the

frontoethmoid

lateral

30

e

pulley

for

the

medial

Whitnall

rectus

is

the

most

fully

developed.

periorbita

rectus

of

the

angle;

to

the

ethmoid;

(7)

inferior

lateral

wall;

(6)

superior

rectus

(9)

to

the

levator

to

oblique

orbital

adjacent

(10)

superior

oblique

to

the

orbital

Superior

roof

(Fig.

oblique

nerve

Lacrimal

vein

Lacrimal

gland

Periorbita

Lateral

retinaculum

Oculomotor

nerve,

capsule

branch

oblique

Fig.

11.7

Whitnall

Connecti ve

ligament.

Saunders;

1994.)

tissue

(From

system

Dutton

JJ.

in

cross-section

Atlas

of

the

(8)

perior-

34

and

tendon

Tenon's

oor ;

31

bita;

ligament

Supraorbital

to

Clinical

through

and

Surgical

anterior

orbit

at

Orbit al Anatomy.

the

to

inferior

muscle

level

of

Philadelphia:

11.7).

CHAPTER

Superior

11

Extraocular

Frontal

ophthalmic

179

Muscles

nerve

vein

Superior

oblique

fascial

Superior

system

levator

rectus–

fascial

system

Periorbita Ophthalmic

artery

Lacrimal

Nasociliary

vein

nerve

Lateral

rectus

fascial

system

Medial

rectus

fascial

system

Zygomatic

Inferior

rectus

nerve

fascial

system

Zygomaticofacial

nerve Oculomotor

branch

to

oblique

Fig.

nerve,

inferior

muscle

11.8

Clinical

e

presence

and

Connective

and

Surgical

orientation

of

tissue

Orbital

these

septa

system

Anatomy.

var y

in

cross

section

Philadelphia:

from

front

to

at

midorbit.

Saunders;

the

(From

Dutton

JJ.

Atlas

of

1994.)

rectus

muscles

are

the

superior,

medial,

lateral,

and

infe-

37

back.

bit.

Fig.

e

11.8

shows

considerable

a

representation

amount

of

of

the

attachment

septa

at

midor-

rior

rectus

between

muscle

increases

muscles.

and

shis

e

volume

posteriorly

of

the

during

extraocular

contraction;

38

and

bone

helps

6

to

stabilize

the

muscle

path

and

can

limit

eye

and

moves

whether

ume

or

ANATOMY

OF

muscle

it

decreases

39

relaxation.

It

is

of

four

extraocular

superior

rior

oblique

rectus,

(Figs.

the

in

increase

myobril

Rectus

is

caused

lament

by

increased

unclear

blood

vol-

spacing.

rectus

muscles

Muscles

have

their

origin

on

the

common

ten-

MUSCLES dinous

tus,

volume

THE

e

EXTRAOCULAR

this

changes

Origin

MACROSCOPIC

six

during

34

movement.

e

for ward

muscles

muscles

inferior

11.9

and

are

the

rectus,

medial

rectus,

superior

11.10).

From

lateral

oblique,

longest

to

and

rec-

infe-

shortest,

tissue

apex

part

are

ring

is

of

of

(annulus

continuous

the

the

orbit

and

lower

with

anterior

superior

thickened

of

Zinn).

the

to

orbital

bands

and

tendons

or

is

oval

periorbita

the

optic

ssure.

limbs.

are

e

and

is

foramen

e

sometimes

band

upper

connective

located

and

and

referred

medial

of

to

and

the

at

lower

as

the

medial

the

lateral

areas

upper

rectus

Trochlea

muscles Superior

oblique

take

their

origin

from

both

the

upper

and

lower

parts

muscle

of

Superior

rectus

Medial

muscle

rectus

muscle

the

upper

(Fig.

tendinous

limb,

and

11.11).

ring.

the

e

e

superior

inferior

medial

rectus

rectus

is

and

rectus

is

joined

the

attached

to

the

superior

to

lower

the

limb

rectus

also

37

attach

to

the

CLINICAL

Retrobulbar

nerve.

Lateral

rectus

The rectus

pain

oblique

with

11.9

Globe

in

the

orbit

as

viewed

muscle

from

the

the

optic

neuritis

there

is

are

an

no

ner ve.

Optic

inammation

observable

Neuritis

affecting

fundus

the

sheath

of

this

the

changes

in

the

presenting

optic

condition,

extreme

nerve

eye

sheath

is

movement

supplied

can

with

be

a

one

of

dense

early

sensory

nerve

signs.

network,

and

muscle

eye

of

lateral

side.

the

movement

sensation

Fig.

of

COMMENT: Retrobulbar

optic

general,

optic

because

Inferior

sheath

muscle

but

Inferior

In

dural

of

close

can

pain.

association

cause

of

stretching

muscle

of

the

sheath

optic

and

nerve

optic

sheath,

nerve

sheath,

resulting

in

a

CHAPTER

180

11

Extraocular

Muscles

1

6

5

4 2

3

A

B

Fig.

11.10

cles. The

sinus

stula

rectus;

T he

are a

e ncl o s e d

o c u l om otor

p ass

t h rou g h

Fig.

t he

4:

t he

t he

T he

o c u l omotor

superior

(indicated

t he

c ana l

opt i c

or

for ame n

t he

f rom

by

the

rectus;

bl o o d

hav i ng

ne r ve

magnetic

5:

t he

arrow

r i ng

is

ve ss els

sup e r i or

in

t he

c ana l.

B).

1:

called

6:

t he

f issu re

(s ee

e nte r

sup e r i or

with

larger

superior

e it he r

ar te r y

T he

is

ne r ve s

or bit

or bit a l

imaging

(arrow)

oblique;

and

opht ha l m i c

opt i c

vein

superior

e nte re d

and

resonance

ophthalmic

te nd i nous

S e ve r a l

for ame n ,

opt i c

1 1 . 1 1) .

Coronal T1

medical

by

for am en.

t h rou g h

A,

right

contrast

than

rectus

lacrimal

and

the

and

and

f rom

fou r

t he m .

oblique

of

extraocular

a

lateral

t he

lie

of

of

right

mus-

cavernous

rectus;

sup e r i or

w it h i n

t he

t he

t he

nas o c i l i ar y

re c tus

t ro ch l e ar, Superior

muscle

2:

d iv is i ons

t he

T hus

su r f a c e

Levator

levator;

i n fe r i or

st r u c tu re s

t he

the

because

3:

inferior

gland.

ne r ve,

me n

showing

left

or bit a l

t he

motor

l a c r i ma l,

and

ne r ve

t hat

and

e nte r

f issu re

mus cl e

mus cl e s

mus cl e

o c u l omotor

ne r ve

to

f ront a l

Fig.

t he

re c tus

w it h i n

t he

ne r ve s

and

t he

ab du c e ns

o c u l omotor

1 1 . 1 1) .

are a

c on ne c t ive

e a ch

lies

(s ee

c one,

t he

ne r ve,

t he

e ncl o s e d

t issu e

mus cl e

by

j oi n i ng

e nte rs

mus cl e

t he

for a -

T he s e

c one.

sup e r i or

t he

T he

oph-

muscle

t ha l m i c

ve i n

lie

ab ove

t he

c om mon

te nd i nous

r i ng .

T he y

are

Trochlea Superior

rectus

muscle

out s i d e

t he

mus cl e

c one

(s ee

Fig.

1 0 . 1 8) .

Trochlear

Superior

Insertions

nerve

orbital

of

the

Rectus

Muscles:

fissure

Spiral

Optic

of

Tillaux

nerve

e

four

rectus

muscles

insert

into

the

globe

anterior

to

the

Medial

equator.

A

line

connecting

the

rectus

muscle

insertions

forms

rectus

a

Oculomotor

spiral,

as

described

by

Tillaux.

is

spiral

starts

at

the

medial

muscle nerve

rectus,

the

insertion

that

is

closest

to

the

limbus,

and

proceeds

Common

tendinous Lateral

to

the

inferior

rectus,

the

lateral

rectus,

and

nally

the

supe-

rectus 2

ring muscle

Inferior

rior

rectus,

In

a

recent

in

specic

the

insertion

farthest

from

the

limbus

(Fig.

11.12).

rectus

study,

variations

were

found

from

person

to

person

was

always

muscle Abducens

nerve

measurements,

but

the

spiral

of

Tillaux

40

Inferior Inferior

Fig.

1 1.1 1

orbital

Orbital

oblique

muscle

fissure

apex

with

the

globe

removed.

The

origin

obser ved.

e

merge

scleral

rectus

ner vating

superior

muscles

is

extraocular

orbital

at

the

common

muscles

ssure

and

and

tendinous

the

common

ring.

relationship

tendinous

ring

Ner ves

between

are

bers.

of

A

insertion

sleeve

of

pierce

the

Tenon

capsule

capsule

covers

the

and

ten-

of

don the

with

tendons

for

a

short

distance,

and

the

muscle

can

slide

freely

within

in-

the

shown.

this

ing

sleeve.

them

Connective

to

each

other.

tissue

extends

from

the

insertions

join-

CHAPTER

Superior

11

Extraocular

181

Muscles

rectus

SR SR

T

N

N

T

SO

LR

MR IR

IO

A Lateral

Medial

rectus

rectus

B

SO SR

IR

T

N

LR

IO

IR

IO

Inferior

rectus

C Fig.

11.12

spiral

Insertions

of

the

rectus

muscles

forming

D

the

Fig.

of Tillaux.

11.13

viewed

side.

MR,

Medial

e

Rectus

me dia l

mus cles,

wit h

its

mus cl e

size

is

t he

prob ably

largest

resu lt ing

of

t he

its

and

t he

t he

in

t he

t ive

of

p ar ts

t he

me dia l

t issue

t his

t ion.

convergence.

lower

she at h

lels

At

us e

e

opt ic

orbit a l

pu l le y

p oint,

it

just

mm

f rom

3.7

mm

long

t he

t he

of

wa l l

t he

t he

me dia l

f rom

ver t ica l

t he

approximately

oblique

ab ove

of

t he

mus cle,

t he

t he

mus cle

r un

ner ve

its

re c tus

III,

latera l

t he

is

to

such

bis e c ts

t he

me dia l

it

me dia l

che ck

inner vate d

of

t he

r ing

t hroug h

t he

g lob e

is

is

f rom

p ara l-

conne c-

t he

to

ab out

tendon

a

of

upp er

and

mus cle

e quator

re c tus

g lob e.

its

5.2

ins er-

mm

to

approximately

ins er t ion

t hat

t he

(Fig.

ar ter y,

Fas cia l

o c u lomotor

t he

e

lo cate d

re c tus.

p ass es

and

of

by

t he

ner ve,

f rom

orbit

(s e e

infer ior

w hich

e

t he

of

e

the

B,

oblique;

rectus;

N,

extraocular

above;

IR,

C,

inferior

nasal;

SR,

muscles.

below;

and

rectus;

superior

LR,

The

D,

lateral

rectus;

globe

the

SO,

lateral

rectus;

superior

temporal.

Rectus

lateral

lower

lateralis,

bone.

until

a

e

it

Muscle

rectus

limbs

of

muscle

the

passes

rectus

through

the

equator

of

the

globe

of

to

has

common

prominence

lateral

to

for m

of

medial

t he

e

crania l

mus cle

on

rectus

the

its

its

on

the

globe.

At

the

and

the

tissue

this

e

both

wing

parallels

connective

insertion.

on

ring

greater

muscle

a

origin

tendinous

the

of

the

lateral

pulley

point,

it

insertion

upper

spina

and

recti

sphenoid

orbital

just

follows

parallels

wall

posterior

the

that

cur ve

of

and

is

approximately

6.4

mm

to

6.8

mm

from

the

the

41–44

limbus,

with

a

straight

or

concave

for ward

shape.

e

length

2

of

the

tendon

e

der

of

ner ve,

is

approximately

lacrimal

the

arter y

lateral

and

between

and

rectus

ophthalmic

the

muscle

from

the

muscle

form

the

lateral

sheath

mm.

ner ve

muscle.

arter y

and

check

8.8

lie

the

attach

run

e

medial

optic

to

ligament

along

ciliar y

to

ner ve.

the

lateral

(see Fig.

the

superior

ganglion,

the

lateral

Fascial

wall

10.22).

of

bor-

abducens

rectus,

expansions

the

e

orbit

lateral

and

rec-

tus is inner vated by cranial ner ve VI, the abducens ner ve, which

enters

11.1

T,

Lateral

lie

she at h

10.22).

division

enters

ner ve

t he

and

Fig.

plane

a

sup er ior

nas o ci liar y

t he

ligament

genera l ly

hor izont a l

11.13A).

exp ansions

wa l l

is

sur face.

TABLE

Inferior

of

front;

f re quenc y

b ot h

re c tus

in

41–44

opht ha lmic

me dia l

wel l-de velop e d

me dia l

line

f rom

tendinous

t he

11.1).

st raig ht

it

to

c ur ve

and

is

me dia l

unt i l

2

e ye

e

p oster ior

limbus,

(Table

or ig in

common

ner ve.

fol lows

ins er t ion

5.7

of

Its

A,

ext rao c u lar

37

of

IO,

medial

oblique;

Muscle

re c tus

Insertions

from

Rectus

Muscle

Insertion

Tendon

of

Measurements

on

the

Superior

medial

Rectus

side

of

the

muscle.

Muscle

in e

superior

rectus

muscle

has

its

origin

on

the

superior

part

millimeters of

Tendon

Muscle

Length

Distance

From

Limbus

Tendon

Width

Medial

rectus

3.7

mm

5.5

mm

10.3

Lateral

rectus

8.8

mm

6.6

mm

9.2

mm

the

ner ve.

e

other,

5.8

mm

7.2

mm

10.8

rectus

5.5

mm

6.2

mm

9.8

passes

enclosing

ring

in

and

for ward

these

two

coordination

resulting

additional

of

elevation

the

beneath

muscles

eye

of

sheath

the

are

eyelid

the

levator

with

with

optic

muscle.

connected

movement

the

of

to

each

eyelid

posi-

band

of

this

tissue

connects

to

the

upward

gaze.

superior

con-

mm

junctival

Inferior

muscle

allowing

and

tendinous

mm

An rectus

e

sheaths

tion

Superior

common

fornix.

e

superior

rectus

muscle

parallels

the

roof

of

mm

the

orbit

until

it

passes

through

a

connective

tissue

pulley

just

CHAPTER

182

posterior

to

the

equator

11

of

Extraocular

the

globe.

At

Muscles

this

point,

it

follows

the TABLE

cur ve

of

e

the

globe

insertion

to

of

its

the

superior

41

to

7.5

mm

oblique,

poral

from

with

side

the

the

(see

rectus

side

e

closer

11.13B).

A

is

approximately

6.8

line

to

line

the

of

the

limbus

drawn

from

insertion

than

the

the

origin

Muscle

Nerve

Medial

rectus

along

the

Inferior

tem-

to

degrees

with

muscle

the

will

form

an

angle

of

Lateral

rectus

sagittal

axis.

e

tendon

5.8

e

length

is

oculomotor

(CN

III)

Abducens

rectus

Superior

(CN

VI)

division

of

oculomotor

(CN

III)

rectus

Inferior

division

of

oculomotor

(CN

III)

oculomotor

(CN

III)

concave

for ward,

approxi-

Superior

and

nerve

the

runs

above

nasociliary

the

nerve

superior

and

the

rectus

and

ophthalmic

levator

artery

oblique

Trochlear

(CN

IV)

Inferior

oblique

aspect

below the anterior part of the superior rectus muscle (see Fig. 11.9).

oblique

superior

rectus

is

inner vated

by

the

superior

Inferior

division

of

lie

below. e tendon of insertion for the superior oblique muscle runs

e

of

mm.

frontal

muscles,

division

approximately

2

mately

Innervation

the

Inferior

23

Muscle

is

Superior

insertion

Extraocular

mm

44

limbus.

nasal

Fig.

11.2

insertion.

division

of

of

the

(see

oblique

globe

Fig.

and

is

11.13B).

insertion

starts

fan

e

shaped,

anterior

approximately

border

12

mm

of

the

from

and

superior

the

limbus

45

the

oculomotor

face.

Branches

inner vate

the

ner ve,

pass

which

either

enters

through

the

the

muscle

muscle

on

or

its

inferior

around

it

and

to

levator.

ends

about

18

mm

from

the

limbus.

e trochlea is considered the physiologic or eective origin of

the superior oblique muscle in determining muscle action because

it acts as a pulley and changes the direction of muscle pull. In con-

Inferior

Rectus

Muscle

sidering

the

action

of

the

superior

oblique,

a

line

is

drawn

from

e inferior rectus muscle has its origin on the lower limb of the

the trochlea to the insertion rather than from the anatomic origin

common tendinous ring. Its insertion is about 6.0 mm to 6.3 mm

to

41

from

the

limbus,

with

the

nasal

side

nearer

the

the

insertion.

e

insertion

makes

2

tendon

length

is

approximately

approximately

parallels

the

5.5

superior

A

line

drawn

from

the

physiologic

origin

to

the

44

limbus.

an

angle

of

approximately

55

degrees

with

the

46

mm.

e

rectus,

inferior

making

an

rectus

angle

of

sagittal

rectus,

axis.

with

e

the

superior

nasociliary

oblique

nerve

muscle

and

the

lies

above

ophthalmic

the

medial

artery

lying

23 degrees with the sagittal axis. e inferior rectus muscle paral-

between them. Innervation is by the trochlear nerve, cranial nerve

lels

IV , which enters the posterior area of the muscle.

the

pulley

follows

the

orbital

just

the

curve

insertion

Below

oor

posterior

of

the

of

the

until

to

it

the

the

passes

globe

superior

inferior

through

equator

to

its

rectus

rectus

of

lies

the

a

insertion,

(see Fig.

the

oor

connective

globe.

At

this

which

is

tissue

point,

parallel

it

to

11.13C).

of

the

Inferior

Oblique

Muscle

e inferior oblique muscle has its origin on the maxillar y bone,

orbit

and

above

approximately

2

mm

posterior

to

the

inferior

medial

orbital

rim

47

it

is

the

the

inferior

inferior

and

the

of

oblique

orbital

inferior

division

Lockwood

(see

and

suspensor y

the

lower

with

tarsal

eyelid

downward

to

Fig.

extension

the

(see

unite

anterior

e

between

11.9).

contribute

the

e

sheath

ligament,

position

oculomotor

comes

Fig.

10.21).

from

plate,

gaze.

the

muscle

oor

muscles

of

and

to

the

inferior

sheaths

the

Anteriorly,

of

the

suspensor y

inferior

into

the

coordination

ensuring

rectus

lowering

is

fascia,

rectus

eye

of

inner vated

an

edge

eyelid

the

and lateral to the nasolacrimal canal.

only

rior

to

of

on

inferior

extraocular

orbit.

the

leling

muscle

movement

the

by

two

ligament

inferior

of

rectus

these

capsulopalpebral

of

inserts

allowing

inferior

e

ner ve.

e

lateral

the

muscle

muscle

aspect

tendon

of

of

to

have

runs

the

its

from

globe,

insertion

of

e inferior oblique is the

anatomic

the

its

medial

length

the

origin

in

corner

of

the

approximately

superior

oblique

ante-

the

orbit

paral-

muscle.

e insertion of the inferior oblique is on the posterior portion

of

the

the

cave

in

globe

macular

on

the

area

downward.

length,

with

lateral

(see

e

the

side,

Fig.

mostly

11.13D).

tendon

anterior

of

inferior,

e

insertion

edge

lying

insertion

is

quite

approximately

is

just

short,

15

outer

curved

just

mm

1

to

con-

mm

from

the

45

division of cranial ner ve III, the oculomotor ner ve, which enters

inferior

the

51

limbus.

e

muscle

makes

an

angle

of

approximately

46

muscle

on

its

superior

surface.

degrees

with

the

sagittal

axis.

Above

the

inferior

oblique

are

the inferior rectus and globe, and below it lies the oor of the orbit.

Superior

Oblique

Muscle

e

e superior oblique muscle has its origin on the lesser wing of

the sphenoid bone, medial to the optic canal near the frontoeth-

moid

suture.

e

muscle

courses

for ward

and

passes

through

inferior

oblique

is

innervated

by

the

inferior

division

of

the

oculomotor nerve, which enters the muscle on its upper surface.

Table

11.2

lists

the

motor

inner vation

of

the

and

the

extraocular

muscles.

the trochlea, a U-shaped piece of cartilage attached to the orbital

plate

of

begins

no

the

frontal

connective

allowing

e

the

bone

approximately

the

1

(see Fig.

cm

adhesions

tendon

superior

extraocular

to

exist

slide

oblique

muscles

11.9).

posterior

e

to

the

between

easily

muscle

because

the

of

its

the

two

insertion

and

(2.5

EYE

MOVEMENTS

Normally,

structures,

trochlea.

longest

long

of

trochlea.

these

through

is

tendon

Before

thinnest

cm)

Fick’s

tendon

Axes

a

discussion

of

the

individual

muscles

resultant

eye

of

movements caused by their contraction, it is necessary to dene cer-

of

tain terms. All eye movement can be described as rotations around

supe-

one or more axes. According to Fick, these axes divide the globe into

through

quadrants and intersect at the center of rotation, a xed nonmoving

37

insertion.

rior

rectus

e

tendon

muscle

and

of

insertion

changes

lies

inferior

direction

as

it

to

the

passes

48

the

trochlea

superior

to

run

oblique

in

a

posterior

muscle

attaches

direction.

in

the

e

insertion

superoposterior

of

the

lateral

point

and

venience,

it

the

is

approximate

assumed

that

geometric

the

eye

center

rotates

of

the

around

eye.

this

For

xed

con-

point,

CHAPTER

11

Extraocular

183

Muscles

Z-axis

L

L

M

M L

M

Y-axis

Adduction

L

Elevation

Intorsion

M L

L

Abduction

Fig.

11.15

point

of

M

M

Depression

Duction

reference

eye

for

Extorsion

movements.

eye

The

anterior

pole

is

the

movements.

X-axis

In

vergence

these

each

adducted,

eye

Version

Fig.

and

11.14

Fick

z-axis

is

axes:

x-axis

is

horizontal;

y-axis

is

sagittal;

vertical.

the

is

eyes

gaze,

13.5

mm

behind

the

cornea;

however,

this

point

varies

are

movements

move

in

and

in

the

eyes

disjunctive

and

are

the

in

le

move

divergence

infraversion

opposite

In

each

le-right

convergence

eye

movements

direction.

gaze.

in

movements.

conjugate

same

and levoversion is

elevated,

located

movements,

directions;

is

and

abducted.

occur

Dextroversion

In supraversion both

both

eyes

are

when

is

right

eyes

are

depressed.

in

ametropia. It is slightly more posterior in myopia and slightly more

Positions

of

Gaze

2

anterior

axis

sagittal

e

in

and

hyperopia.

runs

axis

z-axis

from

running

is

the

e

nasal

x-axis

to

from

vertical

is

the

temporal

the

axis

anterior

and

horizontal

(Fig.

11.14).

pole

runs

to

from

or

transverse

e y-axis is

the

posterior

superior

to

the

pole.

inferior.

e primary position of gaze is described as the position of the eyes

when

the

object

of

the

of

head

is

regard

head

and

erect,

is

a

the

located

eyes

at

horizontal

are

the

focused

intersection

plane

passing

for

of

innity,

the

through

and

sagittal

the

the

plane

centers

of

25

When

the

front

of

the

eye

moves

up,

the

back

moves

down.

When

rotation

of

both

eyes.

Secondary

positions

of

gaze

are

rotations

the front of the eye moves right, the back of the eye moves le. e

around either the vertical axis or the horizontal axis. T ertiary posi-

anterior pole of the globe is the reference point used in the descrip-

tions are rotations around both the vertical and the horizontal axes.

tion of any eye movement. Eye movements are described and based

Movements

on the movement of the muscle insertion toward its origin.

One

of

the

From

earliest

ment

is

the

isolated

Movements involving just one eye are called ductions (Fig. 11.15

straightfor ward

and

uation

Table

11.3).

pole

Rotations

of

the

Rotations

anterior

of

pole

the

(depression

Torsions

or

around

globe

(abduction).

down

models

Position

developed

to

explain

eye

move-

50

Ductions

anterior

Primary

around

globe

or

the

medially

up

the

vertical

axis

(adduction)

horizontal

(elevation

or

move

or

axis

the

of

model

extraocular

are

has

model

been

muscles

described

used

and

widely

can

be

by

in

Duane.

the

used

to

clinical

is

eval-

describe

the

laterally

move

the

supraduction)

or

TABLE

11.3

Monocular

Eye

Movement

Terminology

infraduction).

cyclorotations

agonist

rotations

around

the

sagittal

Eye

Movement

Term

axis and are described in relation to a point at the 12-o’ clock posiMedial

tion

on

the

rotation

is

the

superior

of

that

rotation

occur

in

to

horizon.

is

the

an

intorted

limbus.

point

of

that

attempt

to

With

a

Intorsion

nasally,

point

keep

head

approximately

7

and

(inc yclorotation)

extorsion

temporally.

the

tilt

of

30

degrees,

retinal

degrees,

and

the

Adduction

the Lateral

Abduction

Up

Elevation,

(exc yclorotation)

Torsional

horizontal

is

the

supraduction,

or

sursumduction

movements

raphe

parallel

ipsilateral

contralateral

eye

eye

is

Down

Depression,

Rotation

of

12-o’clock

position

Intorsion,

12-o’clock

position

Extorsion,

infraduction,

incyclorotation,

or

or

deorsumduction

incycloduction

medially

49

extorted

approximately

8

degrees. Rotation

of

excyclorotation,

or

laterally

Vergences

and

Versions Anterior

out

of

orbit

Protrusion

or

exophthalmos

Retraction

or

enophthalmos

Movements involving both eyes are either vergences or versions,

Posterior

depending

on

the

relative

directions

of

movement

(Table

11.4).

into

orbit

excycloduction

CHAPTER

184

TABLE

11.4

11

Extraocular

Binocular

Eye

Muscles

Horizontal

Rectus

e

rectus

Muscles

Movement medial

lies

parallel

to

the

y-axis

and

perpendicular

to

Terminology the x-axis and the z-axis; therefore it has only one action, which is Eye

Movement

Term

rotation around the vertical axis in a nasal direction—adduction

Right

Dextroversion

Left

Levoversion

(Fig. 11.16A). e lateral rectus also lies parallel to the y-axis and

perpendicular

rotation Supraversion

Up

Infraversion

Down

or

and

or

a

to

the

x-axis

temporal

and

the

z-axis;

direction—abduction

contraction

(Fig.

causes

11.16B).

sursumversion

deorsumversion

Vertical

Up

in

Rectus

Muscles

Dextroelevation

right

e action of the superior rectus is more complex than that of the

Up

and

Down

Levoelevation

left

and

medial and lateral rectus muscles because it lies at an angle to each

of

Dextrodepression

right

the

axes.

Because

the

insertion

is

above

the

origin

and

on

the

anterior globe, movement around the horizontal x-axis causes eleDown

and

Levodepression

left

vation.

Both

eyes

e

muscle

insertion

is

lateral

to

the

origin,

so

movement

Convergence

adduct

around the vertical z-axis causes adduction. e oblique insertion

Both

eyes

abduct

Divergence

Both

eyes

extort

Excyclovergence

Both

eyes

intort

Incyclovergence

on

the

superior

surface

of

the

globe

causes

intorsion

on

contrac-

tion (Fig. 11.17A). e primary action of the superior rectus is said

to be elevation. Adduction and intorsion are secondary actions.

e primar y action of the inferior rectus is depression because Rotation

of

12-o’clock

position

to

right

Dextrocycloversion

the insertion is below the origin and on the anterior of the globe.

Rotation

of

12-o’clock

position

to

left

Levocycloversion

Secondar y

eral

to

the

insertion

movement

muscle.

around

However,

the

it

is

axes

that

occurs

important

to

with

contraction

remember

that

of

during

Oblique

eye

e

traction

sion.

and

it

is

strictly

hypothetical

to

the

adduction,

extorsion,

inferior

surface

because

which

of

the

the

results

globe

insertion

from

(Fig.

the

is

lat-

oblique

11.17B).

discuss

Muscles

primar y

2

relaxation,

on

are

and

each

movements, all six extraocular muscles are in some state of con-

or

actions

origin,

25

action

of

the

superior

oblique

muscle

is

intor-

51–53

is

action

Contraction rotates the eye around the y-axis, causing intorsion.

e secondar y actions are depression and abduction. Depression

summarized

TABLE

in

Table

11.5

eye

begins

actions

of

in

each

primar y

occurs

Origin,

Insertion,

and

Origin

Medial

rectus

Common

tendinous

ring

and

optic

Lateral

rectus

Common

tendinous

ring

and

greater

Common

tendinous

ring

and

optic

Common

tendinous

ring

Inferior

Superior

Inferior

rectus

rectus

oblique

oblique

muscle

11.5

Muscle

Superior

position.

extraocular

Anatomic:

Medial

lesser

wing

maxillary

bone

Action

nerve

of

the

Extraocular

sheath

wing

nerve

of

sphenoid

sheath

sphenoid;

trochlea

is

posterior

and

Adduction

None

globe

Abduction

None

Elevation

Adduction,

intorsion

Depression

Adduction,

extorsion

Intorsion

Depression,

Extorsion

Elevation,

anterior

anterior

globe

globe

posterior,

posterior,

lateral

lateral

globe

globe

Action

Secondary

M

L

M

L

Medial

Lateral

rectus

rectus

M

B

the

11.16

medial

lateral

Eye

movements

rectus

rectus

muscle

muscle

with

of

with

the

the

the

eye

horizontal

eye

in

in

rectus

primar y

primar y

muscles.

position.

position.

L,

B,

A,

Adduction

Abduction

Lateral;

M,

on

medial.

on

contraction

contraction

of

of

the

Action

abduction

abduction

Abduction

A

the

Muscles

globe

Superior,

L

to

Anterior

Inferior,

M

Fig.

inferior

11.5).

Anterior

Adduction

L

insertion

Table

Primary

Superior,

Physiologic:

the

(see

Insertion

Inferior,

of

because

globe

on

are

the

secondar y

the

insertion

e

descriptions

of

oblique

of

and

aspect

the

the

these

lateral

from

the movement of the eye as if only one muscle contracts. In each

primar y

posterosuperior

results

CHAPTER

Elevation

Extraocular

L

M

L

M

Superior

23°

L

M

L

M

L

M

Inferior

23°

rectus

rectus

Adduction

Adduction

M

L

185

Muscles

Depression

M

L

11

L

M

L

M

Superior

23°

23°

rectus

Inferior

rectus

Intorsion

Extorsion

M

L

L

M

L

M

Superior

23°

23°

rectus

Inferior

rectus

A

B

Fig.

11.17

rectus

rior

rectus

middle,

B,

in

ment

of

the

eye

origin.

up,

and

muscle,

primar y

around

associated

Globe

the

movement

eye

movement

around

position.

the

anterior

A,

with

movement

Contraction

the

movements

muscles.

adduction,

Globe

eye

physiologic

Eye

(B)

z-axis;

of

the

pole

primar y

around

each

T op,

in

of

the

Fick’ s

z-axis;

Depression,

extorsion,

muscle

pulls

down.

the

contraction

each

position.

axes

bottom,

moves

with

around

on

is

lateral

to

the

trochlea,

contraction

of

the

around

pulls

the

back

of

the

globe

medially,

thus

t he

pole

laterally

primar y

(Fig.

action

because

the

moving

globe,

and

the

Secondar y

insertion

traction

is

the

muscle

inferior

wraps

insertion

actions

pulls

Abduction

on

the

occurs

the

is

are

of

because

supe-

the

x-axis;

around

the

y-axis.

rectus

muscle,

with

adduction,

lateral;

M,

the

move-

medial.

Secondary

t he

g lob e

Positions

changes,

or ig in

and

ins er t ion

t he

rel at ionship

changes

rel at ive

to

b et we en

Fick’s

of

a

mus cle

has

a

dierent

ee c t

t han

axes,

w hen

e ye

is

in

around

elevation

the

the

eye

eye

the

and

and

and

lower

lateral

portion

to

abduction.

above

down,

insertion

pr imar y

p osit ion.

If

t he

e ye

is

ele vate d,

cont rac -

oblique—extorsion—

superior

posterior

back

of

cont rac t ion

of

t he

the

the

on

the

back

re c tus

mus cles

no

longer

or

ab duc t ion,

but

a ls o

c aus es

the

of

c aus es

a

slig ht

st r ic t ly

ele vat ion.

If

orie ye

is

depress e d,

cont rac t ion

of

eit her

B ecause

origin,

elevating

hor izont a l

of

of

t he

hor izont a l

55

re c tus

the

inferior

the

11.18A).

of

t he

gin.

L,

of

around

middle,

From

and

the

adduc t ion

the

y-axis.

p osit ion

mus cle

t ion

occurs

the

movement

inferior

x-axis;

(A)

contraction

superior

t he

e

the

Movements

and

anterior

the

on

the

t he

oblique

of

superior

movement

intorsion,

around

As

insertion

the

axes

Elevation,

bottom,

movement

back

T op,

of

Fick’ s

contraction

movement

Because

of

mus cles

c aus es

f ur t her

depression.

con-

front.

the

eye

Vertical

With

Rectus

the

eye

Muscles

abducted

approximately

23

degrees

from

primar y

is pulled toward the medial side; thus the anterior pole is moved

position, the vertical rectus muscles parallel the y-axis and lie per-

laterally

pendicular

causing

abduction

(Fig.

11.18B).

Some authors oer the contrasting view that the primary action

of

the

superior

oblique

is

depression,

that

of

the

inferior

oblique

to

the

x-axis;

thus

elevation,

and

contraction

54

is elevation, and the torsional actions are secondary movements.

only

vertical

movement

will

occur.

In this position, contraction of the superior rectus will cause only

depression

(Fig.

11.19A).

of

the

inferior

rectus

will

cause

only

CHAPTER

186

11

Extraocular

Muscles

Intorsion

Extorsion Inferior

L

M

L

oblique

M

M

55°

L

M

L

M

51°

Superior

oblique

Depression

Elevation

Inferior

oblique

55°

M

L

L

M

L

M

51°

55°

Superior

oblique

Abduction

Abduction

Inferior

M

L

L

oblique

M

L

M

L

M

51°

55°

Superior

oblique

A

B

Fig.

(B)

rior

1 1.18

oblique

oblique

middle,

B,

eye

ment

movements

muscles.

muscle,

depression,

Globe

the

Eye

primar y

around

the

Globe

with

the

around

position.

x-axis;

with

movement

eye

movement

movement

in

A,

associated

in

T op,

bottom,

around

primar y

around

each

of

the

Fick’ s

contraction

each

position.

x-axis;

axes

of

T op,

bottom,

on

of

movement

abduction,

movement

around

around

Abduction

the

the

the

on

movement

inferior

y-axis;

z-axis.

(A)

and

contraction

movement

abduction,

of

superior

axes

Intorsion,

contraction

Extorsion,

the

Fick’ s

around

inferior

the

the

around

oblique

middle,

L,

of

the

z-axis.

muscle,

elevation,

lateral;

supe-

y-axis;

M,

with

move-

medial.

Adduction

y-axis

to

SR

M

is

parallel

muscle

M

L

L

y-axis

is

perpendicular

to

A

Fig.

11.19

axes

the

Relationship

when

plane

the

of

eye

the

muscle

causes

vertical

rectus

cannot

SR

muscle

B

cause

is

in

vertical

only

between

a

rectus

elevation.

muscles

elevation.

the

secondary

muscles

B,

When

perpendicular

L,

line

Lateral;

M,

of

position.

parallel

the

to

eye

the

medial;

vertical

A, When

to

is

the

the

muscle

eye

y-axis),

adducted

y-axis),

SR,

rectus

movement

abducted

contraction

67

degrees

contraction

superior

is

of

rectus.

the

of

23

the

(putting

and

degrees

superior

the

superior

plane

rectus

Fick’s

(putting

rectus

of

the

muscle

CHAPTER

Adduction

11

Extraocular

187

Muscles

Abduction y-axis

is

perpendicular

to

M

L

M

y-axis

is

to

muscle

SO

the

of

the

Relationship

is

in

exclusively

cause

As

the

eye

adducts,

a

oblique

oblique

between

secondary

muscles

causes

muscles

parallel

depression.

L,

approaches

Lateral;

a

the

position.

to

the

to

M,

position

line

A,

the

oblique

y-axis),

the

SO,

the

the

muscle

eye

is

is

of

abducted

contraction

superior

movement

adducted

contraction

eye

y-axis),

medial;

where

of

When

B, When

perpendicular

depression.

it

L

B

11.20

eye

muscle

parallel

A

Fig.

SO

of

the

35

55

superior

degrees

the

and

degrees

Fick’s

oblique

(putting

superior

axes

(putting

muscle

the

oblique

when

the

plane

almost

plane

muscle

of

the

cannot

oblique.

plane

of the vertical rectus muscles is at a right angle to the y-axis. is

occurs

be

at

approximately

physically

straints

of

muscles

x-axis,

not

is

the

orbit).

at

right

a

contraction

cause

Oblique

67

impossible

vertical

If

the

angle

of

degrees

because

the

of

muscle

to

the

or

(Fig.

adduction

(which

connective

plane

y-axis,

superior

movement

of

the

of

and

the

vertical

thus

inferior

con-

rectus

parallel

rectus

may

tissue

to

muscle

the

will

11.19B).

Muscles

A

As

the

cles

eye

adducts

becomes

(Fig.

11.20A).

depression,

51

parallel

In

this

and

the

to

to

55

the

degrees,

y-axis

position,

inferior

the

and

the

plane

of

the

oblique

perpendicular

superior

oblique

to

oblique

will

cause

only

will

the

mus-

x-axis

cause

only

elevation.

When the eye is abducted 35 to 39 degrees, the plane of the oblique

muscles makes a right angle with the y-axis and parallels the x-axis,

and the obliques cannot cause vertical movement (Fig. 11.20B).

is analysis is used in the clinical assessment of extraocular mus-

cle

function.

depressing

elevating

As

the

As

the

abilities

and

eye

eye

of

increases

the

depressing

increasingly

in

vertical

abilities

moves

abduction,

rectus

of

into

the

the

muscles

oblique

elevating

increase

muscles

adduction,

the

and

as

the

decrease.

elevating

B

and

depressing abilities of the oblique muscles increase as the elevating

and depressing abilities of the vertical rectus muscles decrease.

CLINICAL

COMMENT: Brown

Superior

Oblique

Sheath

Syndrome

Inability to elevate the eye in the adducted position is usually caused by a dysfunc-

tional

inferior

by

immobile

an

oblique

muscle.

superior

However,

oblique

such

muscle

(Fig.

a

limitation

11.21).

could

Using

also

be

caused

electromyography,

56

Brown

determined

that

a

patient

with

an

inability

to

elevate

the

eye

in

adduc-

tion had a functional inferior oblique muscle, but that the movement of the supe-

rior

oblique

lengthen

through

when

the

the

trochlea

inferior

was

oblique

restricted.

contracted.

The

In

superior

congenital

oblique

Brown

could

not

C

syndrome,

Fig. the

cause

could

be

a

short

or

tightly

anchored

tendon.

This

may

be

caused

11.21

straight abnormal

development

of

the

superior

oblique

tendon-trochlea

57

is

dependent

on

normal

development

of

cranial

nerve

complex

the

cause

could

51

trochlea

and

the

59

be

an

accumulation

of

IV.

uid

or

in

duction. In

acquired

tissue

primar y

syndrome

position.

B,

of

left

There

eye.

is

A,

limited

The

eyes

elevation

are

in

ad-

which

58

C,

There

is

normal

elevation

in

abduction.

The

forced

Brown

duction syndrome,

Brown

by

between

test

while

elevating

globe

in

adduction

was

positive

(not

the

shown).

(From

Kanski

JJ,

Nischal

KK.

Ophthalmology:

Clinical

tendon.

Signs

and

Differential

Diagnosis.

St

Louis:

Mosby;

1999.)

CHAPTER

188

11

Extraocular

Muscles

SR

IO

Agonist

and

In

any

is

controlled

each

Antagonist

position

muscle

single

is

muscle

antagonists,

control

of

in

inner vation

or

to

by

some

acts

the

stage

alone.

provide

In

for

Sherrington’s

of

of

extraocular

ner vous

contraction

all

work

these

smooth,

law

all

central

Muscles

synergists.

should

According

gaze,

precisely

SR

IO

Muscles

of

or

and

relaxation.

together

as

movements,

continuous

reciprocal

muscles

system,

MR

LR

MR

LR

No

agonists,

ne

SO

IR

IR

SO

motor

movements.

inner vation,

conA

traction

of

a

muscle

is

accompanied

by

a

simultaneous

and

60

proportional

relaxation

of

the

antagonist.

In

adduction,

the SR

increased

nied

by

rectus

contraction

the

of

increased

the

medial

relaxation

rectus

of

the

muscle

is

antagonist,

IO

IO

SR

SO

IR

accompa-

the

lateral

muscle.

When

muscle

the

superior

contract

at

rectus

the

same

muscle

time,

and

the

the

inferior

adduction

oblique

action

of

the

superior rectus and the abduction action of the inferior oblique,

as

well

of

as

the

tant

the

intorsion

inferior

eye

of

oblique,

movement

is

the

will

superior

rectus

counteract

elevation.

e

and

each

the

other.

muscles

are

extorsion

e

resul-

synergists

in

elevation.

IR

When

the

stimulated

superior

oblique

simultaneously,

and

the

inferior

eye

will

rectus

move

muscles

directly

SO

are

downB

61

ward.

e

superior

oblique

and

the

inferior

rectus

are

syner-

Fig.

gists

in

depression.

e

superior

oblique

is

the

antagonist

A,

the

inferior

oblique

in

vertical

movements

and

torsional

11.22

Direc tion

but

is

synergistic

for

In

primar y

position,

the

muscles

are

in

a

balanced

contraction

the

palpebral

deviated

the

ssure.

from

antagonist

muscle

is

tioned

eral

primar y

of

the

paralyzed,

temporally

rectus

If

sucient

one

to

muscle

position

in

keep

eye,

because

in

of

is

the

eye

inactive,

the

dysfunctional

the

centered

Assessment

the

the

direction

muscle.

primar y

If

the

eye

of

will

the

will

action

in

and

B,

eye

is

of

ple,

the

rectus

and

the

be

of

be

pull

medial

position,

unopposed

COMMENT: Extraocular

of

the

eye

rst

xate

target

cle

a

indicate

unopposed

each

muscle

Ocular

position

integrity

practitioner

on

posi-

the

lat-

IO,

of

notes

by

of

and

the

the

straight

an

the

testing

eye

can

the

eye

Cur ved

tha t

tha t

mus c l e

contraction

p rim a r y

a s s es sme n t .

of

p o si t i on .

c o n tr a c ts ,

a rrows

cause

or

th e

e a ch

For

eye

represent

SO,

IR,

ve rt ic a l

a b d u c ted .

causes

c a u s in g

oblique;

rectus ;

of

each

eye

ahead.

An

eye

that

lateral

rectus

rectus. Fig.

is

in

provides

primary

further

while

is

important

associated

directing

deviated

muscle,

11.22A,

an

and

and

shows

a

the

tool

the

de-

The

patient

toward

medial

in

nerves.

the

rectus

direction

of

to

nose

mus-

pull

ment

ocular

muscles.

Evaluation

of

m us c l e

ex a m pl e,

will

m ove

cannot

adduct,

the

move

into

the

problem

abducted

tors ion a l

inferior

superior

In

e l eva t i o n

d e pre s si on

m ove-

w he n

a d d u ct i o n ,

is

is

rec tus;

oblique;

m ovem en t

the

th e

LR,

SR,

fo r

the

ex a m-

i nfe r i o r

obl i q ue,

superior

ob l iq ue.

lateral

rec tus;

superior

MR,

rec tus.

eye

about

the

movement

is

contractile

lies

with

the

medial

be

the

position,

the

problem

lies

testing,

vertical

a

elevator

are

represented

motility

Using

primary

muscles

by

is

the

and

of

depressor.

primary

“H”

these

elevator

diagrams

important

abilities

testing

small

it

the

to

In

the

and

in Fig.

move

the

muscles.

11.22B.

eyes

The

abducted

depressor.

to

usual

position,

This

Thus

such

a

manner

when

doing

position

of

the

arrange-

as

to

performing

follows:

target,

usually

a

bead,

the

patient

is

instructed

to

follow

the

The

horizontal

and

to

the

far

ability

left,

is

determined

noting

any

rst

inability

by

of

moving

either

the

eye

to

bead

to

the

far

right

follow.

abiliIn

left

gaze,

the

bead

is

elevated

to

determine

the

ability

of

the

left

superior

straightforward.

rectus.

If

the

(left

with

the

lateral

eye

is

abducted)

and

the

right

inferior

oblique

(right

eye

is

ad-

eye The

bead

is

depressed

to

determine

the

ability

of

the

left

inferior

recand

the

right

superior

oblique

muscles.

muscle. 4.

With

way

the

to

which

more

complex

determine

one

muscle

a

movements

dysfunctional

is

the

primary

if

up

target.

2.

information

horizontal

the

motility

isolate

of

position.

can

ocular

1.

are

rectus

rectus tus

in

muscle

a ddu c te d

mus c le

ducted). cannot

intort.

mus cle

rectus If

rectu s

Mus c les

Inferior

vertical

Assessment

be

muscles

position

lateral

the

Muscle

movements

extraocular

underactive

when

motility

the

orig in a ting

either

medial

3. ties

on

in

muscles

would

ex tr a oc ul a r

muscle.

CLINICAL

termining

eye

s uperior

ments.

the

for

m ove m e n t

state, and

exerting

eye

abduction. the

each

of

movewith

ments

Schematic

for

of

the

muscle

actor.

In

is

other

to

the

muscles,

put

the

eye

adducted

the

into

most

a

position,

reliable

position

the

in

oblique

In

right

perior

is

gaze,

rectus

adducted).

inferior

the

bead

(right

The

rectus

and

eye

bead

the

is

elevated

is

is

left

to

abducted)

depressed

superior

determine

and

to

the

the

left

determine

oblique

ability

inferior

the

muscles.

of

the

oblique

ability

of

right

(left

the

su-

eye

right

CHAPTER

the CLINICAL

patient

is

diagnosed

with

strabismus

when

the

visual

axes

are

not

the

the

is

patient

is

asked

to

look

in

the

primary

position

and

two

eyes

movement

coordinated

acquired.

In

adaptation

train

the

gery.

If

between

congenital

response

muscle

the

and

to

the

two

forms

to

of

prevent

achieve

dysfunction

is

eyes.

This

strabismus,

diplopia.

binocular

acquired,

can

suppression

Suppression

vision

the

condition

even

if

causative

is

must

the

be

congenital

often

be

factor

must

used

overcome

treatment

be

are

simultaneous.

normally

us

symmetric.

the

In

movements

dextroversion,

and

simultaneous

right

lateral

rectus

is

supplied

and

le

to

medial

the

yoke

rectus;

in

or

as

an

to

re-

includes

inner vation

is

muscles—the not

equal

189

Muscles

straight

equal when

eyes

Extraocular

COMMENT: Strabismus

of A

two

11

convergence,

to

the

yoke

equal

and

simultaneous

muscles—the

right

inner vation

medial

rectus

is

and

supplied

le

medial

rectus.

sur-

determined.

Compartmentalization Surgical

correction

for

strabismus

can

be

complicated

because

of

the

extensive

Although connective

tissue

network

linking

extraocular

muscles

to

each

other

and

to

clinical

orbital bones. This may be one of the reasons why a patient reverts to a presurgi-

62

cal

strabismic

muscle

posture.

sheath

and

The

realization

connective

tissue

that

there

sheath

of

are

the

connections

globe,

not

between

just

at

the

the

tendon

insertion,

should

be

a

consideration

in

muscle

resection

simplied

situations

tributor

the

during

to

model

identify

discussed

specic

eye

the

muscle

earlier

that

movements,

the

is

is

the

used

major

in

responses

con-

of

each

extraocular muscle are more complex. Although not universally

point

62

of

the

the

1

surgery.

accepted,

there

is

partmentalized,

evidence

allowing

that

for

extraocular

great

muscles

specialization

are

and

com-

multiple

muscles responses. e horizontal extraocular muscles are com-

CLINICAL

Graves

COMMENT: Graves

disease,

a

condition

Disease

associated

with

partmentalized

thyroid

dysfunction,

can

affect

the

rior

areas

of

into

mostly

inner vation.

nonoverlapping

e

ner ves

superior

inner vating

and

infe-

the

superior

before

entering

extraocular muscles. Enlargement of the extraocular muscles produced by Graves

oblique

disease

matory

is

caused

cells

and

by

chronic

inammatory

glycosaminoglycans.

The

inltration

of

hydrophilic

the

muscles

nature

of

the

with

and

inferior

oblique

muscles

bifurcate

inam-

the

respective

muscles.

has

a

branch

e

lateral

third

of

the

inferior

rectus

glycosamino-

separate

of

inner vation

in

addition

to

the

diuse

63 64

glycans results in edema and proptosis.

In addition, restricted ocular motility is 65

arborization

that

supplies

all

inferior

rectus

muscle

bers.

No

evident. Customary evaluation of the restricted eye movement may not depict the

evidence

of

compartmentalization

has

been

found

in

the

supe-

correct dysfunctional muscle because brosis of the muscles can limit muscle ac39

rior

65

rectus.

tivity. For example, if the medial rectus is brotic, eye movement may be restricted

C ompartmentalization in

as

the

a

lateral

check

direction

on

lateral

because

the

movement.

medial

rectus

Restriction

may

is

unable

appear

to

to

elongate

be

an

and

control

of

the lateral rectus but may actually be caused by the brotic medial rectus muscle.

A

forced

lowing

grasp

duction

the

the

test

can

instillation

conjunctiva

of

be

performed

topical

near

the

if

a

brotic

anesthesia,

limbus

and

the

muscle

is

practitioner

attempts

to

move

suspected.

uses

the

in

extraocular

and

width

of

the

the

capability

muscle

bers.

the

extraocular

of

is,

ability

muscle

dierential

and

along

to

with

selectively

tendon

diverse

the

position

insertion,

allows

oculorotar y

func-

Fol-

forceps

eye

implies

acts

impairment

the

tions

for

a

point

may

given

muscle.

e

functional

pull

on

the

insertion

to

shi

depending

on

eye

orientation.

For

example,

the

di-

medial

superior

oblique

bers

attach

near

the

equator

and

are

rection of the restricted movement. Resistance will be met if the cause is bro-

sis,

but

if

the

muscle

is

paralyzed,

the

eye

can

be

moved

easily.

For

example,

responsible

if

the patient is unable to abduct the eye, the practitioner would attempt to move

posteriorly,

the

ner ve

eye

curs.

If

laterally.

the

lateral

If

the

medial

rectus

is

rectus

paralyzed,

is

brotic,

the

eye

resistance

can

be

moved

to

movement

with

the

oc-

for

torsional

allowing

branches

may

rotation;

vertical

provide

the

lateral

movement.

a

bers

e

mechanism

for

insert

two

more

trochlear

these

separate

39

forceps.

movements.

the

medial

Similarly,

rectus

the

show

inferior

dierent

and

superior

contractile

bers

behavior

within

during

39

infraduction

Yoke

and

supraduction.

C ontractile

changes

occur

in

Muscles the

inferior

(not

superior)

compartment

of

the

lateral

rectus

66

Y oke

to

muscles

cause

equal

are

those

binocular

inner vation

muscles

of

movements

states

that

the

(Fig.

the

two

eyes

11.23).

inner vation

acting

Hering’s

to

the

SR

LR

Kanski

Six

LR,

JJ.

muscles

the

of

account

of

eral

orbit

for

rectus

the

is

cardinal

lateral

Clinical

extorted.

vertical

is

deviation

compartmentalization

that

IO

positions

rectus;

MR,

of

Ophthalmology,

ed

SO

gaze

medial

and

rectus;

3.

yok e

SO,

Oxford,

UK:

LR

IR

muscles.

superior

be

SR

MR

SO

can

palsy.

MR

11.23

rectus;

law

when

IO

IR

Fig.

together

IO,

oblique;

Inferior

SR,

oblique;

superior

Butter worth-Heinemann;

IR,

inferior

rectus.

1995:

p.

(From

429.)

seen

with

a

can

lat-

190

CHAPTER

Complexity

of

Some

the

controversy

11

Extraocular

Oblique

exists

Muscles

Muscles

concerning

the

Other

horizontal

abilities

of

a

age-related

greater

variety

the inferior oblique muscle. e relationship of the muscle plane

the

muscle,

of the inferior oblique with the vertical axis determines whether

lipofuscin,

in

changes

ber

increased

in

sizes,

adipose

extraocular

increased

tissue

in

muscles

connective

the

bundles,

include

tissue

in

deposits

of

72

the

inferior

plane

aid

lies

in

oblique

in

front

adduction.

is

of

an

adductor

the

With

vertical

or

an

axis,

increasing

abductor.

the

lateral

If

inferior

the

of

will

the

a

point

will

be

reached

at

which

the

inferior

changes.

REFERENCES

eye, 1.

however,

degenerative

muscle

oblique

movement

and

McLoon

LK,

Vicente

A,

Fitzpatrick

KR,

etal.

Composition,

oblique architecture,

and

functional

implications

of

the

connective

tissue

plane is put behind the vertical axis, causing the inferior oblique network

of

the

extraocular

muscles.

Invest

Ophthalmol

Vis

Sci.

46

then

to

aid

in

abduction.

Animal

studies

in

which

the

muscles 2018;59:322–329.

are

stimulated

directly

either

singularly

or

collectively

seem

to 2.

61

support

this

oblique

were

occurred.

be

When

stimulated

In

some

complete

do

the

positions,

not

superior

oblique

simultaneously,

antagonists,

obser vations

Eggers

and

change

these

no

two

model

ocular

muscles

abduction

the

and

did

used

not

inferior

In:

movement

appeared

occur.

clinically.

In

to

the

obliques

are

responsible

abduction

the

vertical

3.

Guyton

for

elevation

and

AC.

Saunders;

in

and

depression.

recti

are

responsible

Jaeger

anatomy

4.

vol

EA,

1.

eds.

of

the

Duane’s

extraocular

muscles.

Philadelphia:

Textbook

of

Medical

Foundations

Lippincott;

Physiolog y.

of

Clinical

1994.

8th

ed.

Philadelphia:

1991:76.

Wirtschaer

Wobig

JD.

JL,

Neuroanatomy

Wirtschaer

JD,

of

the

eds.

ocular

muscles.

Ophthalmic

In:

Reeh

Anatomy.

San

depression,

Francisco:

and

Functional

W ,

Ophthalmolog y,

ese

adduc-

Tasman

MJ,

tion

HM.

67

view.

for

American

Academy

of

Ophthalmolog y ;

1981:267.

elevation 5.

Karatas M. Internuclear and supranuclear disorders of eye move-

ments:

clinical

features

and

causes. Eur

J

Neurol.

2009;16:1265–

1277.

6.

INNERVATION

AND

BLOOD

SUPPLY

Porter

JD,

Kaufman

St

Louis:

Andrade

PL,

Alm

Mosby ;

FH,

A,

Baker

eds.

RS.

Adler’s

e

extraocular

Physiolog y

of

the

muscles.

Eye,

10th

In:

ed.

2003:787.

Innervation 7.

e

are

medial

rectus,

inner vated

by

inferior

the

rectus,

inferior

and

division

inferior

of

the

oblique

muscles

oculomotor

JR,

extraocular

Kjellevold

muscles

Haugen

and

their

IB.

How

ner ves

does

aect

the

their

structure

function.

of

Eye.

2015;29:177–183.

ner ve.

e superior rectus muscle is inner vated by the superior division

Bruenech

8.

Ruskell

GL.

tion.

Prog

Weir

CR,

Extraocular

Retin

Eye

Res.

muscle

proprioceptors

and

propriocep-

1999;18(3):269.

of the oculomotor ner ve. e lateral rectus muscle is supplied by

9.

the

abducens

ner ve.

e

superior

oblique

muscle

is

inuence

by

the

trochlear

ner ve

(see Table

11.2

and

Fig.

Knox

PC,

Dutton

GN.

Does

extraocular

proprioception

inner vated oculomotor

control.

Br

J

Ophthalmol.

2000;84:1071–

11.11). 1074.

10.

Blood

Lienbacher

in

e

extraocular

muscles

are

supplied

by

two

muscular

extraocular

the

superior

and

the

ophthalmic

and

lateral

medial

arter y :

rectus

branch

e

and

lateral

the

and

various

the

inferior

supplies

oblique

contributions

to

the

branch

superior

the

supplies

oblique

inferior

68

tus

Horn

AKE.

and

muscles:

a

Palisade

endings

comparison

with

and

proprioception

skeletal

muscles.

Biol

branches Cybern.

from

K,

Supply

the

11.

muscles,

medial

Wasicky

human

rec-

2012;106:643–655.

R,

Ziya-Ghazvini

extraocular

chemical

study.

F ,

Blumer

muscles:

Invest

a

R,

etal.

Muscle

histochemical

Ophthalmol

Vis

Sci.

and

ber

types

of

immunohisto-

2000;41(5):980.

69

muscles.

Other

extraocular

arteries

muscle

blood

make

12.

Demer

rectus

supply,

JL,

Oh

SY ,

Poukens

extraocular

muscle

V .

Evidence

pulleys.

for

Invest

active

control

Ophthalmol

Vis

of

Sci.

2000;41:1280.

including

the

lacrimal,

supraorbital,

and

infraorbital

arter-

13.

ies.

ese

vessels

and

the

muscles

they

supply

are

described

Oh

SY ,

tion

Chapter

12

(see

Table

Poukens

V ,

Cohen

MS,

etal.

Structure-function

correla-

in of

laminar

vascularity

in

human

rectus

extraocular

muscles.

12.2). Invest

14.

Ophthalmol

Vis

Sci.

2001;42:17.

Kono R, Poukens V , Demer JL. Superior oblique muscle layers in

monkeys and humans. Invest Ophthalmol Vis Sci. 2005;46:2790–2799.

AGING

CHANGES

IN

THE

EXTRAOCULAR

15.

Oh

SY ,

Poukens

V ,

Demer

layers

JL.

extraocular

muscle

in

mol

2001;42:10–16.

Quantitative

monkey

and

analysis

humans.

of

rectus

Invest

Ophthal-

MUSCLES

Both

horizontal

age,

with

the

tus.

is

may

rectus

medial

muscles

rectus

contribute

are

displaced

to

the

displaced

more

impaired

inferiorly

than

the

ability

to

with

lateral

16.

the

Breinin

17.

Peachy

mals.

eyes

commonly

obser ved

in

elderly

persons

and

may

Eye

them

to

an

incomitant

(nonconcomitant)

superior

rectus

and

inferior

rectus

muscles

of

L.

In:

e

the

e

structure

duality

structure

Bach-y-Rita

and

function

concept.

P ,

of

the

Am

J

of

extraocular

Collins

CC,

extraocular

Ophthalmol.

muscle

Hyde

JE,

eds.

muscle:

Movements.

do

not

bers

e

of

mam-

Control

New

Y ork:

Academic

Press;

of

1971:47.

Montagnani

S,

De

Rosa

P .

Morphofunctional

features

of

human

change extrinsic

ocular

muscles.

Doc

Ophthalmol.

1989;72(2):119.

30

locations. 19.

As

orbital

connective

tissue

loses

strength,

there

is

a

Porter

JD.

Extraocular

displacement

of

the

horizontal

pulleys

and

the

20.

tissue

band

displacement

between

can

result

the

in

lateral

and

divergence

superior

rectus.

insuciency

repertoire.

Ann

N

Y

cellular

Acad

adaptations

Sci.

for

a

diverse

2002;956:7.

connec-

70

tive

muscle:

slight functional

inferior

an

1971;71:1.

strabismus. 18.

e

GM.

predis-

30

pose

Sci.

appraisal

rec-

elevate

Vis

Brandt

DE,

Leeson

CR.

Structural

dierences

of

fast

and

71

is

esotropia.

slow

bers

in

1966;62:478.

human

extraocular

muscle.

Am

J

Ophthalmol.

CHAPTER

21.

Scott

AB,

muscle.

22.

Liu

J-X,

plate

Collins

Arch

in

CC.

Division

Ophthalmol.

Domellöf

human

FP .

A

of

labor

in

human

extraocular

to

1973;90:319.

novel

extraocular

type

of

muscles.

Namba

T,

multiterminal

Invest

motor

Ophthalmol

Vis

end-

43.

Sci.

Hess

and

muscle.

T,

Grob

D.

Neurolog y.

Further

morphological

“en

grappe”

ner ve

bers

Motor

ner ve

endings

in

human

endings

44.

obser vations

on

of

mammalian

with

the

cholinesterase

Feldon

SE.

e

“en

plaque”

Burde

Jr,

RM,

extrafusal

technique.

Rev

ed.

Adler’s

Physiolog y

of

the

Eye,

9th

muscles.

ed.

St

In:

Hart

Louis:

Biol.

Pediatr

WM

Demer

tus

Mosby ;

JL,

RA,

muscle

Miller

JM,

Poukens

muscle

V .

pulleys.

J

Surgical

Pediatr

implications

Ophthalmol

of

the

rec-

Demer

pulley

mol

29.

human

30.

rectus

Invest

Clark

RA,

lar

32.

33.

as

a

and

function

JM,

etal.

monkeys

by

of

stability

gaze.

of

Invest

JL.

Inner vation

and

humans.

of

Exp

the

Kramer

inections

Sci.

of

Vis

36.

Res.

Miller

Y ,

on

in

location

secondar y

surger y

Y ,

gaze

of

posi-

rectus

resonance

50.

extraocular

imaging.

Am

and

tissue.

In:

Teratolog y.

Jakobiec

FA,

Philadelphia:

ed.

J,

the

38.

Eye

C lark

ume

Harper

&

R.

and

RA,

53.

A,

etal.

Lateral

canthal

anatomy :

a

54.

T,

etal.

a

Medial

review.

canthal

Ann

support

Plast

55.

Surg.

RA,

gaze

of

A,

the

JL,

etal.

High-resolution

normal

extraocular

magnetic

ric

the

anatomy

of

normal

musculature.

Eye.

muscle

Orbit.

7th

JL.

o c u lar

paths

by

muscles.

ed.

AL.

human

Eects

magnetic

rectus

muscles.

studies

P ,

of

globe

J

C ho

HK,

In:

in

of

transposition

resonance

Eugene

Wol ’s

Saunders;

ext rao c u lar

Invest

t rao c u lar

imaging.

Anatomy

Functional

Neurophysiol.

the

S.

1976:248–274.

mus cle

O phthalmol

ocular

and

morphometr y

N,

Vi s

60.

vol-

Leigh

Von

of

TA,

via

of

anterior

children

A,

etal.

and

extraocular

segment

optical

comparison

Anterior

horizontal

with

the

and

insertion

segment

vertical

to

optical

extraocular

limbus

distance.

J

2016;53:141–145.

Ali

MH.

aspect

macular

A

of

restudy

the

buckling.

of

globe:

Retina

the

an

surgi-

essential

(Philadelphia,

Pa).

rectus

Tenon’s

SY .

Is

t he

contraction

histologic,

muscles

capsule.

RJ,

K-J,

Lee

origin

S-H,

with

in

Academic

the

oblique

etal.

extraocular

Location

reference

oculofacial

e

of

Klin

and

ins er t iona l

S ci.

61.

demonstrates

during

muscles.

to

of

the

surger y.

the

inferior

lacrimal

Brit

J

caruncle

Ophthalmol.

SJ.

their

Monatsbl

symmet r ica l.

Bron

Z ee

L,

of

62.

vertical

morphomet-

relation

DS.

e

Davis;

GK,

Dawson

H,

ed.

e

Eye.

Cycloduction

of

the

eyes

with

head

tilt.

movements.

Arch

Ophthalmol.

1936;

Neurolog y

1983:145,

Maumenee

Tripathi

ed.

P .

AE.

Ophthalmolog y.

RC,

Eye

Movements.

Atlas

of

Strabismus.

2nd

ed.

3rd

ed.

Oxford,

England:

1994:428.

Tripathi

London:

e

of

170.

1973:112.

Clinical

8th

Boeder

BJ.

Chapman

cooperation

of

Wol ’s

&

Hall;

Anatomy

of

the

Eye

and

1997.

extraocular

muscles.

Am

J

Ophthal-

1969;51:469.

Brown

HW .

ed.

Congenital

Strabismus

Coussens

T,

Ellis

structural

Ophthalmic

FJ.

syndrome.

Suh

SY ,

and

superior

Le

muscle

anomalies.

Symposium.

A,

the

Demer

oblique

EM,

anatomy

Sherrington

J

RS.

Sci.

of

St

Louis:

In:

Allen

Mosby ;

J

the

etiolog y

of

congenital

2015;26(5):357–361.

oblique

extraocular

in

Brown

muscles

syndrome.

2015;56:6114–6120.

WW ,

Ellis

FD,

etal.

e

Ophthalmology.

note

on

two

trochlea.

A

study

1982;89:124.

movements

of

the

1984;17:27.

fundamental

Am

the

contractility

Experimental

Gruber

following

Size

on

Ophthalmol.

physiolog y.

(Lond).

e

OM,

JL.

muscle

Vis

and

muscles.

Hakim

Opin

Merriam

CS.

Physiol

Jampel

Consideration

Curr

Ophthalmol

Helveston

ment

63.

to

Augenheilkd.

re c tus

O phthal

Fernández-Vigo

optical

In:

1971;85:570.

monocular

Mosby ;

JJ.

AJ,

Dutton

thal

64.

ex-

Res.

JI,

coherence

JJ.

Plast

Khong

principle

Ophthalmol.

of

the

action

of

the

oblique

1970;69:623.

El-Hag

Y ,

Maher

disinsertion

of

extraocular

JJ,

Anatomic

Reconstr

McNab

disease:

65.

da

Silva

H.

Persistence

muscle.

J

of

eye

move-

AAPOS.

Ventura-

tion

tomography

2836.

in

Ebeling

and

in

thyroid

eye

disease.

Oph-

2018;34:S7–S12.

update

PR,

on

etal.

Pathogenesis

molecular

of

thyroid

mechanisms.

Brit

J

2016;100:142–150.

Costa

of

considerations

Surg.

AA,

review

Ophthalmol.

vation

domain

Eyes.

1962.

2008;12:62–65.

and

anatomy

the

Press;

Herman

Noorden

Kanski

eye

bino c u larly

Spectral

of

1944;32:204.

Movements

M,

A.

Louis:

eyes.

(abstract).

mus cles

etal.

Shin

M.

Duane

of

2016;115:370–378.

Anatomic,

De-Pablo-Gómez-de-Liaño

Abreu

the

Comparison

Ophthalmol.

Invest

of

2010;43:179–184.

42.

AAPOS.

2019;39:1037–1042.

Sharma

of

Strabism.

exact

muscle

Linwong

ocular

compartmental

Gajisin

Shin

WE.

Y ork:

Brown

59.

Philadelphia:

C hanges

duc t ion.

JL.

muscle

1992;200(5):515

41.

J

1950:250.

58.

Rosenbaum

Extraocular

changes.

eye

healthy

posterior

signicance

Alpern

ED,

1993;100(4):475.

Demer

DeGottrau

its

mol.

56.

D emer

extraocular

40.

for

HJ,

Orbit.

57.

rectus

dur ing

Clark

the

Shin

St

2016;57:1106–1111.

39.

of

Philadelphia:

2012;31:279–285.

retinaculum:

Daxer

Demer

on

51.

J

Ocu-

1989;29(2):223.

War wick

F ,

Measurement

distance

Ophthalmol.

El-Mamoun

Ophthalmol.

Arch

52.

Nakano

medial

Ophthalmolog y.

37.

muscles.

8:531.

human

magnetic

Ichinose

Functional

JM,

Krewson

New

2000;41:3787.

aging

by

Ophthalmol.

imaging

JM.

48.

Ophthal-

1997;11:793.

Miller

of

Butter worth-Heinemann;

Takahashi

resonance

35.

etal.

measurement

Arch

and

extraocular

Invest

ree-dimensional

connective

Embryolog y,

Takahashi

Clin

Eect

Orbital

H,

A,

Intl

Erenler

with

İ,

insertion

tomography

ALH,

Oph-

2002;134:872.

Kang

Ettl

MS,

anatomy

oblique

2015;74:508–514.

34.

Yilmaz

Ophthalmol

rectus

49.

JL.

path

Vis

demonstrated

L.

structures:

in

Demer

pulleys

1982:835.

H,

JM,

Demer

Anatomy,

Kang

rectus

2016;100:179–183.

Miller

muscle

Row ;

review.

V ,

Ophthalmol

paths

Koornneef

paths

Location

1997;38(9):1774.

Ophthalmol.

31.

JL.

1997;38:227.

Miller

tions.

muscle

Demer

Muscle

Sci.

Sci.

RA,

JM,

Poukens

smooth

Vis

Clark

Vis

JL,

46.

Strabismus.

47.

Miller

pulleys.

thalmol

28.

extraocular

191

Muscles

2011;31:1405–1411.

extraocular

Clark

of

tomography

topography

1996;33(4):208.

27.

Siam

cal

1992:101.

26.

Pihlblad

A,

muscle

adult.

muscles

Can

45.

extraocular

insertion

İnal

coherence

1962;21:241.

25.

OB,

healthy

1968;18:403.

A.

muscle

Ocak

horizontal

coherence

Nakamura

extraocular

24.

the

Extraocular

2016;20:201–205.

2018;59:539–548.

23.

assess

11

RM,

primate

horizontal

Kung

J,

Poukens

extraocular

recti.

Invest

V ,

muscles:

etal.

Intramuscular

unique

Ophthalmol

Vis

inner-

compartmentaliza-

Sci.

2011;52:2830–

CHAPTER

192

66.

Clark

RA,

Demer

contraction

Sci.

67.

68.

Extraocular

Dierential

ocular

lateral

Muscles

rectus

counter-rolling.

compartmental

Invest

Ophthalmol

70.

Vis

RS.

mental

study

Doxanas

Hayreh

mol.

e

MT,

&

SS.

in

action

the

of

Anderson

e

RL.

superior

Arch

oblique

muscle.

Ophthalmol.

Clinical

Orbital

An

experi-

arter y :

71.

1966;75:535.

Anatomy:

e

role

of

extraocular

strabismus.

Middle

muscle

East

pulleys

African

J

in

incomitant

Ophthalmol.

Branches.

Brit

J

Ophthal-

JH,

etiologies

Pineles

of

SL,

Demer

strabismus.

J

JL.

Recent

Neuro

advances

Ophthalmol.

clarif ying

2015;35:

185–193.

72.

III.

Peragallo

the

Baltimore:

1984:116.

ophthalmic

1962;46:212.

RA.

2015;22:279–285.

the

monkey.

Wilkins;

Clark

non-paralytic

2012;53:2887–2896.

Jampel

Williams

69.

JL.

during

11

McKelvie

ageing

in

Zealand

J

P ,

Friling

R,

extraocular

Davey

K,

muscles:

Ophthalmol.

a

etal.

Changes

post-mortem

1999;27:420.

as

the

study.

result

Aust

of

New

12

Orbital

Circulation

carotid

to

the

arter y,

head

which

and

neck

divides

is

into

supplied

two

by

the

vessels:

common

the

abducens

internal

internal

carotid and the external carotid. e internal carotid arter y sup-

maxillar y

plies

the

eye

the

and

the

structures

related

supercial

portion

of

the

within

the

structures.

areas

of

e

the

circulation

anterior

external

head

to

cranium,

and

ocular

carotid

neck

and

including

arter y

the

supplies

provides

a

ner ve

small

arter y

adnexa.

is

internal

carotid

lateral

sinus.

to

the

roughout

surrounded

superior

to

the

lateral

trochlear,

internal

its

border

of

ophthalmic,

carotid

pathway—up

arter y

the

the

and

within

neck,

into

cer vical

to

the

by

a

plexus

ganglion.

cavernous

arter y

sinus

branches

of

e

sympathetic

optic

and

from

chiasm

internal

the

ner ves

lies

carotid

internal

from

superior

arter y.

carotid

the

and

e

arter y

just

ARTERY as

e

lie

adherent

oculomotor,

Supply

the skull, and through the cavernous sinus—the internal carotid

ophthalmic

CAROTID

closely

e

ner ves

cavernous

medial

INTERNAL

is

carotid.

Blood

arter y

runs

upward

through

the

neck

it

emerges

from

and

clinoid

process

petrous

branch

from

of

the

the

cavernous

sphenoid

sinus

bone.

It

medial

is

to

usually

the

the

anterior

rst

major

1

enters

the

portion

men.

skull

of

the

Within

separates

the

through

the

temporal

the

bone

anterior

arter y

carotid

just

portion

from

the

canal

located

anterior

of

the

cochlea

to

the

canal,

and

in

the

the

jugular

only

e

internal

carotid

arter y

leaves

the

CLINICAL

bone

trigeminal

canal

and

Severe

gan-

enters

the

cavernous

sinus,

where

it

runs

carotid

arter y.

COMMENT: Ocular

atherosclerosis

the

blood

involving

supply

to

the

Ischemic

the

eye

internal

and

orbit

Syndrome

carotid

(Fig.

artery

12.1).

It

can

can

signicantly

result

in

pain

imme-

and

diately

internal

fora-

thin

reduce

glion.

the

for ward

vision

loss.

The

mortality

rate

is

high

because

of

the

risk

of

cardiovascular

along disease. Carotid duplex ultrasonography or a head computed tomography angi-

the

medial

the

roof

wall

beside

the

sphenoid

bone.

It

then

exits

through ography

of

the

cavernous

sinus.

Within

the

cavernous

sinus,

can

help

make

the

diagnosis.

the

A

B

Fig.

12.1

showing

internal

(white

Ocular

ischemic

insufcient

carotid

arrows).

responding

blood

arter y

B,

syndrome.

supply

lumen

Fundus

uorescein

(red

photo

A,

through

arrows)

showing

angiography

is

Coronal T1

the

left

compared

optic

seen

in

disc

Fig.

magnetic

internal

with

resonance

carotid

that

edema

of

arter y.

the

because

right

of

imaging

Note

the

internal

ocular

with

size

contrast

of

the

carotid

left

arter y

ischemia. The

cor -

12.10.

193

CHAPTER

194

Ophthalmic

e

of

the

Orbital

Blood

Supply

Artery

ophthalmic

sheath

12

medial

ar ter y

optic

enters

ner ve

and

the

passes

orbit

within

through

the

the

dural

optic

canal,

orbital

margin,

supratrochlear

orbital

arteries

and

are

it

divides

dorsonasal

located

in

into

its

terminal

arteries.

the

In

branches,

general,

adipose

the

the

intra-

compartments

and

2–4

below

and

lateral

to

the

ner ve

(Fig.

12.2).

A

network

of

perforate

5

sympathetic

the

ner ves

ophthalmic

runs

inferolateral

then

crosses

the

surrounds

arter y

to

either

nasociliar y

the

emerges

the

optic

above

ner ve,

or

the

vessel.

from

ner ve

below

the

for

the

ophthalmic

a

the

connective

tissue

septa

as

they

pass

between

sec-

7

Once

in

the

meningeal

short

ner ve.

orbit,

tions.

sheath,

globe

distance,

Together

ar ter y

r uns

and

with

toward

the

e

and

ophthalmic

adnexa

external

carotid

roughout

the

but

ophthalmic

its

is

arter y

is

the

main

supplemented

by

blood

a

supply

to

the

few

branches

from

many

branches

from

arter y.

rather

arter y

tortuous

emerge:

(1)

course,

central

retinal

arter y,

(2)

lac-

6

the

medial

between

ing

o

wall

the

of

the

medial

branches

to

orbit.

rectus

various

and

e

arter y

superior

areas.

Just

oblique

posterior

Dorsonasal

Medial

continues

for ward

muscles,

to

the

giv-

superior

rimal

arter y,

times

three),

arter y,

(6)

(3)

(4)

posterior

ethmoid

muscular

ciliar y

arteries

arteries

arteries

(usually

(usually

(usually

two),

two),

(7)

(5)

two,

supraorbital

medial

palpebral

artery

palpebral

artery

Lateral

palpebral

Trochlea

artery

Superior

oblique

muscle

Lacrimal

gland

Supratrochlear

artery Long

posterior

ciliary

artery

Supraorbital

artery

Short

posterior

Anterior

ciliary ethmoid

arteries

artery

Zygomaticotemporal

artery

Ethmoid

sinus

Zygomaticofacial

artery Long

posterior Central

ciliary

Recurrent

meningeal

artery

artery

Lacrimal

Medial

artery

artery

Posterior

ethmoid

retinal

artery

posterior

Lateral ciliary

posterior

ciliary

artery

Medial

rectus Lateral

rectus

muscle

muscle

Ophthalmic

Optic

Internal

artery

nerve

carotid

artery

Fig.

12.2

Orbit

viewed

from

above

illustrating

branches

of

the

ophthalmic

artery.

artery

some-

CHAPTER

superiorly TABLE

12.1

Order

of

Origin

of

Branches

of

and

Ophthalmic

branches,

BRANCHES

OPHTHALMIC

of

Crosses

the

Above

the

retinal

in

Optic

Crosses

Nerve

Optic

Central

retinal

and

Below

Lateral

medial

Lateral

posterior

Lacrimal

Muscular

into

nasal

and

dichotomously

ber

layer.

e

retinal

blood

vessels

are

8.

COMMENT: Retinal

of

the

central

retinal

Venous

artery

Occlusion

and

vein

are

joined

in

a

common

ciliary

Central

ciliary

retinal

tissue

the

sheath

artery

hypertension,

rst,

4

divide

branch

at

the

point

where

the

vessels

cross

each

other.

In

ciliary

posterior

3

ner ve

Chapter

branches

general,

2

to

the

connective posterior

branches

continue

Nerve

The 1

then

ARTERY:

CLINICAL Origin

ese

195

Supply

WHEN

discussed

Order

inferiorly.

Blood

Artery

within OF

Orbital

the

temporal

SEQUENCE

12

Medial

muscular

Medial

posterior

a

the

deection

crosses

over

stiffened

of

the

the

artery

wall

of

vein

may

the

and,

in

disease

compress

vein

is

seen,

the

processes,

vein

which

at

with

the

time

such

as

crossing.

At

may

progress

to a venous occlusion (Fig. 12.4). Restriction of ow in the vein results in retinal

to

superior

rectus

and

ciliary edema

and

hemorrhage

in

the

area

surrounding

the

occlusion.

levator

5

Lacrimal

Posterior ethmoid and supraorbital,

jointly or separately

Lacrimal

6

Medial

posterior

Muscular

ciliary

to

superior

One

and

Artery

rectus

of

the

largest

ophthalmic

7

Medial

Posterior

muscular

branches,

the

lacrimal

ar ter y,

leaves

the

levator

ethmoid

supraorbital,

and

jointly

R arely,

it

arter y

just

branches

or

aer

before

it

enters

the

the

orbit

ophthalmic

(see

Fig.

ar ter y

12.2).

enters

the

10

optic

canal.

e

lacrimal

arter y

and

the

lacrimal

ner ve

r un

separately

for ward

8

Muscular

and

to

superior

medial

Muscular

oblique

rectus,

jointly

oblique

or

jointly

separately

to

superior

and

or

Within

medial

rectus,

the

along

the

lateral

the

orbit

rectus

upper

the

border

lacrimal

of

the

arter y

lateral

may

rectus

supply

muscle.

branches

to

muscle.

separately

A recurrent meningeal artery (see Fig. 12.2) might branch from

9

To

10

areolar

Anterior

Anterior

tissue

To

ethmoid

ethmoid

areolar

the lacrimal artery and course back, leaving the orbit through the

lateral

tissue

aspect

of

the

superior

orbital

ssure

and

then

forming

an

anastomosis with the middle meningeal artery, a branch from the 11

Medial

palpebral

or

Medial

inferior

palpebral

or

inferior 1

external medial

medial

palpebral

carotid

artery

circulation.

Other

branches,

the

zygo-

palpebral

maticotemporal arter y and the zygomaticofacial arter y, exit the 12

Superior

Terminal

Dorsonasal

medial

Superior

palpebral

medial

palpebral

orbit

and

through

foramina

of

the

same

name

within

the

zygomatic

Dorsonasal and supratrochlear

supratrochlear

bone

(see

Fig.

12.2).

ese

vessels

anastomose

with

branches

8

Modied

from

Ophthalmol.

Hayreh

SS.

The

ophthalmic

artery.

III.

Branches.

Br

from

J

1962;46:212.

e

mal

the

arteries

(9)

(superior

dorsonasal

Marked

branches

and

of

inferior),

(8)

supratrochlear

arter y,

and

arter y.

variability

the

evident

ophthalmic

in

the

artery,

order

and

the

of

the

origin

sequence

of

the

appears

to

T able

and

e

12.1.

their

most

common

Many

patterns

anatomic

courses.

ose

of

variations

most

oen

distribution

can

occur

reported

are

are

in

shown

the

gland.

carotid

arter y

Terminal

orbital

septum,

in

the

temporal

continues

branches

and

enter

fossa

for ward

pass

the

and

to

through

lateral

side

on

the

supply

the

of

face.

the

gland,

the

lacri-

pierce

upper

and

lower eyelids to form the lateral palpebral arteries. ese anas-

form

nal

with

vessel

branches

form

a

branches

arches

from

capillar y

from

called

the

the

the

medial

palpebral

palpebral

lacrimal

arter y

arcades.

enter

the

arteries

Other

and

termi-

conjunctiva

and

network.

in

branches

included

external

lacrimal

tomose

is

correlate with whether the artery crosses above or below the optic

nerve.

the

here.

Posterior

e

Ciliary

posterior

Arteries

ciliary

arteries

are

branches

of

the

ophthalmic

11

artery,

Central

Retinal

Artery

and

much

commonly,

there

variation

are

two

can

to

occur

three

in

their

posterior

distribution.

ciliary

Most

arteries

which

12

One

of

retinal

the

rst

arter y,

branches

is

among

of

the

the

ophthalmic

smallest

arter y,

branches.

e

the

central

central

reti-

each

divide

Before

into

reaching

short

the

and

globe,

long

the

posterior

posterior

ciliary

ciliary

13

branches.

arteries

give

o

14

nal

arter y

ner ve

leaves

(see

before

Fig.

entering

the

ophthalmic

12.2).

the

e

arter y

arter y

meningeal

runs

sheath

as

it

lies

for ward

of

the

below

a

the

short

ner ve

optic

distance

about

10

to

branches

terior

10

to

nerve

the

(Fig.

central

retinal

arter y

provides

branches

to

the

ner ve

and

pia

supply

ciliary

20

12 mm behind the globe (Fig. 12.3). While within the optic ner ve,

to

arteries

branches.

and

form

12.5).

the

arise

ey

the

Other

retrobulbar

as

enter

arterial

branches

1,

the

2,

optic

or

network

from

3

sclera

the

nerve.

e

branches

in

a

within

short

ring

the

that

short

pos-

then

form

around

the

choroidal

posterior

optic

stroma

ciliary

arter-

8

mater.

the

Oen,

central

these

retinal

sympathetic

branches

arter y

ner ve

runs

plexus

are

called

for ward

(the

ner ve

collateral

within

of

the

branches.

optic

Tiedemann)

As

ner ve,

a

surrounds

ies

supply

circle

optic

of

the

peripapillary

Zinn

nerve

at

choroid

(Zinn-Haller)

the

level

of

the

(see

and

Fig.

choroid.

anastomose

12.3),

e

which

most

to

form

the

encircles

the

supercial

nerve

9

the

arter y.

cribrosa

e

and

central

enters

the

retinal

optic

arter y

disc

passes

just

nasal

through

to

center,

the

lamina

branching

bers

that

capillaries

occupy

from

the

the

surface

central

of

retinal

the

optic

artery,

disc

with

no

are

supplied

direct

by

choroidal

196

CHAPTER

12

Orbital

Blood

Supply

Circle

of

Zinn

(Haller)

Retina

Choroid

Lamina

cribrosa

Sclera

Short

Short

posterior

posterior ciliary

ciliary

artery

artery

Collateral

branches

Central

retinal

Ophthalmic

artery

artery

Dura

mater

Arachnoid

mater

Subarachnoid

Pia

Fig.

12.3

Longitudinal

A

section

of

the

optic

space

mater

nerve.

B

Fig.

ing

12.4

Retinal

alterations

arter y

vein

(arrow).

becomes

individual

in

B,

changes

the

wall

Fundus

branch

a

retinal

photo

sufciently

venous

associated

of

of

a

left

compressed,

or

involve

with

vein

the

hypertension.

because

eye

of

following

blood

backs

central

up

retinal

A,

Fundus

compression

a

central

into

vein

the

as

photo

as

retinal

it

vein

retina. This

seen

is

here.

of

a

right

crossed

occlusion.

may

be

eye

by

If

show-

a

retinal

a

retinal

localized

to

an

CHAPTER

12

Orbital

Blood

197

Supply

D

J

e k l o

n f

g

e

n

D C

h

A m b

i

b C

f

e

D

C

J

D

Fig.

12.5

Except

ply

of

the

enters

optic

pass

those

as

of

Zinn

by

in

are

sclera

oriented

the

into

and

the

off

and

the

as

to

the

body,

as

the

about

vortex

system

Philadelphia:

the

circle

well

of

the

sclera

anterior

(l),

eye

system,

of

branches

as

part

straight

veins.

of

as

and

(m).

but

(e)

those

the

an

joining

the

the

(D)

iris

pars

optic

the

Alvarado

the

iris

JA,

(C).

as

circle

far

the

and

of

ciliar y

Weddell

and

JE.

to

sends

Zinn

(h)

circle

disc. Vortex

system

sclera

with

muscle

and

the

medial

and

an-

with

major

arteries. The

near

the

They

for ward

ciliar y

vortex

anterior

which

ner ve

plicat a

(k)

one

near

from

joining

ner ve

on

eye

serrat a,

retina

(g). The

ciliar y

the

continuous

through

the

sup-

retina

pass

Before

vortices

the

is

arter y.

blood

arteries:

of

ora

optic

ampulla

of

from

cross

MJ,

in

the

parts

return

veins

to

forming

posterior

back

posterior

supply

after

Hogan

1971 .)

into

the

nourish

arteries

lies

entire

ciliar y

capillaries

body.

pass

(f)

short

at

nourishes

of

ciliar y

for ward

Venous

some

around

ciliar y

iris

(b)

ophthalmic

the

meridian

capillaries

which

the

posterior

branches

that

from

almost

horizont al

system

the

blood

long

choroid

from

(j)

retina,

These

the

whereas

(From

Saunders;

the

Anterior

enter

branches

posterior

join

fairly

12

to

derived

t wo

ve

enter

arteries.

major

well

to

shown). This

sclera

furnishes

that

are

8

The

ciliar y

(i),

circularly

into

episcleral

Eye.

give

are

along

three

is

inner

choriocapillaris,

not

ciliar y

the

There

arteries

posterior

pierce

through

branches

posterior

the

off

eye

the

choriocapillaris.

ciliar y

posterior

then

arteries

eye

oriented

Human

form

the

temporally

give

anterior

(choriocapillaris

branches

the

from

arteries

the

of

supplies

vessels.

enters

choriocapillaris.

pial

Venous

enter

the

these

one

supply

which

uveal

posterior

long

posteriorly

lies

ridionally

mainly

from

muscles,

iris,

exit

sclera.

to

equator

anterior

t wo

Blood

arter y,

the

and

form

Short

rapidly

the

from

These

to

vessels.

retinal

nasally

back

derived

formed

sides

(A).

rather

the

veins

to

uvea

for ward.

branches

of

comes

rectus

circle

is

eye

ner ve

teriorly

join

central

directly

divide

blood

the

the

equator

the

Uveal

for

internal

are

and

me-

lateral

body

(n)

limbus

Histology

is

(o)

of

CHAPTER

198

12

Orbital

peripapillary

network,

Blood

Supply

15–17

supply.

e

formed

by

branches

from

the short posterior ciliary arteries and from the circle of Zinn, sup-

16–19

plies

the

laminar

remaining

region

is

prelaminar

supplied

by

region

the

of

short

the

optic

nerve.

posterior

ciliary

e

arteries

16–20

either

directly

or

as

branches

from

the

circle

of

Zinn.

Retinal

16

vessels do not anastomose with the peripapillary choriocapillaris.

CLINICAL

Anterior

COMMENT: Anterior

ischemic

optic

neuropathy

Ischemic

results

from

Optic

Neuropathy

nonperfusion

or

hypoperfusion

16

of the ciliary blood supply to the optic nerve head (Fig. 12.6).

Although there is

much variation, a watershed zone, the border between vascular territories, may

be

present

between

areas

supplied

by

branches

of

the

posterior

ciliary

arter-

13

ies.

will

If there is decreased perfusion, the end arteries in these watershed zones

be

most

affected.

This

may

be

the

anatomic

basis

for

the

altitudinal

visual

Fig. 12.7

Fundus

photo

of

the

right

eye. A

cilioretinal

arter y

can

eld loss that characterizes nonarteritic anterior ischemic optic neuropathy. The

be

seen

looping

up

into

retina

at

the

temporal

edge

of

the

optic

inferior eld is more often affected, but there is no adequate explanation for the

disc. The

21

preferential

involvement

of

the

superior

part

of

the

ring

of

is

CLINICAL

COMMENT: Cilioretinal

central

retinal

vein

is

exiting

and

the

central

retinal

arter y

vessels.

entering

the

globe

nasal

to

the

center

of

the

optic

disc.

Artery 24

(Fig. A

cilioretinal

artery

may

arise

either

from

the

vessels

entering

the

choroid

12.8).

superiorly from

the

the

circle

ciliary

of

Zinn.

circulation

Thus

and

this

not

vessel,

from

the

located

retinal

within

supply.

the

retina,

Various

arises

studies

the

retina

from

22

area

(Fig.

blood

a

supply

to

temporal

side

of

the

optic

disc

to

supply

the

report

a

macular

vessel,

lar

the

artery

If

the

occlusion

macular

of

area

the

will

central

be

retinal

maintained

artery

in

occurs,

those

the

direct

individuals

with

is

the

arteries.

mm

ing

the

of

major

the

in

circle

the

radial

circle

arteries

branches

lateral

ese

and

long

of

the

one

posterior

medial

posterior

to

ciliar y

ciliary

the

arteries

ring

arteries

of

enter

short

enter

the

the

they

the

ciliary

branches

body

and

anastomose

branch

with

each

of

the

ciliary

iris (Fig.

stroma

12.9).

near

the

is

iris

circu-

root

of

vessels

the

iris,

found

in

branches

the

iris.

from

the

Before

and

long

form-

vessels

nasal

and

3

mm

temporal

to

the

optic

nerve

between

the

sclera

and

the

choroid

to

the

supply

form

from

the

a

the

ciliary

network

short

that

posterior

body

and

the

posterior

anastomoses

ciliary

anterior

with

arteries

the

choroid,

choroidal

(see Fig.

12.5).

ciliary

sclera

sheath

anterior

COMMENT: Fluorescein

Angiography

and Sodium

run

arterial

located

CLINICAL

2.5

enter

ese

artery.

long

one

major

is

source

where

Two

arteries

other and with the anterior ciliary arteries to form a circular blood

ciliary

sclera:

the

inferiorly.

23

12.7).

cilioretinal

the

and

from

cilioretinal artery occurring in 15% to 50% of the population and usually enter-

ing

Here,

or

uorescein

dye

can

be

injected

into

the

systemic

circulation

to

examine

globe the

choroidal

and

retinal

circulation

(Fig.

12.10).

Light

is

passed

through

a

blue

lter which excites the uorescein molecules, and high contrast black and white

photos

the

are

taken

choroidal

ternal

carotid

ciliary

of

and

the

artery,

arteries,

fundus

retinal

passes

which

ll

to

document

vasculature.

into

the

before

the

The

the

dye

movement

enters

ophthalmic

central

the

artery,

retinal

of

the

skull

and

artery.

blood

through

through

enters

Within

the

10

the

in-

posterior

seconds

of

injection, the choroidal ush can be seen. The dye can leak out of the fenestrated

choriocapillaris

easily

but

should

not

seep

into

the

retina

because

of

the

blood-

retinal barrier of zonula occludens in the retinal pigment epithelium (RPE). Ten to

12

in

to

seconds

the

next

exit

the

the

retina

after

injection,

second.

ocular

before

As

the

arise

posterior

sinus.

upper

It

1

Defects

retinal

to

in

arterioles

2

seconds

the

vessels

capillary

ophthalmic

to

retinal

RPE

ll.

leakage,

ll,

can

be

the

veins

be

Abnormal

will

and

the

capillaries

ll,

seen

retinal

if

and

the

the

dye

are

dye

lled

starts

leaks

vasculature,

into

such

as

evident.

Arteries

branches

canal

or

the

another

tissue.

the

neovascularization

Ethmoid

After

ethmoid

supply

also

part

enter

the

courses

the

arter y

the

sends

of

artery

and

passes

posterior

branches

nasal

near

ethmoid

through

ethmoid

into

mucosa.

the

e

the

bone

the

sinus

nasal

medial

(see

Fig.

wall,

12.2).

posterior

and

cavity

anterior

the

to

two

e

ethmoid

sphenoid

supply

ethmoid

the

arter y

generally is larger and passes through the anterior ethmoid canal.

It supplies the anterior and middle ethmoid sinuses, the sphenoid Fig.

12.6

arteritic

Fundus

anterior

photo

of

ischemic

the

left

optic

eye

of

a

patient

neuropathy.

with

non-

sinus,

the

frontal

sinus,

the

nasal

cavity,

and

the

skin

of

the

nose.

CHAPTER

Major

circle

of

the

12

Orbital

Blood

199

Supply

iris

Anterior

Long

ciliary

artery

posterior

ciliary

artery

Muscular

to

lateral

artery

rectus

muscle

Muscular Choroidal

vein

blood

vessels

Retinal

blood

vessels

Vortex

Long

posterior

Short

Fig.

12.8

ciliar y

Central

retinal

artery

Central

retinal

vein

Horizontal

arteries

suprachoroidal

drawn

with

Appleton

Supraorbital

supraorbital

as

lies

orbital

medial

artery

extraocular

orbital

to

permission

&

Lange;

of

the

choroidal

the

from

eye

showing

vessels.

anterior

Vaughan

globe

D,

The

to

to

the

runs

the

long

arises

optic

upward

turns

between

the

to

a

ciliary

anastomose

Asbur y T .

General

artery

ciliary

arteries

circulation.

ciliar y

with

the

arter y

The

anterior

Ophthalmology.

short

passes

ciliar y

East

posterior

through

arter y.

Nor walk,

the

(Re-

Conn:

1980.)

from

nerve

posterior

posterior

the

artery

muscles,

nerve

space

the

Artery

e

it

supply

section

ciliary

vein

the

(see

Fig.

position

anteriorly,

periorbita

and

of

ophthalmic

12.2).

above

runs

the

e

the

with

orbital

artery

supra-

superior

the

supra-

roof

and

or

levator

muscle.

foramen,

oen

skin

and

the

T erminal

the

anterior

muscles

branches

opposite

It

side,

temporal

passes

dividing

of

the

the

artery

two

forehead

anastomose

with

through

into

with

the

and

the

scalp

the

to

artery,

external

notch

supply

(see

supraorbital

supratrochlear

from

supraorbital

branches

Fig.

artery

and

carotid.

the

12.11).

from

with

the

While

the

CHAPTER

200

12

Orbital

Blood

Supply

Conjunctival

capillary

loops

Cornea

Conjunctival

Episcleral Canal

of

plexus

plexus

Schlemm

Anterior

ciliary

artery

Iris

Anterior

ciliary

vein

Long Ciliary

body posterior

ciliary

artery

Major

of

Fig.

12.9

ciliary

ply

artery. The

and

the

Section

sends

long

through

anterior

branches

posterior

the

ciliar y

into

ciliar y

ciliary

the

arter y

body

arter y

ciliar y

to

has

the

iris

and

limbal

entered

body,

form

circle

the

the

episclera,

major

area

and

circle

showing

globe

of

from

the

branches

the

anterior

muscle

blood

sup-

It

anastomoses

with

conjunctiva.

the

of

rectus

also

iris.

supraorbital artery is in the orbit, it sends branches to the superior

CLINICAL

COMMENT: Red

Eye

rectus, superior oblique, and levator muscles and to the periorbita. Inammation generates an increase of the blood ow to the affected area, causing

hyperemia.

Muscular

In

cases

of

a

“red

eye,”

an

understanding

of

the

organization

of

the

Arteries blood supply in the limbal area can help in differentiating a less serious presenta-

Much

variation

occurs

in

the

vessels

supplying

the

extraocular tion,

muscles,

and

any

combination

of

the

vessels

named

here

such

as

conjunctivitis,

from

a

more

serious

situation,

such

as

uveitis.

In

con-

might junctivitis and mild corneal involvement, the supercial blood vessels are injected

be

present.

come

and

In

from

the

one

the

medial

common

presentation,

ophthalmic

branches.

arter y

as

the

two

muscular

branches,

e lateral branch supplies

arteries

the

the

branch

supplies

the

and

inferior

oblique

muscles.

medial

rectus,

inferior

conjunctiva

a

bright-red

color

that

often

increases

toward

the

fornix.

lateral

vasoconstrictor.

8–10

medial

the

The vessels move with conjunctival movement and can be blanched with a topical

rectus, superior rectus, superior oblique, and levator muscles.

e

giving

lateral

rectus,

giving

the

In

uveitis,

circumlimbal

the

area

a

deeper

scleral

purplish

or

and

episcleral

rose-pink

color.

vessels

These

are

injected

vessels

do

not

move with the conjunctiva and are not blanched with a topical vasoconstrictor.

8–10

the

muscles

supplies

bital

may

the

arter y

come

lateral

from

and

supplies

the

Additional

other

superior

superior

sources.

rectus

branches

e

muscles.

rectus,

supplying

lacrimal

e

superior

arter y

supraor-

oblique,

and

Medial

Palpebral

Two medial palpebral arteries (the inferior and superior medial

levator muscles. e infraorbital arter y supplies the inferior rec-

palpebral

arteries)

tus

arter y

from

and

inferior

oblique

muscles

(Table

12.2).

Arteries

or

branch

the

either

dorsonasal

directly

arter y

from

near

the

the

ophthalmic

trochlea

of

the

superior oblique muscle. e medial palpebral arteries pierce the

Anterior

Ciliary

Arteries

orbital

septum

on

either

side

of

the

medial

canthal

tendon

and

25

e

the

cle

anterior

rectus

ciliar y

muscles.

insertions,

run

arteries

ese

branch

arteries

for ward

from

exit

along

the

the

the

vessels

muscles

tendons

a

supplying

near

the

short

mus-

distance,

enter

the

superior

branches

run

orbicularis

and

through

muscle

inferior

the

and

eyelids

eyelid

the

tarsal

and

(see

form

plate.

Fig.

12.11).

arches

ey

ese

between

anastomose

the

with

then loop inward to pierce the sclera just outer to the limbus (see

branches from the lacrimal arter y and form the vessels known as

Fig.

12.5).

point

at

sclera,

tiva

a

which

the

junctiva,

(see

accumulation

the

arter y

anterior

forming

Fig.

network

ar y

An

of

arteries

ciliar y

a

12.9).

vessels

then

the

the

arteries

of

vessels

entering

ciliar y

may

sclera.

send

branches

before

enter

pigment

enters

network

Other

of

in

the

the

the

uvea.

and

at

the

the palpebral arcades. Usually, two arcades occur in each lid: the

entering

the

marginal

evident

Before

branches

enter

body

be

into

limbal

the

conjunc-

episclera

e

con-

to

form

anterior

anastomose

cili-

with

of

the

iris

(see

Fig.

12.5).

In

general,

two

anterior

edge

arcade,

and

of

the

the

which

runs

peripheral

tarsal

plate.

near

arcade,

ese

the

marginal

which

provide

runs

the

edge

near

blood

of

the

the

tarsal

peripheral

supply

for

the

eyelid structures. Additional branches from the medial palpebral

arteries

supply

the

structures

in

the

medial

canthus.

the

branches of the long posterior ciliar y arteries, forming the major

circle

plate,

ciliar y

Supratrochlear

One

of

the

Artery

terminal

arteries emanate from each of the rectus muscles, with the excep-

supratrochlear

tion

rior

branches

arter y,

pierces

of

the

the

ophthalmic

orbital

septum

arter y,

at

the

the

supe-

26

of

the

lateral

rectus,

which

provides

only

one

such

arter y.

medial

corner

of

the

orbit

(see

Fig.

12.11).

It

passes

with

CHAPTER

12

Orbital

Blood

201

Supply

Peripheral

Marginal

Lateral

palpebral

palpebral

palpebral

arcade

arcade

arteries

Superficial

temporal

artery

Supraorbital

artery

Supratrochlear

artery

Middle

palpebral

arteries

Angular

Dorsal

artery

nasal

artery

Infraorbital

A

artery

Facial

Fig.

12.1 1

Supercial

from:

Lemke

orbit,

and

Levine

runs

Lucarelli

related

MR,

Surger y.

BN,

eds:

2nd

facial

St

the

in

MJ.

the

In:

Ophthalmic

Louis:

nose

1998;

to

artery

ocular

Anatomy

structures.

Smith’ s

ed.

alongside

arteries

of

region.

the

Nesi

Plastic

F A,

and

(Adapted

ocular

adnexa,

Lisman

RD,

Reconstructive

Mosby.)

anastomose

with

the

angular

arter y

1

and

infraorbital

arter y

PHYSIOLOGY

OF

from

the

external

OCULAR

carotid

supply.

CIRCULATION

B e

that Fig.

12.10

phy

in

a

Fundus

photos

68-year-old

stenosis.

Note

the

white

delay

showing

male

in

dye

uorescein

with

internal

passage

into

modulate

cells

that

vascular

line

tone

blood

and

artery

vessels.

A,

strongly

dependent

stances,

such

as

on

ll

t aken

rst

arrow

the

20

seconds

followed

indicates

choroidal

by

a

the

after

central

choroidal

ush

as

injection.

dye

retinal

vessel,

seeps

arter y

and

out

The

the

of

the

choroidal

vessels

branches. The

thick

arrow

thin

endothelin-1,

prevented

from

entering

pigment

epithelium.

The

has

dye

along

the

lled

walls

of

B,

the

the

retina

Photo

retinal

retinal

by

t aken

the

choriocapillaris

30

tight

veins

junction

seconds

capillaries

and

(arrow)

after

can

as

it

substances

Blood

ow

is

largely

of

nitric

oxide,

which

dependent

on

causes

vasodilation

and

28

vasoconstrictor.

vasoactive

e

choroidal

autonomic

blood

inner vation.

ow

e

but

12.2

Extraocular

Muscle

Blood

Supply

retinal

Muscle

Arterial

Supply

be

the

seen

Medial

rectus

Medial

muscular

Lateral

rectus

Lateral

muscular

eye.

Lacrimal

the

supratrochlear

ner ve

upward

to

supply

the

skin

of

the

fore-

Superior

rectus

Lateral

muscular

Lacrimal

head and scalp and the muscles of the forehead. e supratroch-

Supraorbital

lear

arter y

opposite

of

the

forms

anastomoses

supratrochlear

external

carotid

with

arter y,

and

the

the

supraorbital

anterior

arter y,

temporal

the

arter y

Inferior

rectus

e

other

sonasal

terminal

the

branch

(dorsal

orbital

tendon.

It

muscular

Lateral

muscular

Supraorbital

of

nasal

septum

the

ophthalmic

arter y),

below

the

also

arter y,

leaves

trochlea

the

above

the

dor-

orbit

the

Inferior

oblique

sends

vessels

to

supply

the

lacrimal

Medial

by

muscular

Infraorbital

medial Modied

canthal

oblique

Artery

arter y

piercing

Medial

Infraorbital

supply.

Superior

Dorsonasal

is

sub-

injection.

now

exits

a

vasoactive

shows

TABLE is

secrete

caliber.

endothelial-derived

27

Photo

vessels

vessel

angiogra-

carotid

the

endothelial

sac,

then

from

Ophthalmol.

Hayreh

SS.

1962;46:212.

The

ophthalmic

artery.

III.

Branches.

Br

J

CHAPTER

202

sympathetic

12

stimulation

Orbital

causes

Blood

Supply

vasoconstriction,

but

the

eect

and

cur ves

upward

over

the

outside

of

the

jaw

and

across

the

27

of

the

sels

ing

parasympathetic

lack

autonomic

blood

ow

to

stimulation

inner vation

remain

is

and

stable

less

are

despite

clear.

Retinal

autoregulated,

transient

ves-

allow-

increases

in

cheek

the

the

to

the

nose

angle

and

medial

of

sends

canthus

a

the

mouth.

terminal

(Fig.

It

ascends

branch,

12.12).

e

the

along

the

angular

angular

arter y

side

of

arter y,

to

supplies

the

27

systemic

blood

pressure.

Retinal

vessel

walls

have

pacemaker

lacrimal

mechanisms that regulate vessel wall tension, as well as constric-

cheek.

tion and dilation. ey are inuenced by changes in the environ-

to

ment

mose

and

of

the

carbon

surrounding

dioxide,

as

tissue,

well

as

responding

pH

to

changes.

levels

Some

of

oxygen

that

choroidal

Although

extremely

(2000

blood

high

vessels

ow

through

compared

mL/min/100

g

exhibit

with

tissue

vs.

some

the

ow

60

choroidal

through

vessels

retinal

g

Some

anastomose

with

medial

branches

the

Supercial

autoregulation.

mL/min/100

the

with

part

pass

the

of

the

lower

beneath

the

infraorbital

dorsonasal

lid,

and

medial

arter y,

the

skin

canthal

and

some

of

the

tendon

anasto-

arter y.

investigators

29

believe

sac,

is

vessels

tissue),

oxygen

Temporal

Artery

e supercial temporal artery is a terminal branch of the exter-

nal

carotid

temporal

artery

artery

(see

that

Fig.

supply

12.12).

areas

Branches

near

the

of

orbit

the

are

supercial

the

anterior

28

extraction

ow

rate

diusion

dria

in

from

the

provides

through

the

blood

ow

retina

from

choriocapillaris

high

oxygen

Bruch

can

also

act

to

low.

tension

membrane

photoreceptor

is

inner

which

and

the

segment.

stabilize

e

high

choroidal

enhances

RPE

e

to

high

temperature,

oxygen

mitochon-

choroidal

protecting

the

temporal,

zygomatic,

and

transverse

facial

arteries.

e

anterior

temporal artery supplies the skin and muscles of the forehead and

anastomoses

with

the

supraorbital

e zygomatic artery extends

and

above

the

supratrochlear

zygomatic

arch

arteries.

and

sup-

plies the orbicularis muscle. e transverse facial artery supplies

28,29

thermal

damage.

the skin of the cheek and anastomoses with the infraorbital artery.

CLINICAL

EXTERNAL

CAROTID

Temporal

e

other

branch

of

the

common

carotid,

the

external

carotid

affect

any

and

branches of this artery that supply the globe or orbit are discussed.

jaw

cause

the

Artery

facial

arter y

arises

from

the

external

carotid

near

the

cranial

pain

(or

giant

artery

with

ischemia

supercial

biopsy

e

arteritis

cell

Arteritis

but

arteritis)

often

is

involves

an

inammatory

the

supercial

is

of

chewing.

the

optic

temporal

taken

from

the

Involvement

nerve

artery

artery

resulting

often

as

it

is

of

in

the

necessary

crosses

posterior

permanent

the

to

conrm

zygomatic

30

the

mandible,

runs

along

the

posterior

edge

of

the

lower

anterior

to

the

ear.

jaw,

Anterior

temporal

artery

Zygomatic

artery Superficial

temporal

Angular

artery

Transverse

artery

facial

artery Infraorbital

artery

External

carotid

artery

(within

infraorbital

Maxillary

artery

groove)

External

Facial

Fig.

12.12

Branches

of

the

external

carotid

artery

artery

carotid

artery

that

supply

ocular

adnexa.

(Modied

ciliary

vision

angle superiorly

of

condition

temporal

that

can

artery.

The

disease usually is accompanied by headache, tenderness in the temporal area,

artery, passes upward through the tissue of the neck. Only those few

Facial

COMMENT: Temporal

ARTERY

from

Clemente CD. Anatomy: a Regional Atlas of the Human Body. Munich: Urban and Schwarzenberg; 1987 .)

the

artery

loss.

diagnosis.

process

can

Biopsy

and

of

The

travels

CHAPTER

shi

Maxillary

causing

other

proximity

the

branch

to

the

of

the

orbit

infratemporal

is

external

carotid

that

supplies

the maxillar y arter y.

fossa

and

then

upward,

It

passes

medial

to

areas

in

through

the

man-

infratemporal

ability

in

both

its

fossa,

the

branching

maxillar y

pattern

arter y

and

in

shows

its

some

by

both

direction

arteries

children.

is

from

internal

the

ocular

dibular joint toward the maxillar y bone (see Fig. 12.12). Within

the

Orbital

of

Blood

blood

ow

203

Supply

within

territories

sup-

Artery plied

e

the

12

are

has

not

and

structures,

shown

in

the

as

to

change

yet

been

ow

studied

external

well

as

chart

within

a

short

in

carotid

time

adults.

arteries

their

most

in Fig.

12.13

period

e

that

common

in

branches

supply

the

anastomoses,

vari-

topographic

rela-

VEINS

OF

THE

ORBIT

31–33

tions

with

arter y,

orbit

other

runs

along

through

for ward

passes

the

along

the

One

orbital

infraorbital

the

(see

Fig.

12.11).

e

in

canal,

the

fossa

ssure.

groove

infraorbital

foramen

branch,

pter ygopalatine

inferior

the

through

infraorbital

structures.

and

enters

arter y

the

and

infraorbital

then

maxillar y

exits

the

an

veins

blo o d

bone,

through

Occasionally,

e

runs

dients.

the

ded

orbital

t he

of

ow

t he

may

O ver

wit hin

orbit.

a

t he

orbit

have

change

large

par t

of

connec tive

Unlike

t he

no

and

valves;

is

t heir

t issue

paral lel

t hus

deter mined

pat h,

s ept a

routes

t he

t hat

of

t he

by

dire c t ion

pressure

veins

are

of

g ra-

emb e d-

compar t ment alize

veins

and

ar ter ies

in

34

branch

extends

from

the

infraorbital

groove

into

the

orbit.

most

of

t he

b o dy,

many

orbit a l

veins

follow

10

e

sac,

infraorbital

and

it

arter y

supplies

anastomoses

with

the

the

lower

angular

eyelid

arter y

and

and

lacrimal

the

fers

dorso-

f rom

t he

opht halmic

cor resp onding

ar ter y

but

two

a

cours e

t hat

dif-

36

ar ter ies.

e

opht halmic

orbit

veins.

has

e

a

sing le

sup er ior

35

nasal

arter y.

arter y

and

sends

teeth

While

supplies

of

the

the

some

in

the

inferior

infraorbital

rectus

branches

upper

to

and

the

canal,

the

inferior

maxillar y

infraorbital

oblique

sinus

and

muscles

and

to

is

great

Superior

anastomoses

the

orbit

variation

between

may

var y

in

the

vessels.

depending

origin

of

blood

Direction

on

the

of

vessels

blood

dominance

and

ow

of

the

opht halmic

veins

pr imar ily

the

angular

within

e

Ophthalmic

superior

carotid

arter y

arter y

or

is

internal

carotid

completely

arter y

occluded,

ow.

blood

into

t he

cav-

and

notch,

internal

above

and

vein

supraorbital

supraorbital

external

Vein

ophthalmic

the

vein

enters

angular

is

veins

the

vein

formed

within

orbit

passes

1

carotid

drain

sinus.

the

jaw.

e

ere

infer ior

er nous

by

the

the

through

through

joining

orbit

the

the

(Fig.

of

the

12.14).

supraorbital

orbital

septum

37

If

ow

the

to

the

entire

the

e

medial

superior

canthal

tendon.

ophthalmic

vein,

the

larger

of

the

two

oph-

14

orbit

may

balance

originate

between

the

from

the

internal

external

and

carotid

external

arter y.

carotid

e

arteries

thalmic

can

Internal

veins,

posteriorly,

Carotid

Ophthalmic

runs

with

receives

the

blood

ophthalmic

from

veins

arter y

that

and,

drain

as

the

it

passes

superior

Artery

Artery

Posterior

Muscular

Anterior

Posterior

Medial

Lacrimal

Supraorbital

Supratrochlear

Dorsonasal

retinal

ciliary

arteries

ethmoid

ethmoid

palpebral

artery

artery

artery

artery

artery

arteries

artery

artery

Central

artery

(or

could

branch

Lateral

ciliary

ciliary

and

and

from

palpebral

arteries

arteries

frontal

sphenoid

dorso-

artery

(10–20)

(2)

sinuses

sinuses

nasal)

Inner

Long

Short

retina

Lateral

LR,

SR,

Ethmoid

Medial

SO,

MR,

IR,

IO

Ethmoid

SR,

SO,

Anastomosis

levator

supplying

lid,

nose,

Lacrimal

lower

sac

and

cheek

levator

Choroid (through

Circle

of

Nasal

Anterior

suprachoroid)

Zinn

ciliary

(from

muscle

cavity

arteries

circle

the

head

gland

Orbicularis

Anastomosis

rectus

vessels)

Eyelids

Zygomatic

Zygomatic

Anterior

Transverse

arteries

artery

temporal

facial

artery

artery

of

body

meningeal

orbital

artery

artery

and

Superficial

Maxillary

Facial

temporal

artery

artery

artery

Middle

meningeal

artery

External

carotid

artery

Flow

structures.

ternal

IR,

Blue

carotid

inferior

chart

of

branches

indicates

artery; green

rectus;

LR,

of

branches

indicates

lateral

rectus;

of

the

the

target

MR,

internal

internal

and

external

carotid

arter y;

structures. Circles

medial

rectus;

SR,

carotid

purple

show

arteries

indicates

that

rectus;

SO,

supply

branches

anastomoses. IO,

superior

artery

Infra-

conjunctiva

Fig. 12.13

Angular

Recurrent

Anastomosis

Episclera

iris

IR,IO

supplying

iris

Ciliary

and

Lacrimal

arcades

forehead

Major

Optic

nerve

Palpebral

of

Inferior

superior

orbital

the

ex-

oblique;

oblique.

CHAPTER

204

12

Orbital

Blood

Supply

Frontal

bone

Superior

vortex

vein Superior

ophthalmic

vein

Supraorbital

vein

Central

retinal

Angular

vein

vein

Cavernous

sinus

Inferior

ophthalmic

vein

Infraorbital

vein

Pterygoid

venous

plexus

Inferior

vortex

vein

Maxillary

Fig. 12.14

orbital

structures.

It

View

passes

from

below

the

the

lateral

superior

side

of

rectus

the

orbit

bone

showing

veins

draining

the

globe

and

orbit.

muscle

not affected because it has a thicker sheath and is not compressed as easily as is

(see

Fig.

11.10)

and

crosses

the

optic

ner ve

to

the

upper

part

of 39

the vein.

the

superior

orbital

ssure

above

the

common

tendinous

The resultant blockage causes congestion of the retinal veins and ede-

ring, ma

of

the

retina.

Edema

of

the

optic

nerve

head

(papilledema)

will

be

evident

as

38

where

it

leaves

the

orbit

to

empty

into

the

cavernous

sinus. blurred disc margins, and hemorrhages will sometimes be evident (see Fig. 8.30).

e

the

veins

anterior

draining

the

that

and

drain

into

posterior

superior

and

the

superior

ethmoid

medial

ophthalmic

veins,

muscles,

the

the

vein

muscular

lacrimal

are

veins

vein,

the

Vortex

37

central

retinal

vein,

and

the

superior

vortex

e

Central

Retinal

Veins

veins.

Vein

or

vortex

ve

veins

vortex

drain

veins

is

the

choroid,

located

in

and

each

usually

quadrant

one

(see

of

the

Fig.

four

12.5).

9

e

venous

branches

located

in

the

retinal

tissue

come

together

ese

veins

and exit the eyeball as a single central retinal vein (see Fig. 12.7).

vortex

is

dilated

vessel

behind

It

the

emerges

either

drains

leaves

lamina

from

joins

the

directly

CLINICAL

The

slightly.

the

cribrosa

the

into

ner ve

the

approximately

alongside

meningeal

superior

within

pressure

The

healthy

optic

the

ophthalmic

cavernous

(IOP),

increase

eye

as

in

the

central

and

at

blood

central

retinal

peak

central

of

vein

the

or

Venous

vein

can

vein

10

to

12

retinal

optic

exits

mm

pupil

be

(Fig.

globe

seen

6

mm

with

an

posterior

indirect

to

the

equator.

ophthalmoscope

12.15).

arter y.

ner ve

the

can

the

and

orbit

and

sinus.

pulse

volume

retinal

the

sheath

COMMENT: Spontaneous

pressure

traocular

the

veins

exit

is

Pulsation

approximately

pressure

be

seen

pulsates

the

during

at

its

equal

vessel

to

walls

the

in-

expand

ophthalmoscopy

exit

through

the

of

optic

28

disc. The IOP can vary slightly (1–2 mm Hg) with this change in blood volume.

CLINICAL

The

sheaths

sheaths

of

contains

the

surround

brain.

cerebrospinal

continuous

tracranial

COMMENT: Papilledema

that

with

the

pressure,

subarachnoid

space

The

on

Thus

found

central

its

optic

nerve

subarachnoid

uid.

uid

the

the

exit

the

uid

throughout

retinal

from

vein

the

are

continuous

space,

that

the

can

optic

located

surrounds

cranial

be

with

cavity.

the

The

optic

as

central

meningeal

these

With

compressed

nerve.

the

within

layers,

nerve

increased

it

crosses

retinal

is

in-

the

artery

is

Fig.

12.15

Fundus

photo

of

vortex

veins

(arrows).

e

and

a

CHAPTER

12

Orbital

Blood

205

Supply

Angle Caver nous

Pituitar y

sinus

gland

Inter nal

of

carotid

section

a.

T emporal

lobe

Oculomotor

T rochlear

n.

n.

Abducens

n.

Ophthalmic

n.

(V1)

Maxillar y

n.

(V2)

Sphenoid

bone

Nasal Sphenoid

Fig.

12.16

location

(From

Inferior

inferior

rior

oor

of

orbit.

It

section

internal

LH,

through

carotid

Chase

RA,

the

artery

Dolph

J,

sphenoid

and

etal.

Clinical

begins

drains

blood

as

a

plexus

from

the

near

lower

the

and

ante-

lateral

muscles, the inferior conjunctiva, the lacrimal sac, and the inferior

and

nerves

the

the

cavernous

as

Anatomy

of

vein

bone

cranial

Vein

ophthalmic

the

the

Mathers

Ophthalmic

e

Coronal

of

cavity

sinus

they

Principles.

superior

temporal

abducens

orbital

bone

nerve

sinus

pass

St

Louis:

ssure

located

the

e

the

sinus.

Mosby;

anteriorly

posteriorly.

are

showing

through

1996.)

to

the

internal

medially

petrous

carotid

within

the

portion

artery

sinus,

and

of

the

covered

by

the endothelial lining of the sinus. e oculomotor, trochlear, oph-

37

vortex

veins.

It

may

form

two

branches:

36

one

that

empties

into

thalmic,

and

maxillary

nerves

are

found

in

the

lateral

wall

of

the

into

the

40

either the superior ophthalmic vein

or the cavernous sinus and

cavernous

sinus

(Fig.

12.16).

e

cavernous

sinus

drains

one that empties into the pterygoid venous plexus (see Fig. 12.14).

superior petrosal sinus, located along the upper crest of the petrous

e latter branch exits the orbit through the inferior orbital ssure

portion

(below

located

either

the

common

above

superior

or

tendinous

below

orbital

the

ssure

ring).

common

and

either

e

former

tendinous

joins

the

branch

ring

to

superior

37

passes

enter

the

ophthalmic

ral

of

in

bone

the

temporal

the

groove

and

the

bone,

and

between

occipital

into

the

bone

the

petrous

(Fig.

inferior

portion

12.17A).

petrosal

of

Both

the

sinus,

tempo-

drain

either

directly or indirectly into the internal jugular vein (Fig. 12.17B).

41

vein or empties directly into the cavernous sinus.

CLINICAL

Anterior

Ciliary

Infections

e

anterior

tival

ciliar y

capillar y

arteries,

veins

network

pierce

Infraorbital

the

and

sclera,

receive

then

and

branches

accompany

join

with

the

from

the

the

conjunc-

anterior

muscular

ciliar y

forms

in

a

of

vein

is

formed

by

several

veins

that

drain

enters

can

canal

the

and

and

the

infraorbital

inferior

ner ve,

groove.

inferior

part

passes

It

foramen

venous

posteriorly

receives

of

the

ophthalmic

pter ygoid

be

e

by

a

sphenoid

vein

can

be

Sinus

Thrombosis

dangerous.

readily

pass

An

into

infected

the

embolus

cavernous

that

sinus

via

and

must

be

treated

aggressively

with

antibiotics.

and,

with

the

branches

orbit

vein.

plexus

and

e

(see

through

from

may

vein

stula

is

an

abnormal

Sinus

Fistula

communication

between

the

in-

infraorbital

infraorbital

structures

communicate

infraorbital

Fig.

the

some

sinus

drains

in

with

the

into

the

carotid

artery

and

the

cavernous

sinus

caused

by

a

tear

in

the

artery

wall,

either traumatic or spontaneous (see Fig. 11.10). The sinus communicates directly

with

the

thalmic

veins

veins,

of

the

which

orbit,

may

so

arterial

become

pressure

enlarged

and

can

be

transmitted

pulsatile.

If

arterial

to

the

oph-

pressure

is

reduced because of this leak, a decrease in perfusion to ocular tissue will occur.

12.14).

DRAINAGE

Sinus

cavernous

splitting

can

COMMENT: Carotid-Cavernous

LYMPHATIC Cavernous

orbital

fatal

carotid-cavernous

ternal

arter y

orbit

the A

It

or

or

Vein

infraorbital

face.

face

an ophthalmic vein because these veins do not have valves. A cavernous sinus

thrombosis

veins.

the

facial

CLINICAL

e

COMMENT: Cavernous

Veins

sinus

of

bone.

the

e

is

a

dura

relatively

mater

cavernous

large

on

sinus

each

venous

side

extends

of

channel

the

from

formed

body

the

of

medial

the

end

No

lymphatic

found

drain

in

the

the

vessels

occur

conjunctiva

medial

aspects

in

and

of

the

the

the

globe

proper.

eyelids.

eyelids

e

and

the

Lymphatics

lymphatics

medial

are

that

canthal

CHAPTER

206

12

Orbital

Blood

Supply

Superior

sagittal

A

sinus

B

Inferior

sagittal

Ophthalmic

Cor tical

sinus

veins

veins

Sphenoparietal

Intercaver nous

sinus

sinus

Caver nous Falx

sinus

Inferior

cerebri Basal

petrosal veins sinus Inter nal

Basilar

Superior

Straight

cerebral

plexus

v.

sinus

petrosal

sinus

Jugular

bulb T entorium

Sigmoid

Marginal cerebelli

Left sinus

sinus sigmoid

Straight

sinus Confluence

T ransverse

of

sinuses

Inter nal

sinus

Occipital

sinus

jugular

sinus

v. Marginal

Left

transverse sinus

Confluence

Fig.

12.17

Venous

sinus

of

sinuses

drainage

sinus

of

the

cranium.

A,

Superior

view.

B,

Superior,

lateral,

posterior

view. (From Mathers LH, Chase RA, Dolph J, etal. Clinical Anatomy Principles. St Louis: Mosby; 1996.)

structures

(including

the

lacrimal

sac)

empty

into

the subman-

REFERENCES dibular

the

lymph

lacrimal

nodes.

gland

ose

empty

that

into

drain

the

the

parotid

lateral

lymph

eyelids

nodes

and

in

the

1.

42

preauricular

area

(Fig.

Bertelli

the

12.18).

E,

Regoli

orbital

M,

blood

Bracco

supply

S.

and

An

update

on

hemodynamic.

the

variations

Surg

Radiol

of

Anat.

2017;39:485–496.

2.

EFFECT

OF

AGING

ON

OCULAR

CIRCULATION

Ganiusmen

of

the

study

Changes

occurring

with

age

dier

between

individuals.

environmental

factors

are

contributor y,

but

Citak

of

20

optic

some

can

be

made.

e

density

of

the

choroidal

Kuruoglu

E,

and

beds

and

the

choroidal

and

retinal

vessel

canals.

in

optic

Turkish

A,

canal

etal.

Anatomic

decompression:

Neurosurg.

evaluation

a

cadaver

2017;27:31–36.

Cokluk

of

C,

the

Marangoz

ophthalmic

AH,

etal.

arter y :

ree

dimensional

spontaneous

intracranial-

retinal extracranial

capillar y

Samancioglu

genermicroanatomy

alities

G,

arter y

Genetic 3.

and

O,

ophthalmic

diameter

all

Neurosurg.

anastomosis

site

within

the

orbital

cavity.

Turkish

2016;26:16–20.

43

decrease

and

can

with

age.

result

in

Endothelial

increased

dysfunction

vascular

tone,

a

can

occur

reduction

with

in

age

4.

vessel

Zoli

my

M,

of

Manzoli

the

L,

Bonfatti

ophthalmic

R,

arter y

etal.

in

the

Endoscopic

optic

canal.

endonasal

Acta

anato-

Neurochirurg

43

distensibility,

is

a

and

coincident

a

decrease

decrease

in

in

tissue

retinal

perfusion.

cells,

this

Because

decrease

in

(Wien).

there

blood

5.

and posterior ciliary arteries. J Neuro Ophthalmol. 2008;28:320–324.

44,45

ow

may

be

a

response

to

decreased

metabolic

2016;158:1343–1350.

Erdogmus S, Govsa F . Anatomic characteristics of the ophthalmic

need.

6.

Zhang

T,

Fan

S,

morphometr y Parotoid

lymph

He

by

W ,

etal.

Ophthalmic

computed

tomography

arter y

visualization

angiography.

and

Graefe's

node

Arch

7.

Clin

Anatomy,

Embryolog y,

10.

2015;253:627–631.

connective

and

tissue.

In:

Teratolog y.

Jakobiec

FA,

Philadelphia:

ed.

Ocular

Harper

&

SS.

e

ophthalmic

arter y.

III.

Branches.

Brit

J

Ophthal-

1962;46:212.

War wick

and

Orbital

1982:835.

Hayreh

mol.

9.

Ophthalmol.

L.

Row ;

8.

Exp

Koorneef

R.

Orbit.

Doxanas

Clinical

Orbital

7th

MT,

ed.

vessels.

Anderson

Orbital

In:

Eugene

Philadelphia:

RL.

Anatomy.

Wol 's

Saunders;

Vascular

Baltimore:

Anatomy

1976:92

supply

of

Williams

146,

the

&

of

the

Eye

406-417.

orbit.

In:

Wilkins;

1984:153–170.

11.

Y oshii

I,

ocular

12.

Bracco

S,

arteries Submandibular

lymph

dial

The

12.18

lids

Lymphatic

and

lateral

drainage

conjunctiva

lids

and

drain

into

conjunctiva

A.

Venturi

in

A

Anat

new

look

Record.

C,

pediatric

Leonini

age

by

at

the

blood

supply

of

the

retro-

1992;233:321.

S,

etal.

high

Identication

resolution

of

intraorbital

superselective

angiog-

node

raphy.

Fig.

Ikeda

space.

of

the

the

drain

ocular

adnexa. The

submandibular

into

the

parotid

lymph

lymph

me-

node.

node.

13.

Orbit.

Hayreh

disease:

SS.

2015;34:237–247.

Posterior

e

ciliar y

Weisenfeld

2004;45:749–757;

748.

arter y

lecture.

circulation

Invest

in

health

Ophthalmol

Vis

and

Sci.

CHAPTER

14.

Biousse

V ,

Newman

Continuum

15.

Onda

E,

human

16.

uation

17.

SS.

of

J

it:

Hayreh

SS.

Ophthalmol.

Hayreh

SS.

Borchert

Clin

21.

the

23.

Hayreh

Vascular

Am.

supply

of

Justice

J

review

of

Siam

e

the

Jr,

DJ,

anatomy

stereo

of

the

and

Microvasculature

of

the

ner ve

Retinal

Eye

anatomy

of

32.

head

Res.

the

and

the

eval-

ner ve

head.

of

optic

optic

cupping

ner ve

of

head

the

and

optic

its

disc.

role

Brit

of

the

optic

disc.

Brit

RP .

fundus

in

exact

34.

J

visual

system.

Ophthalmol

in

man:

of

Brit

J

the

Microvascular

the

possible

Eye.

its

Ophthalmol.

Cilioretinal

signicance

role

Cong

L-Y ,

inferior

roll

26.

S-H,

medial

in

the

a

study

uorescein

on

Ali

aspect

macular

MH.

of

A

a

angiographic

bital

T,

the

globe:

buckling.

an

Retina

of

the

surgical

essential

Plast

studies

of

T,

etal.

arter y

Topographic

and

Reconstruct

P ,

its

Phetudom

the

terminal

and

glabellar

branches

ller

relevance

Surg.

T.

of

anatomy

to

the

Pa).

of

the

the

and

pretarsal

41.

Aesthet

arter y

Plast

Brown

vessel

28.

Cio

PL,

SM,

Alm

Elsevier ;

29.

Kilgaar

Arch

LM.

eds.

New

concepts

Ophthalmol.

Granstam

A,

42.

Surg.

E,

Adler's

Alm

of

regulation

of

1996;114:199–204.

A.

Ocular

Physiolog y

of

43.

circulation.

the

Eye.

10th

In:

ed.

Kaufman

St

Fischbarg

J,

ed.

In

PK.

e

e

choroid

Biolog y

of

and

the

optic

Eye.

ner ve

Amsterdam:

30.

Elsevier ;

K,

of

N,

10th

ed.

St

Louis:

Elsevier;

2003.

in

McNab

Vis

JV .

the

AA.

Sci.

the

maxillar y

arter y

Anzeiger.

C,

Mayr

R.

e

human

relations

in

the

maxillar y

infratemporal

1991;142(4):28.

FA,

etal.

Orbital

of

an

branch

of

important

the

infra-

surgical

Vascular

anatomy

of

the

eyelids.

G,

Komatsu

orbit.

Nippon

A,

etal.

Ganka

Gross

anatomi-

Gakkai

Zasshi.

S,

Whiting

Nakamura

Surg

AS,

Radiol

Wobig

JL.

lid.

Wobig

In:

Am

e

San

anatomy

of

Tabuchi

LN.

the

orbit.

Invest

MJ,

e

superior

magnetic

ophthal-

resonance

2015;37:75–80.

Physician.

Francisco:

etal.

Papilledema:

vessels

Reeh

T,

high-resolution

Anat.

Fam

blood

JL,

M,

with

Johnson

diagnosis.

Venous

2003;44(3):988.

delineation

vein:

Cornelius

C-P ,

Plast

Shoukath

Surg.

S,

of

Mayer

features

and

clinical

clues

and

dieren-

1992;45(3):125.

lymphatics

Wirtschaer

American

JD,

of

the

eds.

Academy

of

orbit

and

Ophthalmic

Ophthalmolog y ;

P ,

in

Ehrenfeld

view

of

M,

etal.

innovative

e

orbits—

surgical

methods.

2014;30:487–508.

Taylor

the

GI,

lower

postoperative

Ehrlich

R,

Mendelson

eyelid

and

chemosis

Kheradiya

vascular

NS,

changes.

Grunwald

foveolar

45.

L am

JE,

BC,

etal.

e

conjunctiva

and

edema.

Winston

Graefe's

Hariprasad

choroidal

AK,

Chan

supply

color

S,

SM,

circulation.

C han

H,

deter mined

2003;89(4):305.

Eye.

of

Anatomischer

characterization

Murakami

veins

and

the

Surg.

1994;101:1118.

Tsutsumi

blo o d

of

Neck

2015;34:212–215.

Lindberg

Sires BS, Gausas R, Cook BE Jr, etal. Orbit. In: Kaufman PL, Alm A,

Physiology

fossa.

topographical

further

eds.

Adler's

variability

Head

lymphatic

and

Plast

correlation

Reconstruct

Surg.

DM,

Arch

etal.

Clin

Age-related

Exp

Ophthalmol.

2009;247:583–591.

In:

2006:273–290.

topography

Jakobiec

mic

ocular

Louis:

head.

arter y

2017;139:628e–637e.

44.

Jensen

Cheung

anatomy

retinal

2003.

JF ,

study

with

Jampol

tone.

GA,

Murakami

Facial

2017;41:678–688.

27.

e

(Basel).

A,

Orbit.

SM,

Anatomical

intraor-

ophthalmic

placements.

maxillar y

Otolaryngol

1981:77.

2016;138:430e–436e.

Periorbital

fossa.

Skopako

Anatom

arter y :

Tucker

tial

40.

(Philadelphia,

ML,

Rashid

Anatomy.

Tansatit

Apinuntrum

periorbital

Acta

AV ,

imaging.

39.

restudy

B.

reinvestigated:

Ophthalmol

38.

based

Internal

207

Supply

1991;95(1):31(Abstract).

blood

1976;94:1355.

TA,

palpebral

augmentation.

Tansatit

for

Lee

Patel

cal

37.

in

A.

infratemporal

Ophthalmolog y.

of

1963;47:651.

arteries:

and

study

1990;4:7.

retina:

Moriggl

the

landmark.

2011;31:1405–1411.

25.

G,

Pretterklieber

fossa.

J

36.

AC.

photographs

posterior

for

the

neuropathy.

Ophthalmol.

the

of

Khan

Blood

1991;172(3):197(Abstract).

33.

35.

arter y

ner ve.

Ortug

arter y

oedema

AL,

pter ygopalatine

within

2001;20(5):563.

optic

the

Orbital

1991;104(2):204.

1995;120:92.

optic

Morton

in

orbital

ner ve

El-Mamoun

of

Prog

anatomy

central

optic

Arch

topography

the

McCartney

optic

Lehmann

ALH,

31.

1996;9(3):327.

ischaemic

ndings.

24.

supply

Spalton

SS.

ischemia.

2008;43:308–312.

glaucoma,

retrolaminar

anterior

22.

ner ve

1974;58:863.

MS.

JM,

of

Vascular

Pathogenesis

North

Olver

etal.

Ophthalmol.

reality.

G.

optic

1969;53:721.

Ophthalmol.

20.

J

and

2014;20:838–856.

DR,

supply

and

Cio

Blood

atrophy,

Am

blood

myth

PJ,

Retinal

Minn).

Bacon

ner ve.

Ophthalmol.

optic

19.

GA,

e

MacKenzie

Can

18.

Cio

optic

Hayreh

N.

(Minneap

12

D oppler

DuPont

Arch

etal.

by

J.

Eect

of

Ophthalmol.

e

eec t

pu ls at i le

ultras onog raphy.

of

o c ular

O ptom

aging

on

1998;116:150.

age

on

blo o d

Vision

o c ular

ow

S ci.

13

Cranial

e

IV ,

orbital

V ,

ated

VI,

structures

and

muscles

motor

ner ve

ner ve.

sor y

the

cranial

vation

15.

of

senting

ner ve

carries

is

the

signs

by

V ,

the

by

Motor

the

and

visual

ner ve

including

and

sensor y

pathways,

is

and

III,

stri-

oculo-

cranial

the

carries

of

II,

the

the

VII,

Cranial

information

of

ner ve;

ner ve

ner ve,

str uctures.

discusses

ner ves

III,

trochlear

cranial

trigeminal

orbital

cranial

functions

cranial

IV ,

ner ve;

chapter

orbit,

of

13.1).

ner ve

the

Inner vation

inner vated

controlled

from

ner ve,

Chapter

are

(Table

abducens

Cranial

supply

optic

VII

are

ner ve;

VI,

Ner ve

facial

the

ner ve

sen-

II,

the

discussed

motor

functions,

become

cranial

is

larger

ner ve,

hoped

enable

the

action

Fig.

dysfunction.

processing

and

communication

tral

nervous

system

branches

occurs

through

within

between

ber

the

brain

dierent

tracts.

A

or

spinal

areas

ber

of

tract

cord

the

that

cen-

con-

nects one area of the brain with another area of the brain is called

called

a

nucleus

bers

ner ve.

orbit

or

a

ganglion.

e

ber

tract

traveling

toward

medial

ent

bers.

fascicular

portion

the

Aerent

to

sensor y

of

the

central

bers

cranial

ner vous

usually

nerve.

system

have

via

aer-

specialized

ner ve

endings that respond to such sensations as touch, pressure, tem-

perature,

and

Division

of

Nerve.

in

the

ganglion

the

enter

actual

and

of

the

the

h

pons.

unconventional,

information

branches

ganglion

and

although

mind

the

the

e

inner vate

the

direction

ow,

paths

Trigeminal

nasociliar y

the

globe

structures

lacrimal

nasal

the

the

ar y

(see

of

and

the

sac,

in

of

of

these

the

It

will

the

bers.

trigeminal

Nerve

ner ve

has

a

surrounding

medial

medial

and

orbit

ner ve

and

Fig.

the

number

areas.

canthal

aspect

of

of

Sen-

area—the

the

it

runs

the

form

orbital

along

skin

the

the

eyelids,

infratroch-

septum,

upper

nasociliar y

along

sinuses

ethmoid

sinuses

ner ve.

suture.

along

the

the

form

companion

frontoethmoid

as

to

enters

border

ner ve

the

of

the

as

other

the

nose,

13.1).

the

ethmoid

their

the

runs

becoming

ethmoid

from

with

the

nose—join

penetrates

from

posterior

center

of

the anterior

and

e

the

sphenoid

ethmoid

arteries

ner ves

medial

aspect

join

of

sinus

ner ves

through

B oth

ethmoid

enter

foramina

the

the

nasocili-

orbit

(see

13.1).

Corneal

Eerent bers, either somatic or autonomic, carry information

it

mucosa,

within

ner ve

the

trochlea,

bers

Fibers

of

muscle,

join

the

side

is

Sensor y

Fig.

pain.

the

rectus

branches

brainstem

comes

at

below

form

the

in

thus

major

the

orbit.

from

lear

ner ve.

is

the

canaliculi,

skin

or away from the cranial nerve nucleus but still located within the

Information

keep

and

the

that

and

a fasciculus or a peduncle. A collection of cranial nerve cell bodies

is

to

exit

SYSTEM

Information

involves

presentation,

Nasociliary

caruncle,

NERVOUS

together

this

shows

within

come

then

reader

Ophthalmic

pre-

sor y

THE

ner ves,

and

potential,

13.1

ner ve

that

Structures

in

inner-

and

Ocular

sensor y

inner vation

is

dense,

estimated

to

be

400

1

from the

central nervous system to the target structures: muscles,

times

as

dense

organs, or glands. e eerent pathway in the somatic system gen-

networks,

erally

basal

consists

of

a

ber

that

runs

the

distance

from

the

central

or

plexus

as

other

plexuses,

collects

epithelial

of

corneal

terminal

tissue

ner ves

branches.

inner vation.

are

is

formed.

ree

e

connects

sub-

with

the

2

nervous system to the target muscle. e autonomic pathway gen-

subepithelial

erally has a synapse within its eerent pathway (see Ch. 14).

ner ves

AFFERENT

PATHWAY:

ORBITAL

are

plexus

found

or

endothelium.

in

the

in

and

the

e

peripheral

the

midstromal

posterior

bers

stroma

from

and

plexus

stroma,

these

radiate

(Fig.

Descemet

plexuses

out

into

13.2).

membrane,

come

the

No

together

limbus

as

70

SENSORY to

80

branches.

ey

become

myelinated

in

the

last

2

mm

of

the

3–5

INNERVATION

cornea.

S ome e

eye

is

richly

supplied

with

sensory

nerves

that

carry

ot her tions

of

touch,

cornea,

pressure,

iris,

warmth,

conjunctiva,

and

cold,

and

sclera

pain.

consist

Sensations

primarily

t he

anter ior

cor ne al

ner ve

of

s egment

branches

st r uc tures

to

join

wit h

for m

two

ner ves

l ong

f rom

ci liar y

from ner ves.

the

of

sensa-

In

addition

to

aerent

b ers,

t he

long

ci liar y

ner ves

pain; transmit

sympat hetic

b ers

to

t he

di lator

mus cle

of

t he

ir is.

even light touching of the cornea is registered as irritation or pain. es e

t he

Trigeminal

medial

s clera

p oints

lar

(Fig.

structures

the

e

208

are

sensor y

description

involved

ciliar y

side

of

ner ves,

t he

one

g lob e,

on

t he

cours e

lateral

b etween

side

t he

and

one

choroid

on

and

Nerve

e bers of the trigeminal ner ve (cranial ner ve V) ser ving ocu-

tures.

long

of

structures

and

the

and

originate

pathways

follows

in

of

the

the

inner vated

these

ner ves

ner ves

as

struc-

begins

they

join

at

to

copy

to

t he

13.3).

at

ciliar y

back

of

approximately

t he

es e

3:00

ner ves

t he

3

ner ves

and

t hen

are

9:00

j oin

e ye

mm

w here

on

e ach

visible

side

wit h

p osit ions

t he

t he y

13.4).

ner ve.

t he

t he

indirec t

(Fig.

nas o ciliar y

le ave

of

g lob e

opt ic

at

ner ve

opht halmos-

e

two

long

CHAPTER

TABLE

Cranial

II.

13.1

Cranial

Nerve

Optic

III.

Retinal

Oculomotor,

Nerves

Innervating

Origin

inferior

13

Cranial

Orbital

Nerve

ganglion

cells

division

Lateral

geniculate

rectus

muscle

nucleus

Motor:

Sensory:

Inferior

rectus

muscle

Motor:

depression,

Inferior

oblique

Motor:

elevation,

muscle

ganglion

Oculomotor,

superior

Midbrain

division

IV:

Trochlear

VI:

Abducens

VII:

Midbrain

Facial

Superior

rectus

Superior

palpebral

Superior

muscle

oblique

Pons

Lateral

Pons

Frontalis,

rectus

A

slight

the

COMMENT: Nerve

variation

bers

loop

can

into

occur

the

in

sclera

the

from

Loops

(of

pathway

the

of

the

long

be

side.

Often

this

differentiated

raised

from

a

area

is

pigmented,

melanoma.

The

and

ciliary

usually

nerve

blue

loop

or

may

nerve

be

motor

to

extorsion

extorsion

iris

sphincter

and

ciliary

muscle

for

miosis

adduction,

of

intorsion

eyelid

depression,

abduction,

intorsion

abduction

facial

expressions,

closure

of

eyelids

muscles

forming

black,

elevation

Motor:

ganglion

Parasympathetic: secretomotor to lacrimal gland for lacrimation

e

space,

elevation,

Motor:

Motor:

corrugator,

adduction,

abduction,

accommodation

Motor:

Axenfeld)

suprachoroidal

sight

Motor:

muscle

in

which

a

dome-

shaped elevation about 2 mm from the limbus on either the nasal or the tempo-

ral

muscle

muscle

Sphenopalatine

CLINICAL

levator

procerus,

orbicularis

209

Structures

adduction

Parasympathetic:

and

III:

Ocular

Function

Medial

Ciliary

of

Structures

Destination

Midbrain

Innervation

and

painful

should

into

body.

limbus

ey

where

e

remaining

the

they

short

sensor y

join

enter

the

leave

ciliar y

as

branches

sensor y

choroid,

6

to

ner ves

10

then

short

exit

radiating

ner ves

the

from

course

ciliar y

sclera

in

from

the

to

the

ner ves

a

ring

iris

the

cornea

and

back

(see

of

ciliar y

the

Fig.

around

eye

13.3).

the

optic

when

ner ve

in

company

with

the

short

posterior

ciliar y

arteries

and

3

touched,

a

characteristic

that

should

aid

in

its

diagnosis.

enter

the

ciliar y

ganglion

(see

Fig.

13.1).

e

Supratrochlear

nerve

Supraorbital

nerves

Superior

oblique

Infratrochlear

nerve Lateral

rectus Medial

rectus

Anterior

ethmoid

Zygomatico-

nerve

temporal

nerve

Zygomatico-

facial

Long

ciliary

Short

nerve

ciliary

nerves

nerve

Ciliary

ganglion

Posterior Long

ethmoid

ciliary

Sensory

ciliary

Nasociliary

Frontal

nerve

Lacrimal

nerve

Ophthalmic

nerve

Infraorbital

13.1

Orbit

viewed

from

above

showing

to

the

ganglion

nerve

nerve

nerve

Maxillary

nerve

Mandibular

nerve

Trigeminal

root

nerve

Zygomatic

Optic

Fig.

nerve

nerve

ganglion

branches

of

the

ophthalmic

nerve.

sensor y

bers

do

CHAPTER

210

13

Cranial

Nerve

Innervation

of

Ocular

Structures

Squamous

epithelium

Basal

epithelium

Subbasal

Sensory

nerve

plexus

terminals

Bowman

layer

Subepithelial

plexus

Stromal

nerve

midstromal

Fig.

13.2

epithelial

the

basal

corneal

not

synapse

but

pass

from

Stroma

plexus

Innervation

plexus

of

the

penetrates

epithelium

and

cornea.

Stromal

Bowman

Bowman

layer

layer.

ner ves

and

The

gives

give

rise

subbasal

rise

to

a

plexus

root

of

the

through

ciliar y

the

ganglion,

ganglion,

which

leaving

then

as

joins

the

the

ner ve.

e

short

ciliar y

ner ves

carr y

sympathetic

the

bers

in

nasociliar y

off

plexus. The

that

branches

lies

that

sub-

bet ween

supply

the

addition

ner ve

is

to

sensor y

formed

by

COMMENT: Herpes

zoster

is

an

acute

CNS

Zoster

infection

caused

by

the

varicella-zoster

virus.

and and

symptoms

include

pain

and

rash

in

the

distribution

area

supplied

bers. by

us

gives

plexus

sen-

Signs

parasympathetic

subepithelial

nasoHerpes

ciliar y

a

epithelium.

CLINICAL

sor y

to

subbasal

the

joining

of

the

a

the

affected

sensory

sensory

ganglion

nerves.

and,

on

It

is

believed

becoming

that

activated,

the

virus

migrates

lies

down

dormant

the

in

sensory

6

infratrochlear ner ve, the anterior and posterior ethmoid ner ves,

pathway

the

persons but may occur at any age and may be related to a delayed hypersensi-

long

ciliar y

ner ves,

and

the

sensor y

root

of

the

ciliar y

gan-

to

the

skin.

An

eruption

of

herpes

zoster

is

more

common

in

elderly

7

glion

(see

Fig.

13.1).

e

nasociliar y

ner ve

exits

the

orbit

by

tivity

reaction.

Approximately

of

all

Involvement

10%

of

cases

affect

the

ophthalmic

division

8

passing

through

the

oculomotor

foramen

within

the

common

of

the

that

tendinous

ring

and

the

superior

orbital

ssure

into

the

trigeminal

It

then

joins

the

frontal

and

lacrimal

ner ves

to

the

eye

form

branch

of

the

trigeminal

Superior

also

be

involved,

reecting

tip

the

of

the

nose

distribution

often

This

association

of

ocular

involvement

with

of

zoster

the

nose

is

called

Hutchinson

sign.

ner ve.

rectus

muscle

Superior Shor t

oblique

posterior muscle

ciliar y

ar teries

Vor tex

vein

Lateral

rectus

Medial

muscle

rectus

muscle

Long

posterior

ciliar y

ar ter y

Optic

ner ve

Long

Inferior

Shor t

Vor tex

13.3

the

The

long

Inferior

Posterior

optic

posterior

and

nerve

short

sclera.

passing

ciliary

apertures.

apertures.

vein

ciliar y

ner ves

ing

ner ve

oblique

muscle

Fig.

ciliar y

The

rectus

Posterior

through

arteries

vortex

and

veins

muscle

portion

the

of

the

posterior

ner ves

are

are

passing

globe

scleral

show-

foramen.

passing

the

indicates

nasociliary

affecting

the of

ophthalmic

will

the

cranial

branches.

cavity.

nerve.

through

through

middle

Fig.

13.4

Long

ciliary

nerve

(arrow)

the

tip

CHAPTER

Levator

Superior

Lateral

tarsus

13

Cranial

Supraorbital

palpebrae

superioris

Nerve

vein,

tendon

and

Innervation

ar ter y ,

of

Ocular

211

Structures

Supratrochlear

ner ve

ar ter y,

vein,

and

ner ve

palpebral

ar ter y

Infratrochlear

ar ter y,

Lacrimal

vein,

Lateral

palpebral

arcade

ar ter y Medial

palpebral

Medial

canthal

ar ter y

canthal

tendon

Lateral

ner ve

ner ve

Superior

Lacrimal

and

tendon

palpebral

ar ter y Inferior

palpebral

arcade

Supercial

temporal

ar ter y

and

vein Angular

Orbital

ar ter y

and

vein

septum

Inferior

tarsus

Infraorbital

T ransverse

facial

ar ter y

and

ner ve

ar ter y

Fig.

13.5

Klonisch

Sensory

S.

innervation

Sobotta.

Clinical

to

Atlas

the

of

upper

Human

Frontal Nerve. Sensory bers from the skin and muscles of the

forehead

and

medial

upper

eyelid

come

together

and

form

and

lower

Anatomy.

the

eyelids.

Elsevier;

receives

From

Klonisch

T ,

Hombach-

2019.

sensor y

bers

from

the

oculomotor,

trochlear,

and

abducens ner ves. Some of these bers likely carr y proprioceptive

11

supratrochlear

notch

or

ner ve.

foramen,

if

is

nerve

present,

and

travels

enters

in

the

the

orbit

supratrochlear

by

piercing

9

superior

medial

Sensor y

scalp,

and

ner ve,

ner ve

corner

bers

upper

lateral

from

the

the

the

eyelid

to

generally

of

orbital

skin

form

a

septum

and

muscles

second

supratrochlear

enters

the

orbit

(Fig.

ner ve,

ner ve.

through

the

the

the

Maxillary

forehead,

supraorbital

e

from

the

extraocular

muscles.

10

13.5).

of

information

the

supraorbital

supraorbital

notch

Division

Infraorbital

sor y

the

bers

maxillar y

the

Nerve.

from

posteriorly

of

the

bone

e

Trigeminal

infraorbital

cheek,

upper

through

through

the

Nerve

the

lip,

ner ve,

and

infraorbital

infraorbital

formed

lower

canal

by

eyelid,

foramen.

and

It

groove

sen-

enters

runs

in

the

9

or foramen, accompanied by the supraorbital arter y.

orbital

and

ner ve

forms

courses

the

joins

the

back

through

periorbita,

sure

above

the

Lacrimal

the

supratrochlear

frontal

exiting

ner ve

ner ve

Fig.

orbit

between

the

orbit

through

tendinous

Sensor y

bers

midway

13.1).

the

common

Nerve.

(see

the

the

e

e supra-

in

the

frontal

levator

orbit

ner ve

muscle

superior

and

orbital

s-

maxillar y

While

it

bone

is

in

eyelid

and

temple

area

the

10.9)

infraorbital

along

canal,

with

the

infraorbital

branches

join

from

arter y.

the

up-

12

per

teeth

bital

and

and

groove,

joins

maxillar y

it

exits

other

the

bers

sinus.

orbit

to

As

the

through

form

the

ner ve

the

leaves

inferior

maxillar y

the

infraor-

orbital

ssure

ner ve.

ring.

from

the

lateral

aspect

of

the CLINICAL

upper

(see Fig.

come

together

(see

Fig.

13.5)

COMMENT: Referred

Pain

and Referred pain is pain felt in an area remote from the actual site of involvement;

enter

the

lacrimal

gland.

ey

join

the

sensor y

bers

that

ser ve however, the two areas are usually connected by a sensory nerve network. Fre-

the

gland

itself

to

form

the

lacrimal

ner ve.

e

lacrimal

ner ve quently,

leaves

the

the

gland

lateral

from

tion

the

of

rectus

runs

muscle

zygomatic

the

through

and

lacrimal

the

posteriorly

(see

ner ve

13.1).

containing

gland.

superior

Fig.

along

orbital

e

It

ssure

may

the

lacrimal

above

the

upper

border

receive

autonomic

ner ve

the

exits

muscle

a

of

branch

inner va-

the

orbit

the

Aer

and

the

exiting

frontal

the

trigeminal

trigeminal

nerve

are

involved

in

referred

pain.

A

An abscessed tooth can cause

pain

should

described

orbital

cause

by

for

a

patient

the

pain

as

can

ocular

be

pain

found.

and

This

be

situation

suspected

likely

occurs

when

no

because

the overload of sensation carried by the infraorbital nerve from the upper teeth

cone.

interpreted

by

the

brain

as

coming

from

another

area

also

served

by

the

nerve.

Formation

orbit,

ner ve

the

3

trigeminal

Nerve

of

experienced when an individual eats ice cream.

is

Ophthalmic

pathways

common example is a momentary severe bilateral frontal headache sometimes

join

ner ve

the

and

(Fig.

nasociliar y

form

13.6).

the

ner ve,

lacrimal

ophthalmic

e

ophthalmic

ner ve,

division

ner ve

Zygomatic

of

then

bit

through

a

Nerve. Sensory

foramen

in

the

bers

from

zygomatic

the

bone

temple

as

enter

the

or-

the zygomatico-

13

enters

the

the

two

lateral

dural

wall

layers.

of

the

While

cavernous

in

the

sinus,

wall

of

coursing

the

sinus,

between

the

ner ve

temporal

lower

nerve.

eyelid

enter

Fibers

the

from

orbit

the

lateral

through

a

aspect

foramen

of

in

the

cheek

the

zygomatic

and

CHAPTER

212

Anterior

13

Cranial

ethmoid

Nerve

Posterior

nerve

Innervation

of

Ocular

Structures

ethmoid

nerve

Infratrochlear

Nasociliary

Frontal

Lacrimal

nerves

nerve

nerve

nerve

nerve

nerve

ganglion

carotid

(V1)

Cranial

Trigeminal

Internal

Ophthalmic

V, Cranial

artery

nerve

V,

mesencephalic

Trigeminal

principle Superior

sensory

nucleus

nerve

nucleus orbital

Cavernous

fissure

sinus

Pons

Foramen

Foramen

rotundum

Infraorbital

Infraorbital

nerve

foramen

Long

ciliary

Short

nerves

ciliary

nerves

Ciliary

Pterygopalatine

ganglion

ganglion

oval

Maxillary

nerve

Mandibular

(V2)

nerve

Petrous

(V3)

temporal

bone Cranial

nerve

nucleus

spinal

Fig.

13.6

lateral

Branches

of

the

trigeminal

nerve

that

innervate

ocular

structures

as

seen

of

V

the

tract

from

the

side.

13

bone

as

the

zygomaticofacial

nerve.

ese

two

nerves

join

to

inner vate

the

muscles

of

mastication,

pass

along

the

lower

edge

14

become

the

zygomatic

nerve

and

course

along

the

lateral

orbital

wall, exiting the orbit through the inferior orbital ssure and join-

of

the

the

ing the maxillary nerve (see Fig. 13.1).

ganglion.

Having

been

zygomatic

teeth

Nerve

and

maxillar y

sphenoid

Formation

formed

ner ve,

gums,

ner ve

bone.

by

and

the

and

it

joining

from

mucous

traverses

As

of

ner ves

the

courses

of

the

the

infraorbital

roof

of

membranes

area

between

within

the

sensor y

bers

have

cell

bodies

within

ganglion.

e bers leave the trigeminal ganglion and enter the lateral

aspect

Maxillary

Only

the

the

of

the

the

ner ve,

mouth,

cheek,

maxilla

pter ygopalatine

the

upper

and

the

from

of

the

the

ascending

the

sor y

it

ing

Aer

and

nuclei

tract

as

of

a

either

ner ve.

structures

structures.

the

fossa,

pons

trigeminal

of

the

e

the

entering

face

the

descending

the

in

the

and

root

root

head,

brainstem,

tract,

trigeminal

terminates

sensor y

sensor y

both

ner ve

the

motor

all

bers

terminating

13.6).

sensor y

root

information

including

these

(see Fig.

principal

or

carries

orbital

form

in

the

e

an

sen-

ascend-

nucleus

in

the

15,16

receives

glion

some

(see Fig.

lacrimal

autonomic

13.6).

gland

and

bers

ese

are

from

autonomic

discussed

in

the

pter ygopalatine

bers

are

Chapter

destined

14.

e

gan-

for

the

maxillar y

pons;

it

registers

descending

tions,

the

tract,

courses

sensations

which

through

of

carries

the

touch

pain

pons

and

and

and

pressure.

e

temperature

medulla

to

the

sensa-

elongate d

15,16

ner ve

enters

the

skull

through

the

foramen

rotundum.

nucleus

of

the

spinal

tract.

is

tract

extends

into

the

15,16

second

Mandibular

Division

of

the

Trigeminal

Nerve

to

fourth

cer vical

at

segments

mesencephalic

nucleus

the

brain

proprioception

of

the

junction

of

spinal

the

cord.

pons

A

and

mid-

15,16

e

mandibular

both

sensor y

ner ve

and

inner vates

motor

bers.

It

the

lower

enters

the

face

skull

and

via

contains

the

fora-

the

receives

trigeminal

nuclei

is

relayed

bers.

to

the

Information

thalamus

from

through

both

16

men

crossed

ovale.

the

Trigeminal

As

the

run

posteriorly

(Fig.

ous

Nerve

ophthalmic

13.7).

sinus.

e

e

and

uncrossed

principal

sensor y

bers.

e

nucleus

in

motor

the

nucleus

is

medial

to

pons.

Formation

and

within

maxillar y

the

mandibular

sensor y

divisions

lateral

wall

division

bers

from

of

lies

the

enter

the

just

three

the

skull,

cavernous

below

the

divisions

they

sinus

cavern-

enter

the

CLINICAL

COMMENT: Oculocardiac

The

oculocardiac

and

faintness

reex

and

can

consists

be

of

elicited

Reex

bradycardia

by

pressure

(slowed

on

the

heartbeat),

globe

or

nausea,

stretch

on

the

17–19

extraocular muscles (e.g., during ocular surgery).

Fibers from the trigeminal

trigeminal ganglion (gasserian ganglion, semilunar ganglion)

spinal

where

the

sensor y

cell

bodies

are

found

(see Fig.

13.6).

e

attened

and

semilunar

in

shape,

is

located

lateral

to

carotid

arter y

and

the

posterior

portion

of

the

can

project

activate

the

reex

can

be

20–22

sinus.

e

motor

bers

of

the

mandibular

division,

the

reticular

synapses,

blocked

cavernmuscular

ous

into

vagus

formation

precipitating

near

this

the

vagus

reex.

The

nerve

motor

nuclei

aspect

the of

internal

nucleus

ganand

glion,

which

atropine.

by

retrobulbar

anesthesia

or

intravenous

or

intra-

CHAPTER

13

Cranial

Nerve

Innervation

Angle

of

Ocular

213

Structures

Inter nal

of

Caver nous

Pituitar y

section

sinus

gland

carotid

a.

T emporal

lobe

Oculomotor

T rochlear

n.

n.

Abducens

n.

Ophthalmic

n.

(V1)

Maxillar y

n.

(V2)

Sphenoid

bone

Nasal Sphenoid

Fig. 13.7

etal.

Detailed

Clinical

cross-section

Anatomy

cavity

sinus

of

Principles.

the

St

cavernous

Louis:

Mosby;

sinus. (From

The

EFFERENT

PATHWAY:

MOTOR

cranial

and

adnexa

abducens

ner ves

are

that

the

ner ve,

supply

the

oculomotor

and

the

facial

nucleus

striated

ner ve,

muscles

the

of

trochlear

the

orbit

ner ve,

the

ner ve.

e

Nerve:

oculomotor

Cranial

ner ve

vating

Nerve

inner vates

the

in

Nuclei

medial

for

t he

t he

Chase

le vator

c aud a l

inner vating

rectus

the

tralateral

Oculomotor

LH,

RA,

Dolph

J,

mus cl e

is

s ing le

and

is

l o c ate d

NERVES cent ra l ly

e

Mathers

1996.)

muscles

superior

eye.

e

are a

the

(Fig .

inferior

supply

rectus

the

muscle

decussating

13.9).

rectus,

inferior

ipsilateral

decussate

bers

pass

eye.

and

oblique,

Fibers

supply

through

the

and

inner-

the

con-

opposite

III

superior

rectus,

medial Cerebral

aqueduct

Superior

rectus,

inferior

rectus,

inferior

oblique,

and

superior

palpebral colliculus Midbrain

levator

muscles.

It

also

provides

a

route

along

which

the

autoOculomotor

nomic

bers

travel

to

inner vate

the

iris

sphincter

muscle,

the nucleus

ciliar y

muscle,

and

the

smooth

muscles

of

the

Oculomotor

eyelid.

Trochlear

nerve nucleus

Oculomotor

Nucleus

Inferior

colliculus

The

o c u l omotor

nu cl e us

is

lo c ate d

in

t he

mi dbrain ,

at

t he

Trochlear

le vel

of

t he

sup er ior

col lic u lus ,

vent r a l

to

t he

cerebra l

aquenerve

duc t,

13.8).

and

A

nucleus

dors a l

to

def init ive

cont rols

t he

are a

e a ch

me d i a l

or

long itu d ina l

subnucleus

mus cle.

The

w it hin

prop os e d

f as c i c u lus

t he

Pons

(Fig .

o c u lomotor

ar range ment

of

Abducens

t he

subnuclei

are

p ostu l ate d

pr imar i ly

on

t he

b asis

of

aniAbducens

nucleus

nerve

23–25

ma l

mo dels.

The

nucleus

for

t he

me d i a l

re c tus

is

lo c ate d

Medial

toward

t he

vent ra l

i n fer i or

b orde r

of

t he

o c u lomotor

nucleus ; longitudinal

t he

infer ior

re c tus

nucleus

li es

toward

t he

d ors a l

sup er ior

fasciculus

26

b order,

The

w it h

nucleus

c aud a l

t he

of

nucleus

t he

t wo-t hirds

subnuclei

are

of

found

for

sup er i or

t he

in

t he

in fer i or

re c tus

o c u lomotor

t he

r i g ht

and

li es

oblique

in

t he

nucl eus .

lef t

b et we en.

me d i a l

E a ch

of

o c u lomotor

and

t hes e

nuclei.

Fig.

the

13.8

Sagittal

oculomotor,

section

trochlear,

through

and

the

brainstem

abducens

nuclei.

showing

CHAPTER

214

13

Cranial

Nerve

Innervation

of

Ocular

Structures

on

the

ner ve.

Superior

posterior

rectus

Levator

Inferior

Medial

e

slightly

aspect

ner ve

cerebral

inferior

of

passes

the

arteries

to

the

midbrain

between

as

it

the

runs

posterior

as

for ward,

circle

rectus

the

of

Willis

uncus

(Fig.

and

13.10).

then

e

pierces

ner ve

the

roof

travels

of

the

it

runs

within

the

two

dural

layers

Oculomotor

nerve

nuclei.

A,

Lateral

view.

The

cells

are

mainly

dorsal

to

the

B,

Superior

view

of

of

the

inferomedial

cavernous

to

sinus

of

the

lateral

wall

the

oculomotor

ner ve

While in the cavern-

sinus,

the

oculomotor

ner ve

sends

small

sensor y

branches

somatic

(likely nuclei.

ar ter y

Eding-

ous

preganlionic

and

to,

26

above the trochlear ner ve (see Fig. 13.7).

13.9

and

lateral

rectus

where

er–Westphal

o culomotor

cerebellar

communicating

B

Fig.

the

superior

30

oblique

Inferior

A

anterior

Edinger-Westphal

proprioceptive)

to

the

ophthalmic

ner ve

and

receives

nucleus.

sympathetic

bers

from

the

plexus

around

the

internal

carotid

31,32

arter y.

superior

nucleus

ment.

rectus

nucleus;

might

e

have

centrally

thus

bilateral

placed

damage

to

superior

caudal

the

right

rectus

nucleus

oculomotor

muscle

provides

The o c u lomotor ner ve exit s t he c aver nous sinus and enters

involve-

t he

inner vation

2

orbit

to

3

t hroug h

mm

t he

p oster ior

sup e r ior

to

t he

orbit a l

sup er ior

f issure.

or bit a l

Approx imately

f issure,

t he

ne r ve

26

for

both

e

in

13.9).

plies

muscles.

div ides

Edinger-Westphal

located

Fig.

levator

the

In

rostral

some

nucleus,

portion

animals,

parasympathetic

of

the

an

the

autonomic

oculomotor

Edinger-Westphal

inner vation

to

the

ciliar y

nucleus,

nucleus

nucleus

muscle

is

are

sup-

and

eit her

w it hin

r uns

sup er ior

iris

sup er ior

lo c ate d

branch

(see

into

t he

me di a l ly

re c tus

pierce

and

on

t he

in fer ior

branche s ;

o c u l omotor

ab ove

its

mus cle

t he

i nfer ior

or

p ass

b ot h

foramen .

opt ic

ner ve

sur fac e.

around

div isions

The

and

sup e r i or

ente rs

Ad dit iona l

it s

b order

to

t he

f ib ers

i nner-

33 , 34

sphincter.

an

area

In

just

humans

dorsal

to

these

the

parasympathetic

Edinger

Westphal

bers

originate

nucleus

called

in

vate

the

t he

e

le vator

inferior

(Fig .

13.11).

branch

of

the

oculomotor

ner ve

runs

below

the

26–29

area

of

Edinger-Westphal

preganglionic

cells.

optic

the

Oculomotor

Fibers

from

fascicular

Nerve

each

part

of

Pathway

of

the

the

of

that

the

decussating

bers

and

the

peduncles.

medial

and

divides

rectus

on

into

its

three

lateral

branches.

surface,

and

One

one

branch

enters

enters

the

infe-

rior rectus on its upper surface (see Fig. 13.11). e third branch

individual

ner ve

ner ve

the

nuclei

passes

join,

near

superior

the

forming

red

cerebellar

the

gives

nucleus,

root

peduncle,

o

parasympathetic

extending

lateral

border

to

of

the

bers

ciliar y

the

that

form

ganglion;

inferior

rectus,

the

then

parasympathetic

it

crossing

runs

it

along

and

the

cur ving

29

cerebral

ese

bers

emerge

just

medial

upward

to

enter

the

inferior

oblique

muscle

on

35

to

the

cerebral

peduncles

within

the

interpeduncular

fossa

face

near

its

midpoint.

Levator

palpebrae

superioris

Superior

Medial

Superior

Inferior

rectus

rectus

branch

branch

Superior

Internal

orbital

carotid

fissure

artery

Posterior

Posterior

communicating

Cranial

cerebral Superior

nerve

artery

III

artery cerebellar

artery

To

sphincter

muscle

of

iris

To

ciliary

body

muscle

Inferior

Inferior

Ciliary

oblique

rectus

ganglion

Fig.

13.10

Lateral

view

showing

the

Cavernous

Basiliar

sinus

artery

cranial

nerve

III

Petrous

bone

pathway.

temporal

the

orbital

sur-

CHAPTER

Levator

Superior

muscle

oblique

13

Cranial

Nerve

Innervation

of

Ocular

215

Structures

muscle

thetic

function

to

the

iris

sphincter

and

ciliary

muscle.

Additional

signs

may

Trochlea Superior

rectus

muscle

be

superior

Trochlear

Superior

if

red

fissure

a

nucleus

cerebellar Optic

the

cerebral

cerebellar

peduncles,

nerve

orbital

present

peduncle,

peduncle

contralateral

will

cause

peduncle

are

red

nucleus,

involved.

hemiparesis

contralateral

If

the

will

tremor.

or

be

decussating

injury

involves

present.

Ataxia

will

bers

the

of

Involvement

occur

with

the

cerebral

a

of

the

superior

lesion.

nerve

Medial

Intracranial

Involvement

rectus Oculomotor

The

oculomotor

nerve

lies

near

several

blood

vessels

in

its

intracranial

path

muscle nerve

and

frequently

is

affected

by

an

aneurysm

of

the

posterior

communicating

Common 37

tendinous Lateral

artery.

An aneurysm of the superior cerebellar artery or the posterior cerebral

rectus

artery

ring

could

also

impinge

on

the

nerve,

damaging

bers.

muscle

Inferior

rectus

Damage

to

this

portion

of

the

nerve

results

in

ipsilateral

ptosis

because

of

muscle Abducens

nerve

levator

Inferior Inferior

orbital

oblique

muscle

fissure

is

positioned

lateral

Fig.

13.11

The

orbital

apex

with

the

globe

removed

muscle

paralysis

out

rectus

(Fig.

because

muscles

of

(Fig.

13.12A).

the

In

primary

unopposed

13.12B).

position,

action

Because

of

the

the

the

ipsilateral

superior

superior

eye

oblique

oblique

and

muscle

is

showing unaffected,

the

eye

also

should

be

positioned

down,

but

clinically

this

is

not

the relationship between the cranial nerves, the rectus muscles, 38

always

the

superior

orbital

ssure,

and

the

common

tendinous

move

the

CLINICAL

Injury

to

COMMENT: Cranial

sensory

cranial

nerve

bers

Nerve

results

Damage

the

innervated

area.

Injury

to

a

cranial

in

anesthesia,

motor

up

nerve

a

loss

causes

of

or

pupil

sions

of

(paresis)

or

a

total

loss

(paralysis)

of

muscle

function.

either

Paresis

will

the

a

eye

cannot

be

Because

dilated,

oculomotor

of

adduct

paralysis

and,

and

nerve

of

in

the

the

iris

abducted

accommodation

are

sphincter

position,

will

not

and

occur.

ciliary

cannot

muscle,

Incomplete

le-

possible.

the

oculomotor

or

nerve

exits

the

midbrain,

the

parasympathetic

bers

are

partial located

loss

The

down.

sensation As

in

evident.

ring.

supercially

along

the

nerve.

Because

of

this,

a

third

nerve

palsy

paralysis caused by a compressive lesion will generally damage these parasympathetic

of

an

extraocular

In

congenital

muscle

can

result

in

diplopia

if

the

involvement

is

acquired. bers

involvement,

diplopia

usually

is

not

a

complaint

because

resulting

striction. brain

has

Nerve

cular

learned

bers

can

diseases

to

be

damaged

(e.g.,

space-occupying

disregard

the

by

double

a

hypertension,

lesions

(e.g.,

image,

resulting

compromised

blood

atherosclerosis,

aneurysms,

or

in

caused

diabetes

or

a

xed,

Alternatively,

dilated

the

pupil,

supercial

in

addition

location

of

to

the

extraocular

by

mellitus)

tumors)

that

vas-

or

by

exert

means

they

spared

in

are

closest

ischemic

extraocular

sphincter

to

the

lesions.

muscles

and

are

ciliary

surrounding

This

is

paralyzed

muscle)

are

called

and

the

spared.

vasa

nervorum

external

intrinsic

It

responses

presenting

nears

A

number

of

and

symptoms.

clinical

signs

and

symptoms

accompany

damage

to

the

the

typically

orbit,

that

innervate

the

extraocular

muscles.

Muscle

paresis

or

be

evident

in

testing

ocular

motility

(as

described

in Ch.

11).

In

muscle

impairment,

a

patient

often

attempts

to

carrying

the

head

in

a

compensatory

position.

If

a

minimize

horizontal

lateral

the

muscles

accounts

for

the

the

head

will

be

turned

to

the

right

or

left.

With

a

deviation

vertical

head

is

raised

or

lowered,

and

if

a

torsional

deviation

occurs

of

toward

the

within

into

39–41

As

the

iris

pupillary

center

of

the

nerve

the

nerve.

cavernous

sinus

and

contains

maxillary

the

nerves.

oculomotor

The

nerve

abducens

as

nerve

well

is

the

cavernous

sinus,

and

sympathetic

bers

to

the

pupil

and

me-

eyelid

the

internal

the

head

cavernous

sinus

carotid

can

artery

affect

all

of

within

the

the

cavernous

extraocular

sinus.

muscles

A

lesion

resulting

in

in

total

is The

pupil

and

accommodation

may

also

be

affected.

Anes-

shoulder.

be

COMMENT: Oculomotor

of

the

present

facial

in

areas

addition

to

served

the

by

the

impaired

ophthalmic

ocular

and

maxillary

nerves

may

motility.

Damage Orbital

Nuclear

move

the

the

is

thesia

CLINICAL

normal

ophthalmoplegia.

bers

to

Involvement

the

ophthalmic,

ophthalmoplegia.

tilted

(those

deviation, the

the

Sinus

wall

trochlear,

surround

present,

parasympathetic

36

often

since

diplopia dial

by

diabetic

are

acquired as

extraocular

the

with

so

paralysis The

will

re-

bers

motor Cavernous

nerves

seen

and

ophthalmoplegia

26

pressure on the nerve bers. The location of the involvement will inuence the

signs

muscle

parasympathetic

suppression.

supply

hemorrhages,

in

the

Involvement

Involvement Both

divisions

of

the

oculomotor

nerve

are

located

within

the

muscle

cone,

A lesion in the midbrain can affect the entire oculomotor nucleus or selectively together

with

the

abducens

and

nasociliary

nerves.

A

retrobulbar

tumor

or

36

affect only some subnuclei; however, such selective damage is unusual.

If the inammation

lesion

affects

the

entirety

of

one

oculomotor

nucleus,

the

extraocular

involving

these

nerves

would

leave

only

the

superior

oblique

muscles muscle functional. In primary position, the eye would be positioned downward

involved

are

the

ipsilateral

medial

rectus,

inferior

rectus,

and

inferior

oblique, and outward slightly and would be fairly immobile. Corneal sensitivity could be

both

levator

tation

down

muscles,

would

and

out

contralateral

of

the

show

pupil

when

eye

and

and

both

bilateral

in

ptosis.

primary

would

inability

be

to

superior

The

position

unable

to

rectus

muscles.

ipsilateral

and

only

elevate

accommodate

in

may

eye

able

to

The

would

abduct

abduction.

also

be

clinical

be

presendecreased

because

ally

cause

and

intort.

Ipsilateral

Once

eral

the

present.

Aberrant

After

eye,

portion

tus,

and

the

within

inferior

the

nerve

exits

dysfunction

midbrain

rectus,

inferior

is

the

nucleus,

unilateral.

would

result

oblique,

in

A

all

its

lesion

bers

involving

ipsilateral

superior

rectus,

supply

loss

of

levator,

the

the

the

and

nasociliary

ipsilat-

fascicular

medial

vision

nerve

impairment

rec-

parasympa-

Regeneration

injury,

the

misdirected,

occur

Involvement

oculomotor

would

involvement.

because

of

optic

An

orbital

nerve

lesion

gener-

damage.

The

dilation

be

Fascicular

of

positioned

with

sponses.

Fibers

eliciting

the

going

causing

the

of

gaze

to

unusual

or

the

adduction.

muscle

with

Oculomotor

repair

clinical

inferior

medial

miosis

the

attempt

an

to

sphincter

innervating

sphincter,

may

downward

Fibers

innervate

body

Some

or

Nerve

and

cases

may

pupillary

may

adduction

nerve,

presentation.

oblique

causing

rectus

a

send

some

Lid

can

sprout

involve

branches

constriction

sprouts

convergence.

attempts

elevation

that

on

may

might

pupil

that

re-

also

elevation.

innervate

the

CHAPTER

216

13

Cranial

Nerve

Innervation

of

Ocular

A

Structures

B

Fig.

13.12

image)

Trochlear

Nerve:

Cranial

and

in

Cranial

nerve

secondar y

Nerve

III

palsy.

A,

gazes. The

Ptosis.

direction

B, The

of

position

attempted

only

IV

of

gaze

one

the

is

eye

in

primar y

indicated

muscle,

the

by

most

gaze

the

(central

arrows.

slender

of

the

extraocular

muscles.

As the trochlear ner ve emerges from the dorsal midbrain immee

trochlear

ner ve

inner vates

the

superior

oblique

muscle.

diately

around

Trochlear

below

the

the

trochlear

nucleus

is

located

in

the

midbrain,

at

the

level

at

the

it

decussates

upper

border

and

of

cur ves

the

inferior

colliculus,

anterior

to

the

cerebral

aqueduct,

paralleling

the

superior

cerebellar

and

pons,

posterior

of cerebral

the

colliculus,

peduncle

Nucleus approximately

e

inferior

cerebral

arteries.

It

passes

between

these

two

vessels

and

runs

dorsal for ward

lateral

to

the

oculomotor

ner ve

(Fig.

13.13).

to the medial longitudinal fasciculus, and below the oculomotor e

trochlear

ner ve

enters

the

wall

of

the

cavernous

sinus

16

nucleus (see Fig. 13.8).

e bers travel dorsally and decussate; and lies between the oculomotor ner ve and the ophthalmic divi-

thus

the

trochlear

nucleus

inner vates

the

contralateral

superior sion

oblique

the

to

Trochlear

Of

the

leaves

the

of

the

trigeminal

ner ve

(see

Fig.

13.7).

While

in

the

sinus,

muscle.

Nerve

cranial

the

cranial

Pathway

ner ves,

dorsal

the

aspect

ner ves,

and

the

the

ner ve

CNS.

attachment

It

is

is

is

the

the

ver y

only

most

one

that

slender

delicate.

e

of

ssure

muscle

cone

frontal

ner ve

and

small

ner ve

ophthalmic

orbital

trochlear

of

its

trochlear

superior

sends

ner ve.

above

(see

to

the

rectus

It

the

Fig.

sensor y

enters

bers

the

common

13.11).

medial

muscles

e

side

and

(likely

orbit

through

tendinous

trochlear

of

the

enters

of

the

ner ve

probably

reects

the

fact

that

it

superior

supplies

oblique

muscle.

Levator

palpebrae

superioris

Superior

Medial

Superior

Superior

Internal

oblique

rectus

rectus

orbital

carotid

fissure

artery

Cavernous

Cranial

nerve

(trochlear

Basiliar

artery

sinus

Inferior

IV

nerve)

Posterior

Superior

cerebral

cerebellar

Inferior

artery

artery

colliculus

Petrous

bone

Inferior

oblique

rectus

Fig.

13.13

Lateral

view

showing

the

cranial

nerve

IV

pathway.

temporal

superior

outside

runs

above

orbital

16,42

diameter

the

ring,

ner ve

orbit

the

proprioceptive)

with

the

the

the

levator

surface

of

the

CHAPTER

Fig.

13.14

downgaze

Right

when

CLINICAL

When

the

the

eye

adducted

site

the

position

to

muscle.

superior

ward

and

For

turned

to

in

palsy.

eye

a

muscle

primary

(Fig.

In

addition,

lateral

example,

The

for

to

must

a

is

head

is

a

limitation

trochlear

unable

may

putting

head

will

Nerve

be

put

superior

move

tilted

eye

in

of

a

eye

oblique

in

the

the

the

oppo-

inferior

left,

positioned

down,

are

13.15).

usually

Under

the

age

congenital,

of

and

10

and

years,

between

tilted

palsies

21

Ocular

217

Structures

head

tilts

head

to

A

toward

the

left

and

40

involving

years

of

the

age

the

diagnosis

head

left

of

with

a

right

toward

and

down.

incomitant

the

superior

left

(From

ocular

oblique

shoulder

Eskridge

deviations.

J

and

JB.

dysfunc-

turns

the

Evaluation

and

Am

Optom

Assoc.

1989;60[5]:378.)

po-

will

be

Nucleus

shoulder

trochlear

the

patient

the

down-

abducted

the

13.15

tion

e (Fig.

of

where

turned

an

palsy,

in

position

commonly

the

damage,

down

toward

extortion

the

is

to

nerve

Abducens the

Innervation

in

Fig.

by

unopposed

the

that

There

Cranial

adducted.

Damage

and

avoid

right

is

affected

the

work,

position

with

is

gaze

13.14).

compensate

oblique

in

sition.

oblique

elevated

shoulder

oblique

nerve

involved

COMMENT: Trochlear

superior

is

fourth

the

13

usual

abducens

nucleus

is

located

near

the

inferior

dorsal

mid-

nerve

cause

line

of

the

Fig.

13.8).

pons

beside

the

oor

of

the

fourth

ventricle

(see

43–45

is

trauma;

otherwise

the

palsy

may

be

idiopathic.

muscle,

Nucleus

Damage

to

Involvement

the

trochlear

that

nucleus

will

affect

the

contralateral

superior

Because

of

the

proximity

of

the

oculomotor

nucleus,

a

the

abducens

communicate

lesion

nucleus

for

both

cranial

nerve

bers

nucleus

via

the

that

control

contains

medial

the

lateral

internuclear

longitudinal

rectus

neurons

fasciculus

the

contralateral

medial

rectus

muscle

with

in

complex.

us,

stimulating

the

right

the

abducens

nuclei.

nucleus

le Intracranial

to

could

oculomotor affect

addition

oblique

the

muscle.

In

will

medial

cause

rectus;

contraction

both

eyes

of

the

will

right

turn

lateral

toward

rectus

the

and

right.

the

is

is

Involvement

the pathway for conjugate horizontal eye movements. is pathFor

the

tor

nerve

nerve

most

and

affects

elevated

(see

part,

Fig.

in

the

trochlear

is

susceptible

the

ipsilateral

primary

gaze

to

nerve

the

same

superior

and

follows

unable

the

injuries.

oblique

to

same

Damage

muscle,

move

path

down

as

the

to

the

causing

in

the

the

oculomo-

trochlear

eye

adducted

to

be

position

way

receives

centers,

the

cerebellum,

Abducens

lesion

nerve.

A

in

Sinus

the

lateral

cavernous

described

Orbital

wall

sinus

of

the

lesion

cavernous

could

also

sinus

affect

could

the

affect

the

oculomotor,

trochlear

ophthalmic,

in

the

Oculomotor

Damage

Clinical

Comment

earlier.

adjacent

the

the

central

pontine

vestibular

ner vous

reticular

system

formation,

nuclei.

Pathway

rectus

the

muscle.

the

corticospinal

leave

the

e

medulla

nucleus,

bers

tract

they

exit

oblongata.

in

In

for

part

of

inner vate

the

its

groove

long,

their

only

path.

the

between

tortuous,

Once

ipsilateral

the

pons

intracranial

Involvement

trochlear

nerve

lies

above

the

muscle

cone

near

the

frontal

nerve,

affecting

both

nerves

could

impair

the

superior

oblique

muscle,

the

of

the

in

the

scalp

adducted

innervated

position.

by

the

Decreased

branches

of

sensitivity

the

frontal

of

the

nerve

areas

might

skull

and

ner ve

up

runs

along

along

the

the

occipital

posterior

slope

bone

of

the

at

the

petrous

limiting

portion depression

abducens

and

base

and

Nerve

to

bers

course,

skin

higher

Fibers from the nucleus pass anteriorly through the pons and lie

and

injury

and

from

paramedial

Involvement

maxillary, abducens, and sympathetic nerves, causing the clinical presentation

The

the

13.14).

Cavernous

A

information

including

of

observed.

of

the

temporal

bone.

It

then

makes

a

sharp

bend

over

the

also

the

petrous

ridge

the

cavernous

of

the

temporal

bone

(Fig.

13.16)

and

enters

be

travels

under

sheath

is

sinus.

the

tightly

At

the

petrous

petrosphenoidal

adherent

to

the

apex,

the

ligament

ligament

abducens

where

and

the

the

ner ve

abducens

dural

tissue

46

around

Abducens

e

Nerve:

abducens

ner ve

Cranial

Nerve

inner vates

the

VI

lateral

near

rectus

muscle.

the

the

bone.

lateral

Sympathetic

wall

Within

of

the

branches

the

cavernous

internal

leave

the

carotid

sinus,

arter y

internal

the

ner ve

(see Fig.

carotid

lies

13.7).

plexus

and

CHAPTER

218

13

Cranial

Nerve

Innervation

of

Ocular

Structures

Levator

palpebrae

Superior

Lateral

Superior

oblique

rectus

rectus

superioris

Internal

Superior

orbital

fissure

Cavernous

carotid

sinus

artery

Cranial

nerve

Inferior

Inferior

oblique

rectus

Fig.

travel

with

ner ve

carries

the

abducens

ner ve

for

a

13.16

short

Lateral

time.

view

e

showing

the

cranial

autonomic

bers,

as

well

as

are

possibly

proprioceptive,

to

the

the

trigeminal

through

the

ner ve.

superior

e

orbital

abducens

ssure

ophthalmic

ner ve

within

enters

the

Medulla

pathway.

Involvement

bers leaving

the

abducens

nucleus,

damage

to

the

nerve

bers

will

result

in

an

division ipsilateral

of

Pons

abducens

sensor y

After

that

temporal

bone

nerve VI

Intracranial

these

Petrous

VI

the

common

orbit

tendi-

fected.

lateral

The

rectus

angulation

palsy.

of

the

The

contralateral

abducens

nerve

medial

over

the

rectus

petrous

will

ridge

not

of

be

af-

temporal

bone and the tight connections at the petrosphenoidal ligament render it particu-

nous ring and inner vates the lateral rectus muscle on the medial

larly susceptible to head trauma or increased intracranial pressure, which causes

surface

the

(see

Fig.

13.11).

brainstem

to

be

displaced

posteriorly

or

inferiorly,

stretching

the

nerve

over

46

the bony prominence of the temporal bone.

the

nerve

basilar

CLINICAL

Damage

muscle.

COMMENT: Abducens

to

the

abducens

Because

of

the

nerve

carotid

to

fractures

arteries

can

of

affect

the

the

base

of

the

abducens

skull.

Aneurysms

of

the

nerve.

Damage

results

unopposed

susceptible

and

Close connections to the bone make

in

action

paralysis

by

the

of

the

medial

lateral

rectus

Cavernous

Sinus

The

nerve

Involvement

rectus

muscle,

abducens

is

located

near

the

internal

carotid

artery

within

the

cav-

this

sec-

an

ernous

sinus.

Often,

it

is

the

rst

nerve

affected

with

an

aneurysm

of

esotropia that is worse at distance is evident. The eye will be unable to abduct

tion of the vessel. A lateral rectus muscle palsy with a Horner syndrome on the (Fig. 13.17). The patient might try to compensate for the diplopia by turning the

same face

toward

the

paralyzed

sinus

Whereas

the

most

side,

suggesting

sympathetic

involvement,

is

indicative

of

a

cavernous

side.

common

cranial

neuropathy

in

children

under

18

years

is

lesion.

a

47

fourth

nerve

palsy,

the

most

common

acquired

isolated

extraocular

muscle

Orbital

Involvement

48–51

nerve paralysis in adults involves the sixth cranial nerve.

length

of

the

abducens

nerve

make

it

susceptible

to

The tortuosity and

compression

and

stretch-

The

abducens

two

divisions

nerve

of

is

the

located

within

oculomotor

the

nerve

muscle

and

the

cone.

It

accompanies

nasociliary

nerve

and

the

will

52

ing

injuries

and

may

explain

why

it

is

damaged

so

result

frequently.

ment

Nuclear

Because

the

clinical

presentation

described

in

the

Oculomotor

Clinical

Com-

Involvement

the

abducens

in

earlier.

abducens

nucleus

will

nucleus

cause

contains

an

internuclear

ipsilateral

gaze

neurons,

palsy

rather

damage

than

an

to

the

isolated

Superior

Orbital

Fissure

lateral rectus palsy. The patient will have a restriction when attempting to turn

both

cle

able

the

eyes

will

to

toward

not

be

converge

pons,

nucleus.

and

the

side

activated

the

the

Damage

of

in

eyes.

Both

fasciculus

here

the

this

can

of

lesion.

lateral

the

the

cause

contralateral

but

abducens

facial

a

The

gaze,

and

nucleus

gaze

the

palsy,

facial

arches

as

medial

patient

well

will

nuclei

around

as

rectus

mus-

generally

are

the

located

be

in

abducens

weakness

of

e

trochlear,

rior

ophthalmic

above

the

muscles,

including

the

forehead,

orbicularis,

and

lower

facial

vein,

muscle

oculomotor

and

are

cone.

ner ve,

lacrimal

located

e

the

in

ner ves,

the

superior

abducens

as

well

superior

and

inferior

ner ve,

and

as

the

orbital

supe-

ssure

divisions

the

of

nasocili-

the

ar y

facial

the

frontal,

ner ve

are

located

within

the

superior

muscles.

common

tendinous

ring

(see Fig.

10.18).

orbital

ssure

and

the

CHAPTER

Fig.

eye

Control

of

Eye

ments.

the

VI.

among

to

produce

areas

cranial

abduct

of

the

controlled

corticonuclear

cerebral

and

the

to

e

Right

unable

hemispheres

fasciculus

connects

nucleus,

nerve

III,

extends

the

and

right

tract

to

the

central

and

palsy. There

gaze

(left

IV ,

and

from

vestibular

trochlear

VI

nuclei

the

nuclei.

nucleus,

bers

is

image).

of

cranial

the

into

the

providing

a

is

move-

travel

nerves

superior

oculomotor

system

eye

that

e medial

midbrain

nucleus,

nervous

coordinated

contains

e tectobulbar tract connects

cranial

nerve VI

in

Movements

Communication

necessary

13.17

is

13

from

III,

IV ,

colliculus

to

longitudinal

spinal

nucleus,

cord

slight

Both

between

eye movement control and the vestibular apparatus (see Fig. 13.8).

e

facial

vates

and

Nerve:

t he

Cranial

ner ve

facial

has

two

mus cles,

parasympat hetic

s ens ations

f rom

parasympat hetic

g lands

of

c uss ed

in

t he

t he

Chapter

ro ots:

and

t he

b ers.

t he

large

smaller

motor

ro ot

s ens or y

t he

ro ot

cont ains

b ers

of

t he

s ecretomotor

supplying

car r y

b ers

lacr imal

inner-

s ens or y

to

g land

e

oculi

from

lar

formation

of

both

facial

facial

in

the

of

this

ipsilateral

Facial

e

the

facial

pons.

e

ner ve

upper

is

located

segment

in

nucleus,

the

ral

and

lower

of

the

and

the

e

unilateral

of

(right

lower

the

lesion

nucleus

entire

or

the

frontalis,

procerus,

corrugator

bone

and

temporal

bers

are

of

foramen,

the

dis-

reticu-

nucleus

o

as

whereas

will

spare

the

will

the

the

ramus,

the

the

lower

the

zygomatic,

en

and

and

zygomatic

and

corrugator,

orbicularis

the

is

are

e

Stylomastoid

foramen

Facial

nerve

Facial

nerve

pathway.

Motor

pathway

of

facial

ner ve

to

facial

muscles

of

orbit.

motor

over

branches

and

supplied

nerve

supply

muscles.

inner vated

54

acoustic

the

(Fig.

respectively.

foramen

in

lacrimal

travel

medial

nerve

the

tempo-

stylomastoid

orbicularis

e

muscle

enters

the

branches

Zygomatic

13.18

result

abducens

the

canal,

nucleus

Fig.

upper

brainstem

While

to

ner ve.

buccal

oculi

of

canal.

several

and

ner ve.

orbicularis

branches,

ner ve

route

auditor y

into

the

the

portion

through

divide

temporal

facial

petrosal

emerge

external

from

facial

bers

greater

and

superior

of

e

petrous

through

procerus,

the

the

around

ner ve

Temporal

Internal

lower

cortex.

ner ve

Pons

Facial

the

input

the

contralateral

facial

arch

facial

pons.

in

ner ve

below

branch

of

the

runs

temporal,

frontalis,

portions

of

nucleus,

the

parasympathetic

facial

pass

as

meatus

then

given

e

facial

border

mandibular

frontal

the

emerge

bone,

the

var ious

superciliaris,

supplies

receive

face.

53

supplies

segment

muscles

cortices,

only

cortex

the

the

by

right

image).

upper

motor

219

Structures

(center). The

gaze

le

to

Ocular

Pathway

auditor y

are

the

a

and

Damage

leave

Specically,

the

gaze

left

inner vated

paralysis

Nerve

bers

13.18).

of

of

muscles.

are

muscles.

in

muscles,

right

muscles

B ecause

gland

14

nucleus

primary

facial

e

Nucleus

motor

in

normally

remaining

t aste

tongue.

Innervation

orbicularis

the

Facial

move

internal

two-t hirds

supply

os e

VII

e

anter ior

ner ves

face.

Nerve

esotropia

eyes

at

Facial

Nerve

and

abducens

connection

Cranial

by

by

the

lateral

buccal

CHAPTER

220

13

Cranial

Nerve

Innervation

of

Ocular

Structures

19. CLINICAL

COMMENT: Corneal

Hampl

KF ,

following The

corneal

reex

results

in

bilateral

involuntary

eyelid

closure

in

response

stimulation.

This

reex

protects

the

cornea

from

foreign

substances.

cataract

SC,

Schneider

surger y

under

M,

etal.

local

Vasovagal

anesthesia.

heart

block

Ophthalmic

to

Surg. corneal

Marsch

Reex

1993;24(6):422.

The

20.

Doxanas

MT,

Anderson

RL.

Ner ves

of

the

orbit.

In:

Clinical

afferent, or sensory, bers of this reex pass through the long ciliary nerves to the

Orbital ophthalmic

division

of

the

trigeminal

nerve.

The

efferent

signals

are

sent

facial

nerve

to

the

orbicularis

muscle

causing

the

eyes

to

blink.

A

Baltimore:

Williams

&

Wilkins;

1984:131.

through

21. the

Anatomy.

lesion

Chong

JL,

Tan

SH.

Oculocardiac

reex

in

strabismus

surger y—a

anesthesia.

Singapore

of

study

of

Singapore

patients

under

general

either the trigeminal nerve or the facial nerve will diminish this response.

Med

22.

J.

1990;31(1):38.

Grover

VK,

during

anesthesia.

REFERENCES 23.

1.

Ehlers

the

2.

3.

N,

Eye.

Hjortdal

vol

Marfurt

10.

CF ,

Wirtschaer

JD.

and

Wirtschaer

can

4.

Müller

Müller

neal

6.

7.

LJ,

Pels

ner ves.

cranial

courses

Ophthalmic

Vrensen

E,

GF .

Invest

Vrensen

Invest

TF .

Jaeger

Row ;

Kanski

EA,

GF ,

etal.

Vis

associated

of

Sci.

corneal

JJ.

the

third,

Reeh

San

24.

Vis

MJ,

fourth,

Wobig

Francisco:

25.

JL,

Ameri-

organization

Sci.

of

Stoerin

an

H,

anatomic

to

26.

frontal

R,

supratrochlear

migraine

of

human

cor-

Feldon

ed.

Moriggl

3rd

B,

exploration

migraine

Pikula

ner ve:

headaches.

12.

SE,

Adler's

Nguyen

1997;38(5):985.

ed.

Ricketts

Burde

R,

Plast

RM.

ed.

etal.

of

bital

14.

Farber

Chew

surger y.

Beck

EA,

S,

RW ,

ed.

SJ,

the

V ,

for

Reconstr

In:

Duane

Philadelphia:

London:

e

Harper

Butter worth-

supraorbital

neuro-vascular

J

Plast

etal.

the

Surg.

oculomotor

the

Um

of

J

Eye.

GT,

the

G,

review

of

CH.

9th

ed.

29.

Joo

W ,

Clin

etal.

Sunderland

for

surgical

30.

Aesthet

of

the

17.

Stott

DG.

treatment

of

Eustis

AN.

imaging

AL.

(New

Surg.

32.

St

In:

Louis:

ner ve.

J

Hart

WM

Mosby ;

study

Jr,

33.

1992.

in

of

the

Craniofac

Surg.

etal.

Transection

access

and

of

visibility

inferior

in

reex

nitrous

narcotic

extrao c ular

mon ke y.

J

mus cles

Comp

in

Neurol.

HK,

Y ork:

Lee

infarction.

KJ,

Clin

etal.

Anat

In:

Harper

&

AC.

Bender

Row ;

Isolated

Arch

Neurol.

Microsurgical

(New

Y ork,

MB,

ed.

e

1964:173.

inferior

anatomy

N.Y .).

oblique

1990;47:235.

of

the

2017;30(1):

Eberhorn

monkey

PJ,

of

J

Sun

unitar y

Härtig

man

properties:

Comp

the

A,

and

W ,

Neurol.

etal.

by

reappraisal

Perioculomotor

their

of

the

cell

histochemical

Edinger-Westphal

2008;507(3):1317–1335.

Erichsen

JT.

perioculomotor

primate

W ,

dened

Dening

the

pupillar y

preganglionic

Edinger-Westphal

compo-

population

nucleus.

Prog

within

Brain

Res.

Vitošević

Z,

course

the

of

Eiswirth

Marinković

clinical

Esmer

AF ,

of

of

ner ve.

Clinical

anatomy

35.

War wick

R.

Orbit.

War wick

Anat

Comert

Orbital

7th

R,

A,

Sci

etal.

ner ve.

M,

bers:

Int.

e

Clin

etal.

Intramesencephalic

microanatomy

and

pos-

2013;88(2):70–82.

neurovascular

Anat

(New

Y ork,

relation-

N.Y .).

In:

Tasman

Sacks

Jaeger

Ophthalmolog y.

vol

and

ner ve:

an

patholog y.

36.

1.

illustrated

Clin

Williams

G,

38.

of

the

trochlear

ner ve.

39.

2015;28(7):857–864.

in

facial

surger y.

Br

J

Plastic

Surg.

40.

S,

inferior

Brazis

In:

Eugene

PL.

Gray's

Wol 's

Saunders;

Anatomy

of

the

Anatomy.

35th

ed.

Philadelphia:

Notaris

M,

Cavallo

and

LM,

etal.

endoscopic

e

study.

oculomotor

Neurosurgery.

Nakamura

oblique

imaging.

PW .

inner vation

of

the

extraocular

muscles.

Am

M,

ner ve

Surg

Radiol

Localization

Mayo

Margolin

E,

Clin

Freund

Tabuchi

with

of

Proc.

P .

T,

etal.

An

anatomic

high-resolution

Anat.

study

magnetic

Smith

DR.

correction.

Vagal

Am

J

responses

Ophthalmol.

to

adjustable

1992;

41.

RS.

Ocular

muscles.

Goldstein

JE,

reference

to

Gray

A

Ing

of

2013;35(5):377–383.

lesions

of

the

oculomotor

ner ve:

recent

1991;66(10):1029.

ird

ner ve

palsies:

review.

Int

Ophthalmol

2019;59(3):99–112.

Jampel

LG.

EB,

ment

J

reso-

torsion

Am

J

Cogan

the

DG.

pupil.

clinical

and

the

function

Ophthalmol.

Diabetic

Arch

guide

third

the

vertical

ophthalmoplegia

Ophthalmol.

to

of

extra-

1975;79:292.

ner ve

with

special

1960;64:592.

palsy.

Opt

J

Rev

Optom.

1994;1:86.

CC,

Eye

1976:275.

1983;95:520.

concepts.

ocular

anatomy

de

Peripheral

Tsutsumi

Clin.

Radiol.

ner ves.

Philadelphia:

microanatomical

J.

nance

W ,

ed.

1973:1001–1006.

Iaconetta

the

37.

trigeminal

N.Y .).

T,

oculomotor

Cetković

ner ve

signicance.

Sen

the

S,

oculomotor

2010;66:593–601.

34.

or-

1994.

e

bradycardia

strabismus

114(3):307.

May

ner ve:

2014;25(2):557–562.

Microsurgical

Y ork,

Reex

HS,

sutures

in

nent

and

1989;42(5):595.

18.

AK,

ships

31.

2014;133(5):

Anatomical

IRP ,

improved

Trigeminal

Lippincott;

Rhoton

Anat

t he

Mamourian

stem

ner ve.

functional

sible

2013;68(2):203–213.

16.

Horn

a

region

bundle

Reconstr

Anatomy

system.

infraorbital

Foundations

Hegde

its

of

t he

and

1998;29(3):207(Abstract).

organization.

New

LN,

brain

Rha

Ophthalmol.

Craniofac

Duane's

Bathla

HF ,

contents

Smith

Philadelphia:

15.

Lasers.

Oculocardiac

block

2011;24(5):583–589.

Berchtold

e

of

pathway

ssure

System.

Johnson

HK,

nucleus.

2016;27(4):1094–1097.

orbital

Park

and

2nd

28.

infections.

headache.

implications

Physiolog y

DC,

of

Oculomotor

from

Saunders;

intraosseous

13.

R.

O,

groups

723e–724e.

11.

nucleus

etal.

21–31.

27.

2017;70(9):1171–1180.

Pauzenberger

Castro

paresis

hu-

1996;37(4):476.

Pharmacolog y.

viral

War wick

oculomotor

Ophthalmolog y.

Ophthalmolog y.

Berchtold

regard

Surg

Repres ent at ion

o c ulomotor

N,

peribulbar

2008;171:97–106.

Clinical

V ,

R.

Shobana

using

Ophthalmic

Oculomotor

1989:544.

with

War wick

t he

1982.

1994:111.

Surg.

Biolog y

human

Architecture

Ocular

Heinemann;

with

the

Ultrastructural

Clinical

Clinical

of

In:

Ophthalmol

SD.

eds.

e

1981:234.

Ophthalmol

Uveitis

of

Anatomy.

Butter worth-Heinemann;

Schlaegel

Jaanus

ed.

N,

surger y

1953;98:449.

ner ves.

Boston:

revisited:

10.

E,

J,

2010;90(4):478–492.

Ophthalmolog y ;

ner ves.

Fischbarg

Anatomy

JD,

&

9.

Pels

etal.

peripheral

eds.

of

S,

Res.

e

In:

Bartlett

TD,

8.

LJ,

corneal

Eye

cornea.

2006:83–111.

Deek

seventh

JD,

Academy

man

5.

J,

Exp

sixth,

e

Elsevier ;

Cox

inner vation.

h,

J.

Bhardwaj

retinal

in

Leavitt

JA,

ischemic

2000;32(2):90.

Y ounge

BR.

oculomotor

Incidence

ner ve

of

palsies.

pupillar y

Ann

involve-

Ophthalmol.

CHAPTER

42.

Zhang

motor

43.

44.

Y ,

46.

Burger

LJ,

ner ve.

Y oung

Sutla

and

palsies.

J

Am

Icke

Holmes

sixth

Smith

JL.

anatomy

of

the

ocular

Analysis

Mayo

Maxow

Arda

N.

of

ML,

49.

Acquired

lesions

of

the

Clin

Avilla

Proc.

CW .

ner ve

palsies:

51.

1977;52:11.

of

CN

and

Mutyala

palsies:

a

S,

Maus

Elder

palsy :

Rep.

C,

Hainline

update

on

C,

surgical

evaluation

2016;16(8):69.

Rush

and

e

sixth

JA,

Y ounge

BR.

Ophthalmol.

Tin

of

the

intracranial

perspective.

52.

PA,

Umansky

with

Turk

diagnostic

ner ve

dilemma

palsy.

221

Structures

Curr

of

Opin

neuro-imaging

Ophthalmol.

Paralysis

of

cranial

ner ves

III,

IV ,

and

VI.

1981;99:76.

MacEwen

J,

CJ,

trochlear,

Nathan

special

etal.

Pediatric

study.

third,

Am

J

fourth,

and

53.

De

Craig

and

H.

reference

Bonnecaze

muscle

Ophthalmol.

lation

SL,

MT.

isolated

Ocular

EA,

etal.

abducens

Acquired

ner ves.

Eye.

palsy

of

the

1996;

e

to

lateral

the

wall

ner ves

of

the

related

cavernous

to

it.

J

sinus:

Neurosurg.

1982;56:228.

TL.

population-based

Galetta

Bhatti

of

10:377.

study

1999;127(4):388–392.

48.

Innervation

oculomotor,

IV

2001;51:99.

interest

SL,

acute

Arch

diagnosis,

Epidemiolog y

Nerve

2009;20:423–426.

fourth

50.

trochlear

Chi

in

2010;32(7):623–628.

Microanatomical

clinical

Cranial

2010;20(4):449–456.

JM,

ner ve

Microsurgical

Anat.

1970;93:567.

Orthoptics.

C,

ner ve:

Neurosurg.

NH,

F .

etal.

treatment.

CA,

E,

EZ,

Radiol

Brain.

Gunderson

Ozer

Liu

Surg

Kalvin

BR,

abducens

47.

H,

cranial

etiolog y,

45.

Liu

ner ves.

13

etal.

Isolated

diagnosis.

abducens

Curr

Neurol

Vergez

and

a

S,

Chaput

comparative

anatomical

dissection.

B,

etal.

study

Clin

Variability

based

Anat

on

(New

in

facial-

electrostimu-

Y ork,

N.Y .).

2019;32(2):169–175.

ner ve

Neurosci

G,

inner vation:

54.

Hwang

K.

Surgical

rejuvenation

anatomy

surger y.

J

of

the

Craniofac

facial

Surg.

ner ve

relating

to

facial

2014;25(4):1476–1481.

14

Autonomic

e

autonomic

glands,

tem,

and

which

Inner vation

ner vous

the

heart

when

system

and

inner vates

consists

stimulated

of:

prepares

(1)

the

of

smooth

the

Ocular

muscles,

sympathetic

body

to

face

an

sys-

carotid

glionic

emer-

Structures

arter y.

Here,

preganglionic

bers

synapse

with

postgan-

neurons.

Postganglionic

bers

these

two

systems

inner vated

by

the

and

both

autonomic

muscle,

tival

by

smooth

blood

is

state.

particularly

systems.

ner vous

muscles

vessels,

and

Balance

e

the

the

are

in

those

structures

the

eyelids,

lacrimal

maintained

evident

ocular

system

of

is

iris

between

structures

inner vated

muscles,

choroidal

and

ciliar y

network

pathways

Most

to

of

division

the

of

orbit.

sympathetic

thoracic

spinal

and

leave

the

pathway

spinal

pathway

segments

originates

cord.

originates

lumbar

Sympathetic

in

bers

around

superior

destined

for

the

internal

orbital

struc-

target

the

structures.

trigeminal

in

ner ve

the

and

bers

ner ve

orbit,

then

travel

from

these

travel

with

the

the

sympathetic

with

ophthalmic

cavernous

the

sinus

bers

long

into

follow

ciliar y

the

ner ves

to

PATHWAY

upper

cord.

originates

sympathetic

sympathetic

Once

inner vate

e

the

the

nasociliar y

AUTONOMIC

ne

plexus

tures leaves the plexus in the cavernous sinus and takes multiple

conjunc-

gland.

of

carotid

area

carotid arter y, and enter the skull through the carotid canal. e

resting

the

orbital

restores

body’s

form

the

cer vical

the

ganglion,

to

gency ; and (2) the parasympathetic system, which maintains and

in

the

(T1

inner vation

T1

the

in

segments

through

Parasympathetic

for

T3.

midbrain,

lateral

horn

through

ocular

e

pons,

L2)

the

the

structures

parasympathetic

medulla,

inner vation

of

of

of

and

ocular

Other

the

iris

bers

dilator

from

and

the

the

ciliar y

internal

muscle

carotid

(see Fig.

plexus

follow

14.2).

the

naso-

ciliary nerve and then branch to the ciliary ganglion as the sympa-

thetic

root.

ese

synapsing.

ey

bers

enter

pass

the

through

globe

as

the

ciliary

the

short

ganglion

ciliary

without

nerves

to

sacral

innervate the choroidal blood vessels. Alternately, the sympathetic

structures

root to the ciliary ganglion may emanate directly from the internal

1 2

originates

in

the

midbrain

and

pons.

carotid plexus.

e autonomic eerent pathway consists of two neurons. e

cell

body

of

the

rst

ner ve,

the

preganglionic

neuron,

is

located

an

A population of intrinsic choroidal neurons forms

interconnected

vasculature

and

plexus

that

makes

nonvascular

contact

choroidal

with

smooth

the

choroidal

muscle.

ese

3 4

in the brainstem or spinal cord, whereas the cell body of the sec-

neurons

ond

ner ve

A

e

preganglionic

is

in

a

ganglion

ber,

outside

which

the

central

generally

is

ner vous

system.

myelinated,

termi-

may

receive

sympathetic

nerve

adrenergic

network

input

from

accompanies

sympathetic

the

bers.

ophthalmic

artery

and its branches could also have a role in the control of blood ow

5

nates

in

an

autonomic

postganglionic

ganglion

glia

are

and

which

inner vates

usually

sympathetic

ber,

ganglion,

located

ganglia

usually

the

target

near

are

where

the

located

is

a

synapse

nonmyelinated,

structure.

spinal

near

occurs.

the

exits

Sympathetic

column,

target

e

whereas

the

to

ocular

structure.

e

pathway

to

the

conjunctival

vasculature

may be through either the long or the short ciliary nerves.

gan-

para-

structures.

Still

nerve

other

and

bers

travel

from

with

it

the

into

carotid

the

plexus

orbit

to

join

the

oculomotor

innervate

the

smooth

muscle of the upper eyelid. ese bers follow the same path as the

Ocular structures supplied by the sympathetic system are the

superior division of the oculomotor nerve as it supplies the levator

6

iris

dilator,

ciliar y

muscle,

smooth

muscle

of

the

eyelids,

lacri-

muscle

(see

Fig.

14.2).

An

alternate

route

to

Müller

muscle

from

5

mal gland, and choroidal and conjunctival blood vessels. Ocular

structures

sphincter,

Fig.

14.1

supplied

ciliar y

provides

pathways

to

by

the

parasympathetic

muscle,

a

orbital

ow

lacrimal

chart

of

gland,

the

system

and

common

are

blood

the

iris

vessels.

autonomic

the infratrochlear or lacrimal nerve has been suggested.

ner ve

structures.

Sympathetic

pupillar y

Pathway

to

vessels

Ocular

Structures

and

activates

thereby

the

increasing

iris

dilator,

retinal

causing

illumination.

It also causes vasoconstriction of the choroidal and conjunctival

and

smooth

Sympathetic

stimulation

dilation

ner ves

widening

muscle

exhibit

of

a

of

the

the

palpebral

eyelids.

small

In

ssure

some

inhibitor y

by

people

eect

on

stimulating

the

the

the

sympathetic

ciliar y

muscle

7–10

Sympathetic

a

pathway

bers

that

are

controlled

terminates

in

the

by

the

hypothalamus

cer vical

spinal

cord.

through

Fibers

aer

of

sustained

accommodation.

Postganglionic bers to the majority of sweat glands of the face

the preganglionic neurons that inner vate ocular structures leave

split

the

external carotid artery. Sudomotor bers to the medial part of the

spinal

ventral

root

adjacent

then

rior

cord

to

and

the

ascend

in

in

cer vical

one

of

enter

the

vertebrae

the

the

rst

thoracic

sympathetic

(Fig.

14.2).

sympathetic

ganglion,

three

located

chain

near

chain

ese

to

the

a

ner ves

ganglia

via

located

preganglionic

synapse

second

in

and

the

the

bers

supe-

third

cer-

from

forehead

follow

the

may

the

remainder

of

accompany

supraorbital

the

the

sympathetic

internal

branch

of

the

bers

carotid

frontal

and

artery.

nerve

follow

ese

to

the

the

bers

medial

forehead. Relatively few sympathetic bers are found in the maxil-

lary and mandibular branches of the trigeminal nerve, accounting

11

vical

222

vertebrae,

just

anterior

to

the

bifurcation

of

the

common

for

a

lack

of

facial

sweating

in

areas

other

than

on

the

forehead.

CHAPTER

Parasympathetic

Pathway

to

Ocular

14

Structures

Autonomic

however,

in

Innervation

humans

the

of

Ocular

223

Structures

Edinger-Westphal

nucleus

is

thought

3,12,13

e

the

preganglionic

intrinsic

ocular

parasympathetic

in

muscles

accessor y

Edinger-Westphal

nucleus

neuron

contains

nucleus.

the

is

parasympathetic

located

in

third-ner ve

In

animals,

parasympathetic

the

midbrain

nucleus,

the

pathway

also

to

to connect to other brain regions.

In humans, the pregangli-

near

the

onic neurons are located dorsal to the Edinger-Westphal nucleus

called

the

and

Edinger-Westphal

preganglionic

neurons;

are

called

the

Edinger-Westphal

preganglionic

bers

tor

follow

ner ve

and

leave

the

with

the

inferior

preganglionic

motor

bers

division

of

of

that

cells.

the

e

oculomo-

ner ve

into

the

Preganglionic T1-T3 neuron

Preganglionic

Ventral

of

fiber

root

spinal

cord

Ganglion Superior

cervical

ganglion

Postganglionic Internal

carotid

artery

plexus

fiber

Ophthalmic

Oculomotor

nerve

nerve

Deep

petrosal

nerve

Nasociliary Vidian

nerve

nerve

Long

ciliary

Sympathetic

Superior

root

division

nerve

Pterygopalatine

ganglion

(no

Ciliary

synapse)

ganglion Maxillary

(no

nerve

synapse)

Short

ciliary Zygomatic

nerve

nerves

Communicating

branch

Lacrimal

nerve

Lacrimal

gland

Structure Choroidal Iris

and

dilator

Muller

muscle

conjunctival blood blood

vessels

vessels

Action Widening

of

Vasoconstriction

Mydriasis

Vasoconstriction palpebral

fissure

A

Fig.

A,

14.1

Flow

Sympathetic

chart

of

the

inner vation.

autonomic

B,

nervous

Parasympathetic

system

innervation

inner vation

shown

on

of

the

ocular

structures.

following

page.

g

14.1

continued

on

next

page

CHAPTER

224

14

Autonomic

Innervation

of

Ocular

Structures

Preganglionic Edinger

Lacrimal

Westphal

nucleus

neuron preganglionic

in

cells

pons

Preganglionic

fiber

Oculomotor

nerve

Facial

Greater Inferior

nerve

petrosal

division nerve

Parasympathetic Vidian

nerve

root

Ganglion Pterygopalatine (synapse

Ciliary

occurs)

ganglion ganglion

Postganglionic

fiber

Short

ciliary

nerves

Maxillary

nerve

Zygomatic

nerve

Communicating

branch

Lacrimal

nerve

Lacrimal

gland

Structure

Iris

sphincter

Ciliary

muscle

Action

Miosis

Accommodation

Lacrimation

B

Fig.

orbit.

e

parasympathetic

bers

14.1

leave

the

B,

Parasympathetic

inferior

division

and

inner vation

enter

to

the

enter the ciliar y ganglion as the parasympathetic root (Fig. 14.3).

inner vate

e ciliar y ganglion is a small, somewhat at structure, 2 mm

inner vate

ocular

globe,

the

and

iris

the

structures.

travel

sphincter

ciliar y

to

the

and

muscle;

anterior

ciliar y

only

segment

muscle.

of

Most

approximately

the

of

3%

eye

the

to

bers

supply

the

17–19

long

the

and

1

lateral

mm

high,

rectus

located

muscle

within

and

the

the

optic

muscle

ner ve,

cone

between

iris

approximately

sphincter.

Parasympathetic

inner vation

to

the

uveal

blood

vessels

is

2,14–16

1 cm anterior to the optic canal and common tendinous ring.

believed

ree

glion

to

emanate

directly

from

the

pter ygopalatine

gan-

3

the

roots

are

located

parasympathetic

at

the

root,

posterior

mentioned

edge

of

the

previously ;

ganglion:

the

sensor y

through

a

Parasympathetic

network

of

activation

ne

ner ves,

causes

the

rami

vasodilation

oculares.

either

because

3

root,

the

which

carries

nasociliar y

sensor y

ner ve;

and

bers

from

the

globe

and

joins

the sympathetic root, which

with

supplies

of

nitric

oxide

increases

or

choroidal

cholinergic

blood

ow

neurotransmitter

and

might

raise

release.

intraocular

is

pres-

20,21

the

blood

synapse

vessels

in

the

of

the

ciliar y

globe.

Only

ganglion.

the

e

parasympathetic

sensor y

and

bers

sympathetic

sure.

In addition, trigeminal inner vation within the uvea may

result

in

vasodilation

because

of

noxious

stimuli

or

temperature

3

bers

pass

e

ciliar y

thetic

through

short

ciliar y

ganglion,

bers.

without

e

ner ves,

carr y

synapsing

located

sensor y,

postganglionic

at

(see Fig.

the

14.3).

anterior

sympathetic,

and

parasympathetic

increases.

edge

of

the

parasympa-

bers,

which

Parasympathetic

thus

decreasing

stimulation

retinal

causes

illumination

and

pupillar y

reducing

constriction,

chromatic

and

spherical aberrations. It also causes contraction of the ciliar y mus-

17

are

myelinated,

exit

the

ganglion

in

the

short

ciliar y

ner ves,

cle,

enabling

the

eye

to

focus

on

near

objects

in

accommodation.

CHAPTER

14

Autonomic

Innervation

Superior

division

oculomotor

of

Ocular

225

Structures

of

ner ve

Shor t

ciliar y

ner ve

Ciliar y

Sympathetic

to

the

ciliar y

ganglion

root

ganglion

Superior

tarsal

Nasociliary muscle

of

nerve Müller

Ophthalmic

nerve Iris

dilator

muscle

Trigeminal

ganglion

Lacrimal

gland

Maxillary

nerve

Sympathetic

carotid

Lacrimal

plexus

Long

Inter nal

carotid

ar ter y

ciliar y

ner ve

ner ve

Vidian

ner ve

Zygomatic

ner ve

Pter ygopalatine

ganglion Deep

Cer vical

spinal

petrosal

cord

ner ve

Superior

cer vical

ganglion

Ventral

Fig.

root

14.2

lacrimal

Sympathetic

innervation

to

the

iris

dilator,

Müller

Autonomic CLINICAL

The

iris

COMMENT: Iris

contains

sympathetic

muscles

system

the

by

both

sphincter,

autonomic

and

the

systems.

sympathetic

The

para-

system

in-

nervates the dilator. The parasympathetic and sympathetic nerves are in some

state

pupil

of

balance

changes

in

the

normal,

constantly

and

healthy,

awake

rhythmically,

individual,

reecting

this

and

the

balance.

size

This

of

the

e

eerent

complex

pupillary

unrest

is

called

During

sleep,

the

decreases

and

the

and

to

the

Lacrimal

Gland

hippus

and

is

independent

of

changes

pupils

are

small

because

the

sympathetic

parasympathetic

system

autonomic

Fibers

pathway

to

controlling

the

the

lacrimal

gland

parasympathetic

follows

a

innerva-

nerve VII designated as the superior salivatory nucleus. ese pre-

physi-

in

bers

exit

the

pons

with

the

motor

bers

of

the

facial

illu-

enter

the

internal

auditory

canal,

and

pass

through

the

system

geniculate activity

vessels,

tion originate in the pons in an area within the nucleus for cranial

nerve, mination.

Innervation

route.

ganglionic

ologic

blood

Equilibrium

innervated

innervates

muscle,

gland.

ganglion

of

the

facial

nerve

without

synapsing.

ey

predominates.

leave the ganglion as the greater petrosal ner ve. Aer exiting the

CHAPTER

226

14

Autonomic

Innervation

of

Ocular

Structures

Superior

division Inferior Ciliary division ganglion

Lacrimal

ner ve

Oculomotor

nerve

Greater

petrosal

Maxillary

nerve

Ophthalmic

nerve

nerve

Edinger-Westphal

preganglionic

Iris

cells

sphincter

muscle

Lacrimal

Internal

gland

auditory

canal Facial

nerve

Lacrimal

nucleus

Zygomatic

ner ve

Vidian

nerve

Pter ygopalatine

Deep

ganglion

petrosal

Sympathetic

ner ve

plexus

Stylomastoid

foramen Facial

nerve

Parasympathetic

root

Shor t Parasympathetic ciliar y

Sensor y

Sympathetic ner ves

root

Sensor y

Sympathetic

root

Fig.

14.3

mal

glion;

petrous

is

portion

joined

by

the

of

Parasympathetic

gland.

only

the

deep

Inset

shows

parasympathetic

temporal

petrosal

bone

ner ve,

innervation

the

the

sensor y,

bers

synapse.

greater

composed

to

petrosal

of

the

iris

sympathetic,

Each

nerve

sympathetic

sphincter

and

short

ciliar y

of

and

ciliary

parasympathetic

the

then

ner ve

carries

trigeminal

the

muscles

bers

all

in

three

nerve,

and

and

the

types

pass

zygomaticotemporal

the

lacri-

ciliar y

of

into

branch,

gan-

bers.

the

zygomatic

which

nerve

innervates

the

and

lac-

22

postganglionic

sal

and

the

bers

deep

from

petrosal

the

carotid

nerves

plexus.

together

e

form

greater

the

petro-

vidian

ner ve

rimal

is

gland.

sent

from

In

the

an

alternate

pathway,

zygomaticotemporal

a

communicating

nerve

to

the

branch

lacrimal

nerve

16,22

(nerve

e

of

the

pterygoid

vidian

nerve

canal)

enters

(see Figs.

the

14.2 and

pterygopalatine

14.3).

before

ganglion,

where

e

its

entering

parasympathetic

the parasympathetic bers synapse. e pterygopalatine ganglion

of

(also

sympathetic

tion

called

of

the

the

sphenopalatine

pterygopalatine

ganglion)

fossa

(see

Fig.

lies

in

13.6).

the

It

is

upper

a

por-

parasym-

the

the

secretomotor

indirectly

bers

cause

lacrimal

bers

type

that

and

innervate

decreased

gland

(see

Figs.

innervate

thus

the

cause

blood

production

the

14.2

lacrimal

increased

vessels

of

and

of

lacrimal

14.3).

gland

secretion.

the

gland

gland

are

e

and

secretion

5

pathetic

ganglion

because

it

contains

parasympathetic

cell

bodies

and synapses. Sympathetic bers pass through without synapsing.

e

autonomic

bers

(all

of

which

are

now

postganglionic)

by

restricting

increased

blood

the

pterygopalatine

ganglion,

join

with

the

maxillary

branch

Parasympathetic

Sympathetic

bers

stimulation

from

the

causes

zygomatic

nerve also branch into the lower eyelid to innervate Müller muscle

23

leave

ow.

lacrimation.

of the lower eyelid.

CHAPTER

Trigeminal

Opthalmic

Nasociliary

ganglion

nerve

nerve

14

Autonomic

Long

and

Innervation

of

Ocular

227

Structures

short Cornea

ciliary

nerves

Pain

Edinger

Westphal Oculomotor

Ciliary

nerve

ganglion

Short

ciliary

Sphincter

preganglionic nerves

(miosis)

cells

Facial

nerve Facial

Zygomatic

Orbicularis

nerve

(blink)

nerve

nucleus

Greater Lacrimal

Facial

nucleus

nerve

Vidian

Pterygopalatine

Maxillary

Zygomatic

Lacrimal

nerve

ganglion

nerve

nerve

nerve

Lacrimal

gland

petrosal (lacrimation)

nerve

Fig.

14.4

miosis,

Pathways

blinking,

involved

and

when

pain

from

the

cornea

results

parasympathetic

CLINICAL

COMMENT: Corneal

touch

initiates

the

three-part

corneal

reex:

lacrimation,

miosis,

and

secrete

blink

(Fig.

14.4).

The

pain

sensation

elicited

by

the

touch

travels

trigeminal

ganglion

and

then

into

actions

of

system

both

the

pons

as

the

trigeminal

nerve.

acetylcholine

preganglionic

(Fig.

14.5).

and

Fibers

postganglionic

that

are

called

cholinergic,

and

bers

that

release

release

ace-

norepi-

to

nephrine the

reex

a

tylcholine protective

the

Reex

bers

Corneal

in

lacrimation.

are

called

adrenergic.

Com-

e

neurotransmitter

binds

to

eector

sites

on

the

muscle

munication from the trigeminal nucleus to the Edinger-Westphal preganglionic

and initiates a contraction. e neurotransmitter then is released cells

causes

activation

of

the

sphincter

muscle.

Communication

to

the

facial

from the muscle and is either inactivated or taken back up by the nerve

the

nucleus

blink,

and

pathway

other

to

activates

water,

the

lacrimal

of

the

lacrimation.

as

motor

communication

branches

creased

the

well

as

gland

the

nerve

example,

in

the

to

lacrimal

stimulates

trigeminal

For

pain

to

pathway

the

orbicularis

nucleus

and

increased

activates

plucking

a

nose

a

the

muscle,

parasympathetic

lacrimation.

reex,

hair

will

causing

Irritation

of

precipitating

cause

the

in-

eyes

to

naris.

ner ve

ending,

muscle

potential

ergic

and

PHARMACOLOGICAL

INTRINSIC

RESPONSES

and

preventing

should

release

neuromuscular

inactivates

junction

and

thus

contraction

of

continual

occur

additional

junction,

acetylcholine.

norepinephrine

is

muscle

only

with

transmitter.

spasm.

At

acetylcholinesterase

At

the

taken

adrenergic

back

up

by

Further

another

the

action

cholin-

hydrolyzes

neuromuscular

the

ner ve

ending

recycled.

OF

MUSCLES

Pharmacological agents can alter autonomic responses. Topical

Superior CNS Effector cervical

ophthalmic

drugs,

which

readily

pass

through

the

cornea,

cell

ganglion

can Adrenergic

be

used

to

Aer

drug

a

activate

brief

types

specic

that

drugs

or

inhibit

discussion

aect

that

the

iris

induce

the

of

intrinsic

ocular

neurotransmitters,

musculature,

mydriasis

or

this

muscles.

section

miosis,

division

receptors,

as

well

and

presents

as

Acetylcholine

Norepinephrine

drugs

used in the dierential diagnosis of certain pupillar y abnormali-

ties.

e

reader

is

encouraged

to

review

a

text

on

pharmacolog y Ciliary

for

detailed

Effector

cell

CNS

information.

ganglion

Cholinergic

Neurotransmitters

When

an

action

division

potential

reaches

the

terminal

end

of

an

axon,

Acetylcholine

a

neurotransmitter

ber

in

the

pathway

sympathetic

by

released

or

pathway,

preganglionic

released

is

ber

the

is

the

the

that

target

activates

structure,

the

neurotransmitter

acetylcholine,

postganglionic

ber

and

is

either

the

the

eector.

released

In

by

the

the

neurotransmitter

norepinephrine.

Acetylcholine

next

In

the

Fig.

14.5

action.

SD.

Autonomic

CNS,

Clinical

Heinemann;

Central

Ocular

1989.)

neurotransmitter s

ner vous

system.

Pharmacology,

ed

(From

2.

at

their

Bartlett

Boston:

sites

JD,

of

Jaanus

Butter worth-

CHAPTER

228

14

Autonomic

Innervation

of

Ocular

Structures

Receptors

e

response

of

the

cell

to

a

neurotransmitter

is

dependent

NE

NE

NE

NE

NE

Ep

NE

Ph

on Dilator

the

receptor

receptors,

type

rather

nicotinic

than

and

the

neurotransmitter.

muscarinic

receptors,

Cholinergic

respond

to

choA

linergic

neurotransmitters

receptors,

rine.

to

e

alpha

iris

iris

tion

and

muscle,

(eyelid

ocular

respond

muscarinic

e

of

alpha

Stimulation

Adrenergic

to

receptors

norepineph-

that

predominant

vasculature

stimulation

elevation).

acetylcholine).

receptors,

has

neurotransmitters.

dilator

Müller

beta

sphincter

cholinergic

the

and

(i.e.,

are

1

alpha

1

receptors

of

alpha

2

respond

receptors

receptors.

causes

on

On

contrac-

receptors

causes

24

relaxation

(ptosis).

Ep

Ph

B

Drugs:

A

drug

Agonists

that

and

replicates

Antagonists

the

action

of

a

neurotransmitter

is

called

an agonist. A direct-acting agonist is structurally similar to the

neurotransmitter

mitter

by

acting

rect-acting

a

ner ve

and

on

agonist

ber,

duplicates

the

causes

thereby

the

receptor

an

action

causing

action

sites

of

to

release

of

the

occur

of

a

the

neurotrans-

eector.

either

An

by

NE

NE

NE

NE

indi-

exciting

neurotransmitter,

or Hydroxy

by

preventing

the

recycling

or

reuptake

of

the

neurotransmitter, C

thus allowing it to continue its activity. Antagonists either block

the

receptor

thus

sites

preventing

or

block

action

of

the

the

release

of

the

neurotransmitter,

eector.

NE

Ophthalmic

Agonist

Agents

NE

NE

Epinephrine

and

agonists

that

traction

(Fig.

phenylephrine

bind

to

14.6).

sites

on

are

the

direct-acting

dilator

muscle,

Hydroxyamphetamine

and

adrenergic

causing

con-

cocaine

are NE

D indirect-acting

causes

thus

the

the

adrenergic

release

indirectly

reuptake

of

norepinephrine

initiating

of

agonists.

muscle

norepinephrine

Hydroxyamphetamine

from

the

contraction.

by

the

ner ve

ner ve

Cocaine

ending;

ending,

prevents

thus

nor-

NE

NE

epinephrine

remains

at

the

neuromuscular

junction

and

can NE

continue

to

activate

the

dilator.

Pilocarpine is a direct-acting cholinergic agonist that directly

stimulates the sites on the iris sphincter and ciliar y muscle, caus-

NE Cocaine

E ing

contraction

(Fig.

14.7).

Physostigmine

is

an

indirect-acting Fig.

cholinergic

agonist

that

inhibits

acetylcholinesterase.

14.6

Adrenergic

adrenergic

acetylcholine

is

not

broken

down

but

remains

in

the

the

sphincter

and

ciliar y

muscle

contraction

agonists.

A,

junction

Norepinephrine

(NE)

and

is

actions

released

at

of

the

junction, axon

and

neuromuscular

erefore

continues

in

terminal

and

binds

to

sites

on

the

iris

dilator

muscle,

causing

a contraction. B, Epinephrine (Ep) and phenylephrine (Ph) are direct-

spasm.

acting

iris

Ophthalmic

Atropine,

Antagonist

Agents

cyclopentolate,

antagonists

that

and

compete

(Hydroxy)

tropicamide

with

are

acetylcholine

cholinergic

by

blocking

ner ve

and

ciliar y

muscle

sites,

thereby

inhibiting

miosis

from

the

(Fig.

is

an

effector

ending.

that

E,

release

site,

bind

to

contraction.

indirect-acting

causing

adrenergic

of

an

same

agonist

is

sites

on

the

Hydroxyamphetamine

norepinephrine.

norepinephrine

Cocaine,

those

C,

that

D,

taken

indirect-acting

acts

Once

back

up

adrenergic

on

the

released

by

the

agonist,

reuptake

of

norepinephrine,

allowing

it

to

remain

in

the

14.8). neuromuscular

CLINICAL

causing

and

prevents

accommodation

agonists

muscle,

ber,

ner ve

sphincter

adrenergic

dilator

COMMENT: Drug-Induced

Mydriasis

junction

and

rebind

to

the

effector

ACCOMMODATION-CONVERGENCE

site.

REACTION

For maximum pupillary dilation to occur, the dilator muscle should be activated

(NEAR-POINT

REACTION)

and the sphincter muscle should be inhibited. This is achieved by the combina-

tion

of

a

direct-acting

adrenergic

agonist

and

a

cholinergic

antagonist.

2.5%

e accommodation-convergence reaction is not a true reex but phenylephrine

and

1%

tropicamide

are

often

both

administered

for

a

dilated

rather fundus

a

synkinesis

or

an

association

of

three

occurrences:

conver-

examination.

gence,

accommodation,

and

miosis.

As

an

object

is

brought

near

CHAPTER

ACh

14

Autonomic

Innervation

ACh

of

Ocular

229

Structures

ACh

Cyclo

Sphincter

ACh

Sphincter

ACh

Trop

ACh

A

Cyclo

Trop

Fig.

14.8

Actions

neuromuscular

camide ACh

(T rop)

of

cholinergic

junction.

are

antagonists

Cyclopentolate

cholinergic

(Cyclo)

antagonists

that

at

the

and

block

tropi-

receptor

Pi

ACh

sites

of

the

iris

from

binding

sphincter

and

muscle,

causing

preventing

muscle

acetylcholine

(ACh)

contraction.

Pi

Pi

convergence

occur

without

accommodation.

If

a

base-in

prism

is

placed in front of each eye, pupillary constriction and accommodaPi

B tion occur without convergence. Shining a bright light in the eye will

cause pupil constriction without accommodation or convergence.

e aerent pathway for this reaction follows the visual pathway

to

to

the

striate

the

nucleus

e

cortex.

frontal

and

eye

the

eerent

From

elds,

the

which

striate

Edinger-W estphal

pathway,

via

cortex,

communicate

the

information

with

preganglionic

oculomotor

the

cells

nerve,

is

sent

oculomotor

(Fig.

14.9).

innervates

the

medial rectus muscle, and the parasympathetic pathway innervates

ACh

the ciliary muscle and iris sphincter.

ACh

PUPILLARY

A

LIGHT

PATHWAY

AChe

Ch

An

understanding

of

the

pupillar y

light

pathway

can

be

an

C

important

tool

in

manifestations.

initiate

from

Shining

pupillar y

information

visual

diagnosing

a

clinical

bright

constriction.

are

called

bers,

light

e

pupillar y

which

carr y

problems

into

an

aerent

bers,

visual

with

eye

bers

to

pupillar y

normally

that

carr y

distinguish

will

this

them

information.

ACh

e

ACh

from

aerent

pupillary

intrinsically

from

rods

as

far

in

the

as

and

the

light

pathway

photosensitive

cones.

posterior

ese

optic

retinal

bers

tract,

is

mediated

ganglion

parallel

with

the

cells

the

by

visual

nasal

signals

with

input

pathway

bers

crossing

Physo ACh

of

e

the

14.7

Cholinergic

cholinergic

the

axon

cle,

causing

neuromuscular

agonists.

terminal

and

A,

binds

contraction.

B,

junction

Acetylcholine

to

sites

on

Pilocarpine

(ACh)

the

(Pi)

is

iris

a

and

is

actions

released

sphincter

at

mus-

direct-acting

optic

colliculus

olivar y

occurs,

tract

to

and

an

and

the

agonist

that

causing

binds

to

contraction.

those

C,

sites

Once

on

the

released

iris

from

site,

acetylcholine

which

is

prevents

broken

down

acetylcholine

by

from

Physostigmine

that

remain

in

the

posterior

bers

(Physo)

is

an

inhibits

active

in

neuromuscular

the

leave

known

superior

the

of

as

the

third

of

the

pretectal

colliculus.

pretectal

region

superior

Synapse

travel

preganglionic

cells

bilaterally,

to

the

distributing

to

both

sides.

Edinger-W estphal

e

bers

preganglionic

that

cells

cross

travel

in

to

the

the

oppo-

posterior

acet ylcholinesterase

rebinding

indirect-acting

acetylcholinesterase,

the

brachium

midbrain

near

that

the

25

equally

to

the

cholinergic

allowing

14.10).

site.

eerent

parasympathetic

pathway

from

the

Edinger-

ago-

W estphal nist

exit

effec-

e D,

the

located

commissure (Fig. (AChe),

of

within

sphincter

the

site tor

bers

cho-

about muscle,

travel

area

nucleus,

Edinger-W estphal

linergic

pupillary

AChe

D

Fig.

chiasm.

acetylcholine

preganglionic

cells

to

the

iris

sphincter

and

ciliary

to

muscle is described earlier under the Parasympathetic Pathway to

junction.

Ocular Structures section. As the third nerve leaves the midbrain,

to

the

to

move

keep

eyes

the

along

the

the

image

near

midline,

onto

object

in

each

the

medial

fovea;

focus;

and

the

the

rectus

ciliary

muscles

muscle

sphincter

contract

contracts

muscle

to

constricts

the pupillomotor bers generally lie supercially; but as the nerve

leaves

the

cavernous

bers

move

in

inferior

sinus

centrally

and

and

then

enters

into

the

an

orbit,

inferior

the

pupillomotor

position

to

travel

25

to decrease the size of the pupil, thereby improving depth of eld.

Each

of

these

actions

can

occur

without

the

others.

If

plus

the

While

the

division

of

the

oculomotor

parasympathetic

system

is

nerve.

activated,

an

inhibition

26

lenses

are

placed

in

front

of

each

eye,

pupillary

constriction

and

of

the

dilator

muscle

can

occur.

When

light

is

removed

from

CHAPTER

230

14

Autonomic

Innervation

of

Ocular

Structures

Medial

rectus

Short

ciliary

nerve

muscle

Ciliary

Optic

ganglion

nerve

Frontal

Optic

eye

fields

tract

Oculomotor

nerve

Edinger-Westphal

preganglionic

cells

Oculomotor

nucleus

rectus

(medial

subnucleus)

Lateral

geniculate

nucleus

Visual

optic

Striate

Fig.

14.9

visual

ate

eye

ing,

ited,

and

the

the

cortex

ring

to

the

ciliar y,

rate

and

from

the

response.

eye

eye

to

sphincter

and

bers

the

the

elds,

Dotted

visual

then

lines

cortex.

indicate

Solid

lines

oculomotor

of

cortex

the

visual

indicate

nucleus,

pathway

the

and

bers

pathway

from

there

from

to

carr ying

the

the

stri-

to

the

medial

stop

r-

retina likely pass through an accessor y optic system to the cer vi-

inhib-

cal spinal cord. ere is similar inhibition of the parasympathetic

muscles.

preganglionic

sympathetic

increases,

pupillary

frontal

Edinger-Westphal

preganglionic

their

near

information

rectus,

the

The

fibers

radiations

are

dilator

no

cells

longer

muscle

increases

inner vation

while

the

sympathetic

ner ves

cause

27

in

tone.

dilator

contrac-

27

e

bers

that

carr y

the

inhibition

message

from

the

tion.

ese

inhibitor y

bers

course

through

the

midbrain.

CHAPTER

14

Autonomic

Innervation

of

Ocular

Short

ciliary

nerve

Ciliary

Optic

Optic

ganglion

nerve

chiasm

Oculomotor

Optic

231

Structures

nerve

Cerebral

tract

aqueduct

Edinger-Westphal

preganglionic

Brachium

of

cells

the

Pretectal

olivary

nucleus

Posterior

Fig.

14.10

lines

The

indicate

pupillary

the

light

efferent

pathway.

commissure

Dotted

lines

indicate

Disruption CLINICAL

In

COMMENT: Pupillary

assessment

consensual

both

a

of

the

response

direct

pupillary

are

response

light

tested.

Light

pathway,

When

(constriction

of

a

both

the

light

direct

is

ipsilateral

response

directed

iris)

and

into

a

and

one

the

eye,

consensual

response (constriction of the contralateral iris) occur. The consensual response

occurs

retinal

because

bers

pretectal

of

cross

olivary

the

in

two

the

nucleus

crossings

chiasm,

cross

in

and

the

of

the

afferent

pathway

and

solid

in

the

Afferent

Pathway

Response

bright

the

the

pathway.

bers

in

approximately

posterior

the

half

pathway:

the

bers

the

from

nasal

A

disruption

consensual

in

the

aerent

responses.

For

pathway

example,

will

in

the

aect

both

presence

direct

of

a

and

disrup-

tion in the right aerent pathway, a light directed into the right eye

will

cause

a

poor

response

in

both

the

right

eye

and

the

le

eye,

although both responses would be normal if the light were directed

each

into

the

(i.e.,

all

le

eye.

If

the

damage

to

the

aerent

pathway

is

complete

commissure.

the

bers

from

one

eye

are

aected),

there

would

be

no

CHAPTER

232

direct

and

aected

the

no

eye.

consensual

More

abnormal

compared

relative

14

oen,

pupillary

with

aerent

the

Autonomic

response

only

responses

normal

pupillary

when

some

defect

light

bers

might

pupillary

Innervation

are

be

is

directed

damaged,

recognized

responses.

(RAPD)

is

of

into

such

only

us

applied.

Ocular

e

Structures

the

that

when

the

term

swinging-

ashlight test can be used to determine the presence of an RAPD.

Disruption can occur anywhere in the aerent pathway: retina,

optic

nerve,

posterior

to

chiasm,

the

optic

crossing

tract,

in

the

or

superior

chiasm

brachium.

might

not

be

Damage

evident

with

the swinging-ashlight test unless the damage aects a great numA

ber

of

bers

from

one

eye

compared

with

the

other

eye.

ere

are

more crossed (contralateral) bers in the optic tract than uncrossed

(ipsilateral) bers; therefore with a complete optic tract lesion, the

pupillary

constriction

will

be

greater

with

light

into

the

ipsilateral

eye than with light into the contralateral eye (i.e., you would get an

RAPD in the eye contralateral to the optic tract lesion).

CLINICAL

During

the

COMMENT: Swinging

swinging

ashlight

test,

the

Flashlight

patient

is

Test

asked

to

xate

on

a

distant

ob-

ject, and the practitioner swings a light from eye to eye, several times rhythmically,

taking

care

to

illuminate

each

pupil

for

an

equal

length

of

time,

about

2

or

3

sec-

B

onds. If both afferent pathways are normal, little or no change in pupil size will be

noted; the eye will not recover from the consensual response before it is subjected

to the direct light beam. The normal, symmetric response is characterized by equal

pupillary

constriction

in

both

eyes

when

the

light

is

presented

to

either

eye.

An

abnormal response is characterized by larger pupils when the light is directed into

the affected eye than when the light is directed into the normal eye ( Fig. 14.11).

As

is

the

intensity

presented

increase

to

of

a

occurs.

however,

the

the

light

normal

A

very

increases,

eye.

There

bright

luminance

light

level

is

stronger

a

can

should

constrictions

threshold,

be

be

used

however,

for

recorded

occur

detecting

because

a

when

beyond

subtle

measured

RAPD

might

be

reective

of

different

lighting

future

no

defects;

change

28

the

light

which

in

29

conditions.

C

Fig.

CLINICAL

The

to

most

the

COMMENT: Optic

common

optic

nerve

site

of

results

damage

in

a

is

Neuritis

causing

decreased

an

RAPD

signal

to

is

the

the

optic

ipsilateral

nerve.

Damage

pretectal

olivary

nucleus. Because the signal from the pretectal olivary nucleus goes to both Edinger-

Westphal preganglionic cells, neither eye constricts well to light ( Fig. 14.12). When

14.11

equal

cating

pupillar y

directed

is

when

would

not

seem

result

a

in

that

a

dense

cataract

an

contralateral

opacity

to

RAPD.

eye.

probably

In

Light

cataract

stimulate

fact,

a

dense

scattered

produces

an

would

the

cause

retina.

cataract

more

will

diffusely

enhanced

an

RAPD

However,

may

on

pupillary

because

media

cause

the

an

retina

response,

less

as

an

left

into

the

right

pupillar y

light

is

RAPD

RAPD

from

the

which

is

the

lens

of

the

Within

in

the

the

contralateral

the

might

pupils

eye

eye

left

enlarge

of

pupils

and

both

eye. This

is

response

each

a

eye,

are

as

constrict

(RAPD

both

in

B, There

indicative

left

with

the

defect.

pupils

pupillar y

light

the

when

severe

OS).

pupils

light

is

light

is

relative

C, The

growing

indi-

unequal

pupil-

larger

as

constricting

not

leaving

can

the

Nervous

a

involve

nucleus,

preganglionic

cause

injur y

to

the

the

cells.

pupillar y

bers

dorsal

the

or

in

the

right

indicative

eye

of

(RAPD

a

mild

OD).

eral

pupils

that

preganglionic

show

a

poor

cells

direct

generally

and

results

consensual

in

bilat-

response

light

but

a

is

brisk

said

constriction

carr ying

to

the

the

defect,

the

of

pretectal

olivar y

parasympathetic

to

as

the

bers

the

pretectal

show

to

a

near

light-near

target.

is

message

for

the

preganglionic

dissociation.

pupillar y

near

cells

reaction

from

a

Because

approach

more

ventral

the

the

loca-

System

Damage

tegmentum

between

defect

mani-

pretectal

from

the

other pretectal nucleus still supply both parasympathetic nuclei.

interrupts

into

is

a

eye.

Central

midbrain

bers

Edinger-Westphal

An

the

right

pupillar y

Edinger-Westphal

tion,

nucleus

in

the

directed

both

both

eye. This

unequal,

into

Edinger-Westphal

Disruption

lesion

and

A, The

will

in

bers

nucleus,

pupillar y

which

eye

defect

are

afferent

response

A

in

the

test.

shining

light

opacities

to

fested

afferent

responses

directed

when

COMMENT : Relative Afferent Pupillary Defect in Cataract

relative

penetrates

relative

responses

light

It

symmetric

into

directed

lar y

CLINICAL

no

afferent

light is directed into the nonaffected eye, both pupils constrict normally.

Swinging-ashlight

and

midbrain

nuclei

and

that

the

e

ent

they

not

pathway

path

will

do

is

from

viable,

constrict

retained

(Fig.

pass

near

14.13),

to

through

the

frontal

therefore

a

near

when

the

object.

response

and

the

eye

elds

sphincter

With

exceeds

the

aected

is

best

looks

of

intact

and

the

midbrain.

and

ciliar y

light-near

the

patient

area

the

eer-

muscle

dissociation,

direct-light

from

near

still

the

response

to

distant,

the pupils redilate briskly. A near response that exceeds the light

response

is

always

a

sign

of

a

pathological

pupil.

CHAPTER

14

Autonomic

Disruption

Damage

to

Innervation

in

the

the

of

Ocular

Efferent

eerent

233

Structures

Pathway

pathway

results

in

anisocoria,

a

dier-

ence in pupil size between the two eyes. If the dierence between

the pupils is greater in dim light, the smaller pupil is the defective

one

and

the

clinician

coria

and

With

benign

and

to

will

all

drugs,

it

it

may

be

is

pupil

may

a

in

bright

is

be

the

the

pupil

poorly

occurs

the

to

dark.

light

is

will

in

by

pupil.

react

the

Associated

caused

is

the

to

pupil

aniso-

pathway).

all

stimuli

reacts

Anisocoria

pupil

one.

of

well

dark.

generally

defect

benign

sympathetic

Horner

the

because

a

between

the

e

pathological

caused

tonic

dierentiate

(damage

redilates

in

defect.

larger

well

but

evident

pathetic

must

pupil

anisocoria,

redilate

stimuli

more

e

Horner

by

a

be

may

poorly.

caused

oculomotor

symptoms

is

parasym-

constricts

may

well

that

by

ner ve,

assist

in

or

the

diagnosis.

CLINICAL

COMMENT: Physiologic

Approximately

Fig.

14.12

Right

relative

afferent

pupillary

defect

in

a

right

optic

of

the

population

Anisocoria

have

physiologic

anisocoria

(also

patient called

with

20%

simple

or

benign

anisocoria),

which

is

usually

more

apparent

in

dim

neuritis. light

than

in

bright

light,

with

the

difference

between

pupils

usually

less

than

30

1

mm.

and

CLINICAL

COMMENT: Light-near

Dissociation

Sometimes

react

sents

an

well

to

the

all

asymmetric

If the light-near dissociation is associated with small, irregularly shaped pupils

innervation

it

nuclear

to

the

anisocoria

stimuli

balance

iris.

may

and

switch

dilate

between

Benign

sides,

equally

the

anisocoria

but

with

both

the

sympathetic

may

be

and

caused

pupils

lights

by

are

off.

It

round

repre-

parasympathetic

asymmetric

supra-

30

is

called

Argyll

Robertson

pupil.

This

is

classically

associated

with

neuro-

inhibition

of

the

Edinger-Westphal

preganglionic

cells.

syphilis but has been reported with other conditions, such as diabetes, multiple

sclerosis,

stroke,

dissociation,

syndrome.

the

Here,

pupillary

onic

cells.

and

Wernicke

associated

a

tumor

bers

with

may

crossing

Blindness

be

to

resulting

encephalopathy.

xed,

pressing

the

from

Another

middilated

on

the

contralateral

bilateral

pupils,

posterior

cause

is

of

midbrain,

Edinger-Westphal

afferent

light-near

dorsal

visual

midbrain

including

pregangli-

pathway

Disruption

A

lesion

regeneration

of

the

medial

rectus

bers

to

the

iris

of

sphincter

direct

tonic

pupil

(discussed

later)

can

also

result

in

light-near

the

Parasympathetic

oculomotor

ner ve

Pathway

and

consensual

will

pupillar y

cause

the

responses

eye

and

a

to

show

poor

near

muscle,

response. and

the

damage,

poor

aberrant

of

e

pupil

appears

large

on

clinical

presentation,

and

dissociation.

other

the

ocular

oculomotor

rectus,

medial

muscle,

and

motility

motor

tes,

structures

the

are

bers

are

are

or

ner ve

be

involved.

involve

inferior

spared

in

ischemic

as

to

the

for

the

lesions,

in

as

or

levator

the

from

ocular

oculo-

from

lesions

emerges

in

superior

related

bers

compressive

ner ve

Damage

oblique,

examined

parasympathetic

vulnerable

supercial

be

could

rectus,

should

e

oen

especially

generally

inferior

patient

impairment.

ner ve

but

nucleus

rectus,

the

will

diabe-

because

the

mid-

27

A

brain.

ird

highly

an

ner ve

suspicious

involvement

of

a

that

compressive

includes

a

intracranial

dilated

pupil

lesion,

such

is

as

aneur ysm.

Damage

could

be

pupil,

to

the

caused

which

is

ciliar y

by

local

ganglion

injur y

characterized

or

by

or

the

disease

poor

short

and

ciliar y

results

pupillar y

ner ves

in

light

a

tonic

response

B and

loss

occurs

pass

of

through

aected

tion

sual

14.13

responses

direct

eye.

Light-near

and

C,

when

consensual

Normal

near

dissociation.

light

is

shined

responses

response

A,

in

in

when

both

Poor

the

light

eyes.

direct

right

is

and

bers

short

pupil

ciliar y

muscle

directly

response

redilates

Decreased

aerent

a

ner ves

may

retained,

sluggishly

bers

and

exhibit

physiological

inner vating

is

corneal

sensor y

a

aer

it

ciliar y

the

phenomenon

is

are

constricting

and

to

a

e

dener va-

occurring

injured.

delayed

oen

cornea

ganglion.

cholinergic

muscle

but

sensitivity

from

e

slow,

near

near

and

target.

consen-

eye.

shined

the

sphincter

pupillar y

the Fig.

some

hypersensitivity,

when

C

accommodation.

because

in

B,

Poor

the

left

One

theor y

despite

of

the

as

damage

to

to

why

the

inner vation

to

a

slow

bers

the

near

pupillar y

postulates

ciliar y

that

muscle

is

response

because

much

the

occurs

density

greater

than

CHAPTER

234

the

density

of

14

inner vation

Autonomic

to

the

Innervation

sphincter,

some

of

ciliar y

Ocular

Structures

muscle CLINICAL

ner ve

bers

remain

intact.

With

near

stimulation,

these

COMMENT: Tonic

Pupil

bers In addition to a dilated pupil that does not respond to light but responds slowly

release

acetylcholine,

which

diuses

into

the

aqueous

humor to a near target (Fig. 14.14), tonic pupil has a number of other characteristics. If

31

and

causes

the

hypersensitive

sphincter

to

constrict.

Another a

theor y

suggests

that

if

not

all

of

the

bers

supplying

the

tonic

pupil

irregular

muscle

erate

are

damaged,

aberrantly

to

the

remaining

inner vate

the

ciliar y

muscle

sphincter.

us

bers

when

regen-

a

evident

accommodate

is

received,

the

pupil

also

constricts.

and

examined

(Fig.

segmental

with

the

biomicroscope,

constriction

affecting

the

only

a

pupil

border

section

of

the

will

iris

appear

may

In

the

differential

diagnosis

of

tonic

pupil,

a

very

mild,

direct-acting

choliner-

late 17

gic

stages

of

this

condition,

the

pupil

becomes

miotic

and

the

agonist

tive

becomes

facility

dicult

generally

17

tion

of

the

to

demonstrate,

recovers,

perhaps

but

as

a

the

can

be

used

because

the

sphincter

muscle

is

hypersensitive.

concentration

of

pilocarpine

(0.125%)

has

minimal

of

sphincter

but

ter.

one

With

greater

A

will

cause

drop

signicant

instilled

in

clinical

each

eye,

miosis

the

tonic

in

a

C

should

constriction

than

the

normal

pupil

(Fig.

14.16).

D

E

the

the

left

direct

does

eye.

light,

near

the

tonic

pupil.

B, The

Note

but

constrict

lasting

that

Left

right.

right

that

the

right

when

right

eye

and

eye

is

slight

responds

anisocoria

looking

response

normal

the

A, There

pupil

is

responds

at

a

takes

dilates

a

a

hypersensitive

pupil

B

14.14

on

A

normal

sphinc-

regenera-

30

than

effect

accommoda-

result

bers.

Fig.

32

near dilute

reaction

be

14.15).

signal In

to

is

ciliar y

near

long

anisocoria

well

greater

well

to

target.

time

quickly

in

light,

in

in

After

dim

but

bright

light

E,

to

when

to

light.

the

illumination,

there

redilate

when

looking

back

eye.

at

a

a

poor

left

D,

near

looking

to

a

C, The

left

looking

is

with

the

pupil

does

Although

target,

back

distance

left

consensual

to

a

not

slow,

the

larger

respond

the

pupil

distance

target.

pupil

response

left

has

in

to

eye

a

long-

target.

Note

show

a

much

CHAPTER

14

Autonomic

making

under

in

the

Innervation

pupil

normal

dim

light,

smaller

room

with

Ocular

than

light

the

of

normal.

conditions

abnormal

eye

235

Structures

Anisocoria

but

is

more

having

the

is

present

pronounced

smaller

pupil.

e pupil responds briskly to light but with slow and incomplete

dilation

in

the

CLINICAL

Clinical

Damage

which

Fig.

14.15

border

Segmental

associated

constriction

with

tonic

causing

an

irregular

ptosis,

pupil

ly

pupil.

to

the

sympathetic

Loss

of

of

whereas

such

(Fig.

COMMENT: Horner

Syndrome

Features

consists

cretion).

dark.

that

the

ptosis,

pathway

miosis,

innervation

loss

of

to

the

ssure

the

head

facial

smooth

innervation

palpebral

to

and

to

the

will

muscle

lower

appears

cause

anhidrosis

of

the

eyelid

narrow,

Horner

(absence

upper

causes

sweat

eyelid

it

simulating

syndrome,

of

to

se-

causes

rise

slight-

enophthalmos

14.17).

Damage

stem

can

occur

spinal

anywhere

cord,

along

preganglionic

the

sympathetic

pathway,

or

pathway

in

postganglionic

the

brain-

pathway.

In-

Causes of tonic pupil include orbital surgeries, trauma, or masses that damage

volvement the

ciliary

ganglion

or

systemic

conditions

that

affect

the

autonomic

as

diabetes.

If

no

cause

of

the

tonic

pupil

is

apparent,

the

the

central

neuron,

which

sends

its

ber

from

the

hypothala-

nerves,

mus such

of

syndrome

through

the

brainstem

to

a

synapse

with

the

preganglionic

neuron

in

stroke

or

of

the

dorsal

horn

of

the

cervical

spinal

cord

is

often

caused

by

a

Adie tonic pupil should be considered. The typical patient with Adie tonic pupil

multiple is

a

woman

diminished

lieved

20

to

40

tendon

that

similar

years

reexes.

of

age.

Some

Because

degenerative

of

90%

this

processes

of

these

systemic

are

patients

also

manifestation,

occurring

in

the

ciliary

it

sclerosis.

have

is

be-

The

ganglion

preganglionic

chest,

course

bers

over

the

leave

apex

the

dorsal

the

lung,

of

horn

and

of

the

loop

spinal

around

cord,

the

pass

into

subclavian

the

artery

33

and

in

the

dorsal

column

of

the

spinal

cord,

but

the

cause

is

unknown.

en route to the superior cervical ganglion (Fig. 14.18). These bers can be dam-

aged

The

CLINICAL

Recent

onset

induced

the

such

cause

is

a

the

dilator

a

xed,

of

an

dilated

Investigation

drugs

effect

(e.g.,

(e.g.,

or

red

1%

out”

the

farmers,

pilocarpine.

may

pupil

of

also

could

Some

cause

a

or

crop

agent,

be

Dilated

caused

individual’s

pharmacists

parasympatholytic

pilocarpine

“get

of

mydriasis.

handling

exert

COMMENT: Pharmacologically

the

dusters,

or

or

will

pupil

might

that

drops

due

to

that

to

drug-

could

If

the

age

promise

of

Sympathetic

along

interruption

in

the

Pathway

sympathetic

pathway

causes

enter

miosis.

syndrome

should

with

the

a

rest

Anhidrosis

addition

be

sixth

of

cause

in

to

is

treated

nerve

the

in

metastatic

the

skull

a

as

disease

through

classical

an

the

paresis

symptom

emergent

indicates

postganglionic

Horner

miosis

reduced

nerves

innervating

Müller

muscle

with

An

that

or

internal

a

neuron

of

internal

situation.

can

involve

a

and

is

no

counteracting

pull

against

the

sweating

the

bers

sweat

to

postganglionic

glands

follow

Horner

central

and

ipsilaterally.

the

of

the

face

external

syndrome

preganglionic

The

may

majority

separate

carotid

sphincter

14.16

and

pupil

is

Patient

with

unreactive

to

a

right

light.

constricted. There

B,

along

the

medial

travel

through

forehead.

Sympathetic

not

sweat

was

tonic

no

pupil.

change

the

artery

syndrome

lesion.

in

Dam-

nasociliary

Horner

of

or

syndrome

postganglionic

the

dilator

Therefore

experience

bers

to

the

supraorbital

nerve.

muscle,

Following

carotid

sinus

from

artery.

B

large

plexus

and

patients

anhidrosis

except

e

A

Fig.

chest.

Syndrome

ptosis,

34

there

the

carotid

Horner

cavernous

usual tone that the dilator muscle normally exerts is not present,

and

involving

to

the

In

the

surgery

long ciliary nerves.

will

in

or

bers

Horner

and

combination

0.125%

stimulation

Painful

dissection

muscle.

Disruption

injury

postganglionic

artery.

indicate

exterminators).

respond

thoracic

can be damaged by a fracture of the skull base or an injury to the internal carotid

accidental

chemicals

not

over-the-counter

dilated

by

profession

nurses)

pupil

Pupil

in

A,

Before

instillation

to

the

left

of

pilocarpine

0.125%

pupil.

instillation,

pilocarpine

in

the

both

right

eyes,

pupil

the

is

right

the

medial

forehead

CHAPTER

236

14

Autonomic

Innervation

of

Ocular

Structures

pathway.

acts

on

lesion

and

Topical

the

is

in

will

the

contain

will

If

damage

should

to

an

An

Fig.

14.17

Ptosis

and

miosis

in

the

right

eye

caused

Horner

syndrome.

pseudoenophthalmos.

There

Lack

of

is

also

sweating

present

(not

shown),

but

the

left

side

of

the

right

Iris

the

right

Heterochromia

Normal

sympathetic

tenance

normal

Fig.

than

of

iris

iris

in

melanocyte

is

the

is

to

to

48

postganglionic

norepinephrine.

of

the

be

stored

in

instillation

of

hours

Instillation

neurotransmitter,

autonomic

after

the

ganglion

the

adrenergic

or

nerve

of

and

the

ber

still

If

and

the

viable

hydroxyamphet-

will

occur.

postganglionic

endings,

test,

is

dilation

and

hydroxyamphetamine.

cocaine

agonist

norepinephrine.

ber,

therefore

The

dilation

no

instillation

may

take

up

hour.

drug

might

postganglionic

be

used

involvement,

in

1%

localizing

a

Horner

phenylephrine

can

syndrome

cause

lesion.

pupillary

because

the

face

is

the

dilator

muscle

is

hypersensitive

to

the

dila-

sympathomimetic

In

the

normal

pupil,

1%

phenylephrine

will

generally

cause

only

mini-

more

dilation.

With

a

preganglionic

lesion,

the

Horner

pupil

would

be

expected

to

only

to

occur.

dilate

minimally

although

validation

with

published

ndings

has

yet

Syndrome

develop,

rarely

with

the

of

face.

necessary

pigmentation.

fails

Heterochromia

of

Horner

innervation

pigmentation

14.17).

side

24

not

pathway,

release

side

mal

hyperemic

occur

the

indirect-acting

heterochromia

on

drug.

is

will

occur

alternative

tion

and

in

this

causing

by

With

congenital

will

of

release

is

norepinephrine

dilation

stores

cause

of

ber

preganglionic

amine

the

administration

postganglionic

seen

in

for

In

the

development

congenital

and

Horner

heterochromia

acquired

Horner

is

and

main-

syndrome,

present

syndrome

(see

but

may

27

develop

after

long-standing

Diagnosis

In

addition

curs

in

ologic

and

to

dim

the

off

Localization

clinical

illumination,

anisocoria.

being

because

parasympathetic

conditions.

The

of

presentation

and

this

normal

the

will

pupil

normal

inactivation

of

of

ptosis

dilates

miosis,

Horner

within

sympathetic

the

and

differentiate

5

activity

sphincter.

In

dilation

pupil

seconds

to

the

Horner

lag

from

of

the

dilator

lights

and

syndrome,

oc-

physi-

the

there

is

reduced sympathetic activity, and the pupil thus dilates only from inactivation

of the sphincter muscle. This dilation occurs more slowly, taking 10 to 20 sec-

30

onds

(Fig.

35

14.19).

Diagnostic

Dilation

drugs,

including

lag

does

topical

not

occur

cocaine

and

with

physiologic

apraclonidine,

anisocoria.

aid

in

the

diagPostganglionic

nosis

of

Horner

syndrome.

Hydroxyamphetamine

can

be

used

to

localize

the Preganglionic

causative

If

the

lesion,

sympathetic

ophthalmic

the

the

with

a

of

dilates

mal

2

because

vation

The

is

its

a

direct

but

resulting

of

in

1

as

as

to

an

installation

The

in

for

pupil.

It

2

weeks

36

hours.

(Fig.

location

0.5

to

of

a

the

in Fig.

of

14.20

one

dilation

in

30

Central

drop

adrenergic

pathway,

cocaine

alpha

does

is

weak

1.0%

2

to

of

a

has

little

2%

agonist

60

or

to

that

minutes.

norepinephrine

may

agonist.

afnity

cause

receptors.

upregulation

36

early

causes

adrenergic

have

hypersensitive

the

general,

shown

instillation

therefore,

acting

does

afnity

results

dilation

are

indirect-acting

anywhere

junction;

apraclonidine

of

intact,

an

norepinephrine,

receptors

eye,

is

which

no

is

10%

blocks

In

con-

lacking

effect,

and

in

the

poorly.

Apraclonidine

alpha

of

solution,

disruption

neuromuscular

pupil

effects

pathway

cocaine

reuptake

trast,

the

of

alpha

receptors

take

time

necessary,

but

for

no

for

predominantly

pupil

However,

1

the

to

1

change

on

the

In

a

nor-

slight

miosis

syndrome

dener-

the

or

dilator

muscle.

apraclonidine

causing

hypersensitivity

positive

activates

receptors.

Horner

receptors

respond

a

It

alpha

response

has

to

develop.

been

In

reported

spinal

cord

Reduced

disruption

appropriate

into

determine

whether

at

The

the

the

innervation

hypothalamus

preganglionic

thoracic

The

ptosis

also

occurs

following

apraclonidine

of

the

sympathetic

pathway

is

useful

in

ganglion

care.

Hydroxyamphetamine

1%

can

be

and

sinus

where

orbit.

(From

cavity

pathway

and

postganglionic

of

then

bers

the

and

eye.

travels

courses

up

to

leave

the

the

The

central

down

from

to

the

superior

superior

the

spinal

cer vical

cer vical

the

damage

is

in

the

preganglionic

or

follow

they

the

then

Maloney

internal

travel

WF ,

carotid

with

Y ounge

arter y

various

BR,

to

the

cranial

Moyer

NJ.

cavernous

ner ves

to

the

Evaluation

of

de-

causes

and

accuracy

of

pharmacologic

localization

in

Horner

administered

syndrome. to

Sympathetic

starts

cord.

ganglion.

the termining

14.18

pathway

37

14.21).

the

Fig.

Am

J

Ophthalmol.

postganglionic

from

the

Mayo

Foundation.)

1980;90:394.

W ith

permission

CHAPTER

14

Autonomic

Innervation

of

Ocular

237

Structures

A

B

A

C

B

D

E

Fig.

the

14.20

left

right

ria

eye

is

Horner

pupil

indicating

greater

syndrome.

larger

in

than

the

involvement

dim

A,

right

illumination.

of

Anisocoria

pupil.

in

Ptosis

Müller

bright

is

light

present

muscle. B, The

C, T opical

cocaine

5%

with

in

the

anisoco-

is

instilled

C in

each

eye.

interruption Fig.

14.19

Right

Horner

syndrome

demonstrating

a

A,

Anisocoria

in

bright

illumination.

B,

Anisocoria

5

dilates.

removal

of

the

light.

C,

Anisocoria

15

seconds

after

the

light.

Note

that

the

anisocoria

is

much

greater

at

5

at

15

seconds.

This

indicates

that

the

right

pupil

is

t aking

time

to

dilate,

a

dilation

Fig.

14.21

sympathetic

the

right

D,

Hydroxyamphetamine

pathway. The

1%

is

Right

in

Horner

both

syndrome.

eyes.

indicating

normal

instilled

pupils

dilate

E,

indicating

interruption

Hydroxyamphetamine

of

1%

the

is

right

instilled

is

no

response

in

the

right

eye,

but

the

indicates

interruption

of

the

right

in

left

both

pu-

eyes.

preganglionic

A,

left

in

both

pupil

postganglionic

lag .

apraclonidine

pupil

eyes.

dilates.

a This

long

of

seconds There

than

right

response

removal pathway.

of

the

no

seconds Both

after

of

is

dilation pil

lag.

There

Before

instillation

of

eyedrops. B,

After

instillation

of

1%

pathway.

CHAPTER

238

14

Autonomic

Innervation

of

Ocular

Structures

19.

REFERENCES

Kozicz

T ,

nucleus:

1.

Natori

Y ,

orbital

2.

ssure.

Izci

Y ,

and

its

Min

3.

Gonul

Invasive

McDougal

5.

Microsurgical

e

Neurosurg.

DH,

of

the

superior

in

anatomy

orbital

of

traumas:

20.

the

an

ciliar y

ganglion

anatomic

PD.

Autonomic

Res.

21.

control

of

the

eye.

W ,

Auton

Schrödl

Neurosci:

akker

MM,

pathetic

ner ve

F .

Compr

Huang

J,

&

Clin.

Possin

pathways.

Pick

TP ,

Crown;

7.

R.,

control

of

the

eye

and

the

22.

2011;165(1):67–79.

B,

DE,

etal.

Ophthalmol

Human

Plast

orbital

Reconstr

sym-

accommodation:

Physiol

8.

Opt.

Gilmartin

23.

Sci.

Gray’s

Anatomy.

15th

ed.

New

Y ork:

Wolsohn

evidence

Hogan

and

for

JS.

Sympathetic

inter-subject

control

variation.

of

RE.

ciliar y

logical

B,

e

eects

on

Ophthal

Winn

tor

B,

between

inner vation.

Invest

tonic

accom-

Ophthalmol

antagonists

11.

MA,

Roseneld

accommodative

in

a

(Hoboken,

12.

Horn

AK,

groups

and

M,

etal.

adaptation.

in

May

the

Pharmaco-

PJ,

2007).

Eberhorn

W ,

Optom

Vis

Sci.

and

R.

Anatomy

of

the

etal.

of

Eect

ciliar y

of

ß-adrenocep-

smooth

muscle.

etal.

Signicant

among

the

facial

dierences

Hamel

O,

eerents

W ,

etal.

dened

by

reappraisal

JT .

Dening

nucleus.

autonomic

Orbit.

Corre

mydriasis.

16.

Joo

W ,

Surg

Ruskell

muscle:

18.

Burde

Brain

Ploteau

a

F ,

ner ve.

GL.

Res.

S,

skin

specimens.

ner ves:

Anat

their

of

the

29.

Rec

subtypes

Anat.

Funaki

Clin

T,

Anat

Ophthalm

Direct

the

cell

histochemical

31.

7th

ed.

component

system.

a

Vasomotor

Philadelphia:

Ciliar y

ganglion

explanation

unitar y

of

pri-

Eugene

on

a

di-

ner ve

pathway

pressure.

of

facial

Exp

Eye

eects

in

of

the

facial

eye.

ner ve

Acta

stimula-

Physiol

Scand.

etal.

and

&

M,

clinical

etal.

Patterns

application.

of

Clin

inner vation

Anat

(New

of

Y ork,

JF ,

Merida-Velasco

Müller :

Acta

obser vations

Anat

JS,

(Basel).

etal.

responses

to

blepharoptosis.

JR,

on

Jimenez-Collado

human

fetuses

J.

measur-

1990;139(4):300.

Distribution

topical

0.5%

Ophthalmol

of

adrenergic

apraclonidine

Plast

Reconstr

recep-

in

Surg.

Saunders;

HS.

9th

JE,

of

aerents

and

32.

Y ork,

the

Physiol

N.Y .).

ner ve

anatomy

33.

Optics.

34.

Hackmiller

prejunctional

iris-ciliar y

Loewenfeld

IE.

Johnson

e

the

LN.

relative

to

the

the

the

eye:

WM

M2-type

Exp

Eye

Jr,

ed.

Adler’s

eect

of

muscarinic

of

light

receptors

norepinephrine

Res.

Anatomy,

release

in

the

1994;58(2):175–180.

Physiolog y,

intensity

pupillar y

Physiolog y

1992:412.

and

Butter worth-Heinemann;

aerent

Lam

BL,

ompson

defect.

Kawasaki

A,

Am.

defect.

on

Am

Clinical

1999.

measurement

J

Ophthalmol.

Kardon

Wirtschaer

JD,

acetylcholine

for

HS.

Am

J

Brightness

Ophthalmol.

R.

Disorders

sense

and

the

relative

aerent

1989;108(4):462.

of

the

pupil.

Ophthalmol

Clin

2001;14(1):149.

the

Volk

to

tonic

Bourgon

P ,

ity

iris

of

the

Pilley

CR,

Sawchuk

dener vated

pupil

FJ,

iris

syndrome

ompson

sphincter

Selhorst

JB,

Madge

in

G,

Adie’s

Ghatak

syndrome.

RJ.

Transaqueous

sphincter

(Adie

muscle:

syndrome).

a

diusion

mecha-

Ann

Neurol.

HS.

Cholinergic

tonic

pupil.

Am

supersensitiv-

J

Ophthalmol.

Ann

N.

e

Neurol.

neuropatholog y

of

the

1984;16:138.

Salvesen R. Innervation of sweat glands in the forehead. A study in

35.

Wilhelm

36.

Cooper-Knock

of

ciliar y

1990;10(3):239.

to

RC.

Pupil:

Boston:

Hart

Mosby ;

inhibition

body.

e

In:

Louis:

patients with Horner’ s syndrome. J Neurol Sci. 2001;183(1):39–42.

2014;27(1):61–88.

pathway

pathway

of

pupil.

St

1978;85:373.

postganglionic

Microsurgical

e

ed.

1978;4:1.

Wol ’s

2012;34(10):897–902.

(New

Kluckman

with

Applications.

of

2008;171:97–106.

In:

Eye,

Jumblatt

nism

within

Res.

the

North

Edinger-Westphal

pupillar y

Brain

ner vous

parasympathetic

1988;463:158.

perspective

2011;519(8):1413–1434.

intraocular

vasodilation

Baek

and

with

pupillar y

30.

Perioculomotor

population

Prog

etal.

possible

Accommodation

review.

RM.

a

Radiol

Y oshioka

trigeminal

17.

P ,

of

SY ,

Holmes-Adie

variations:

Neurol.

on

Edinger-W estphal

1990;109(4):481.

1976:396–405.

15.

e

functional

parasympathetic

A.

H,

mm.

Jang

ompson

of

cadaveric

preganglionic

and

28.

2008;507(3):1317–1335.

Erichsen

Eye

HS,

density

Härtig

Neurol.

Orbital

Jang

man

Comp

inuence

Bill

gland

muscle

SJ,

human

2016;299(8):1054–1059.

A,

Edinger-W estphal

War wick

B,

control

human

properties:

Comp

Sun

ber

J

etal.

and

2014;27(8):1174–1177.

mediate

2002;22(5):359.

KH,

using

monkey

J

Opt.

ner ve

perioculomotor

mate

14.

N.J.:

Gilmartin

autonomic

Cho

study

functional

nucleus.

13.

T,

sympathetic

histologic

on

J,

Balsiger

35–150

Park

of

27.

HM,

Physiol

Matsubayashi

25.

Vis

26.

Culhane

Ophthalmol

G,

lacrimal

patients

1992;69(4):276.

10.

its

PJ,

2018;34(6):547–551.

relationship

muscle

Bullimore

ocular

and

Rodriguez-Vazquez

tor

1985;26:1024.

Gilmartin

Scott

ing

2002;22(5):366–371.

B,

modation

9.

editors

EH,

An

non-cholinergic

N.Y .).

Surg.

24.

Mallen

GL.

Stjernschantz

the

1977:799.

Gilmartin

terminology.

origin

Orbital

Howden

May

1970;106:323.

tion:

2008;24:360–366.

6.

JC,

structural,

1980;109:45.

Autonomic

Basic

Ruskell

ner ve

study.

2006;49:156–160.

Gamlin

historical,

chotomous

1995;36:762–775.

microsurgical

importance

anatomy

2015;5(1):439–473.

Neuhuber

iris.

AL.

Neurosurgery.

E.

clinical

Physiol.

4.

Rhoton

Bittencourt

a

revisited.

H.

Horner

Lebas

M,

hours

aer

Curr

Pepper

I,

using

Opin

Neurol.

Hodgson

topical

T,

2008;21:36–42.

etal.

Early

apraclonidine.

J

diagnosis

Neuro-

2011;31(3):214–216.

Seror

medullar y

pupil.

J,

syndrome

Ophthalmol.

37.

e

J,

acute

Debroucker

onset

stroke.

J

of

T.

Positive

horner

apraclonidine

syndrome

Neuro-Ophthalmol.

in

test

dorsolateral

2010;30(1):12–17.

36

ponto-

15

Visual

e

visual

pathway

consists

of

the

series

of

cells

and

synapses

synapses

that carr y visual information from the environment to the brain

exit

for

each

processing.

optic

and

tract,

striate

special

into

a

It

cortex

sensor y

neuronal

amacrine

includes

lateral

cell

(Fig.

cell,

retina,

e

ner ve,

(LGN),

rst

cell

optic

optic

in

the

photoreceptor—converts

that

then

optic

nucleus

15.1).

the

signal

and

the

geniculate

to

is

passed

the

to

ganglion

the

bipolar

cell.

All

chiasm,

radiations,

cell

these

and

cells

eye

from

energ y

e

lie

the

the

in

the

in

this

via

crossing

side

of

chiasm

bers

and

within

retina

opposite

pathway—a

light

the

leave

visual

the

the

in

the

to

the

the

the

of

LGN,

as

the

Central

axons

with

chiasm

e

optic

where

the

optic

occipital

information

circle

e

ner ve,

optic

brain.

LGN

cortex

pathway,

retina.

optic

about

Pathway

of

the

and

tract

the

the

the

bers

terminating

carries

next

From

visual

these

synapse

radiations

lobe.

ganglion

nasal

that

cells

from

in

the

bers

occurs.

terminate

various

points

environment

is

darker

represents

Overlapping macular

visual

zone

fields

Lightest

shades

represent

monocular

Projection

on Projection

left

fields

on

retina right

retina

Optic nerves

Optic

Projection

on

chiasm

left Projection

dorsal

on

right

lateral dorsal

geniculate

lateral

nucleus

Optic

tracts

geniculate

nucleus

Lateral

geniculate

nuclei

Calcarine

fissure

Projection

Projection

on

on

left

striate

cor tex

right

striate

Fig.

15.1

The

visual

cor tex

pathway.

239

CHAPTER

240

transferred

ciation

to

related

15

Visual

neurological

Pathway

centers

and

to

visual

asso-

areas.

is

tough,

dense

bers.

pathway

sends

a

and orientation of the bers within each structure, then it briey

space

to

reviews

arachnoid

cic

chapter

characteristic

locations

and

discusses

optic

in

disc

the

are

the

visual

visual

structures

eld

defects

pathway.

discussed

of

e

in Chapter

the

visual

Inner

associated

anatomy

with

of

the

spe-

retina

8

ne

this,

e

a

space

to

tissue

thin

network

connect

intracranial

uid.

connective

to

of

the

containing

collagenous

trabeculae

innermost

around

the

subarachnoid

subarachnoid

optic

space

is

through

layer,

the

ner ve

space

numerous

membrane

and

larger

is

the

pia

of

subarachnoid

mater.

e

continuous

contains

directly

elastic

arachnoid

sub-

with

the

cerebrospinal

behind

the

globe

16

compared

that

ANATOMY

OF

VISUAL

PATHWAY

STRUCTURES

with

relatively

the

low

remainder

cerebrospinal

compared

with

the

comatous

damage.

intraocular

17

Optic

e

Nerve:

retinal

Cranial

nerve

bers

Nerve

make

a

II

the

90-degree

turn

at

the

optic

disc

pia

tissue

and exit the globe as the optic ner ve. is nerve consists of visual

the

bers,

runs

mater

septa

pia

e

the

continues

its

course.

uid

ere

pressure

pressure

may

is

evidence

within

play

a

the

role

in

orbit

glau-

18

branches,

into

of

loose,

sending

ner ve

along

vascular

blood

(see Fig.

the

connective

vessels

15.2).

Of

intracranial

and

these

optic

tissue

of

connective

sheaths,

ner ve

only

where

15

90%

bers,

of

which

will

approximately

terminate

10%,

in

project

the

to

LGN.

areas

e

rest

of

controlling

the

pupil

e

through

the

arachnoid

subarachnoid

does

not

space

continue

to

the

through

optic

the

it

19

chiasm.

optic

canal

but

20

responses,

circadian

rhythm,

or

the

orientation

of

the

head

and

merges with the pia mater within the canal.

eyes toward stimuli. V arious counts of the optic nerve bers range

uous

from 1 million to 2.22 million, with their size ranging from small-

of

with

the

sclera

anteriorly

and

the

e dura is contin-

periosteum

and

tendons

20

the

extraocular

muscles

posteriorly.

1–5

diameter

e

four

macular

optic

bers

ner ve

segments

on

is

the

to

5

larger-caliber

to

6

basis

cm

of

long

extramacular

and

location:

can

be

bers.

divided

intraocular

(0.7–1

into

CLINICAL

Increased

mm),

within

intraorbital (30 mm), intracanalicular (6–10 mm), and intracra-

4

nial

(10–16

e

6

7

mm).

intraocular

section

of

the

optic

ner ve

can

be

COMMENT: Papilledema

intracranial

the

sheaths

cerebrospinal

of

the

the

optic

nerve

resulting

nar

optic

nerve

bers.

optic

in

This

stasis

is

uid

nerves.

of

seen

pressure

The

the

axoplasmic

clinically

will

increased

as

increase

pressure

ow

bilateral

pressure

compresses

within

the

swelling

of

prelami-

the

optic

divided

disc. When disc edema is caused by increased intracranial pressure it is called

into prelaminar and laminar sections depending on the location 16

papilledema

relative

glial

to

the

tissue

lamina

network

cribrosa.

provides

In

the

prelaminar

structural

support

optic

for

ner ve,

the

fascicles.

e

orbital

portion

of

the

optic

ner ve

15.3).

delicate

ner ve bers, with sheaths of astrocytes bundling the ner ve bers

into

(Fig.

a

contains

As the unmyelinated retinal bers pass through the scleral perfo-

rations of the lamina cribrosa, they become myelinated by oligoden-

8

approximately

within

the

e

border

extends

Bruch

928

fascicles.

intracranial

tissue

anteriorly

membrane

of

number

decreases

slightly

the

drocytes,

It

Elschnig

from

to

at

section.

consists

edge

separate

of

the

the

of

brous

sclera

choroid

and

from

tissue

fuses

that

with

ganglion

cell

is

the

myelin-producing

postulated

cytes

e

because

sheath

with

the

the

lamina

myelination

of

pia

that

connective

mater

cells

does

not

tissue,

meningeal

of

cribrosa

the

is

central

a

normally

branching

covering,

is

nervous

barrier

to

occur

from

added

in

and

to

system.

oligodendro-

the

retina.

continuous

the

glial

sheath

9–11

axons

as

they

pass

through

the

optic

ner ve.

e

length

of

this

border tissue may correlate with the lamina cribrosa defects and

of

each

tissues

fascicle

double

posterior

the

to

the

diameter

of

lamina

the

cribrosa.

optic

nerve

ese

as

it

additional

leaves

the

eye.

12

microvascular

cyte

and

pia

dropout

mater

associated

form

a

with

tissue,

the

glaucoma.

border

e

tissue

of

astro-

e

nerve

is

approximately

1.5

to

1.8

mm

in

diameter

at

the

level

Jocoby,

of the retina and 3 mm aer its exit from the globe, increasing to 4 to

As

5 mm

21–24

that

separates

the

choroid

from

the

optic

ner ve

bers.

that

with

the

inclusion

of

the

optic

nerve

sheaths.

e

septa

6

tissue

it

extends

separates

to

the

the

outer

outer

edge

retinal

of

the

layers

retinal

from

the

ner ve

optic

6

and

is

tions

called

within

the

intermediar y

the

glial

border

tissue

tissue

of

13

ner ve

layer,

bers

that

separate

present

in

the

the

ber

optic

fascicles

nerve

end

probably

near

the

function

chiasm.

similar

to

Astrocytes

Müller

cells

14

Kuhnt.

may

ber

Tight

prevent

leakage

junc-

from

of

the

retina.

ey

provide

structure,

store

glycogen,

and

regulate

the extracellular concentration of certain ions.

15

the

adjacent

border

tissue

choriocapillaris

is

shown

in

Fig.

into

the

optic

ner ve

head.

e

15.2

e

tract,

e intraorbital (postlaminar) optic ner ve length exceeds the

only

a

nal

sine

without

ner ve

shaped

stretching

rounded

medial

wave

by

the

rectus

(which

associated

the

rectus

muscles

explains

with

optic

cur ve,

ner ve.

Within

muscles.

are

the

allowing

e

to

full

orbit,

sheaths

adherent

pain

the

for

the

associated

of

eye

the

the

ner ve

is

superior

sheath

with

excursions

eye

of

the

sur-

and

the

perforated

anterior

substance,

cerebral

arter y

the

root

lie

of

the

superior

to

olfactor y

the

optic

ner ve in its intracranial path. e sphenoid sinus is medial, with

distance from the globe to the apex of the orbit, giving the ner ve

slight

anterior

and

a

thin

carotid

plate

of

arter y

bone

is

separating

below

and

then

it

from

lateral

the

to

ner ve.

the

e

ner ve,

inter-

and

the

ophthalmic arter y enters the dural sheath of the optic ner ve as it

passes

through

the

optic

canal.

optic

movements

neuritis).

Optic

e

Chiasm

optic

chiasm

is

roughly

rectangular,

approximately

15

mm

4,7,25

e

ingeal

the

intraorbital

sheaths

cranial

optic

ner ve

continuous

contents.

e

is

with

surrounded

the

outermost

by

meningeal

sheath,

the

three

men-

coverings

dura

mater,

of

is

horizontally,

with

the

8

mm

anterior

intracranial

subarachnoid

space

optic

and

is

to

posterior,

ner ve,

the

surrounded

and

optic

by

4

mm

high.

chiasm

lies

cerebrospinal

As

in

the

uid.

CHAPTER

Fig.

15.2

optic

Intraocular

disc

edge,

membrane

tion

of

the

choroid,

canal

ar y

(4)

and

of

about

dotted

in

blue).

rated

by

Anderson

is

chiasm

that

an

is

a

lies

within

common

anastomotic

the

of

1969;

for

of

lies

in

in

the

of

(6),

and

of

the

the

by

along

and

tissue,

its

is

e

circulation

internal

including

of

the

carotid

most

of

the

vertebral

arteries

cerebral

Jacoby

Ner ve

On

(Gl.C)

from

Willis,

and

and

a

circle

e

posterior

basilar

the

of

blood

circle

of

arteries

arteries

anterior

hemispheres

pia

Ar,

the

the

dotted

white

in

all

with

lamina,

line),

the

by

Du,

human

a

to

few

intermedi-

(upper

Pia,

tissue

become

astrocytes

to

pia

be

optic

tissue

monkey

of

form

sepa-

chiasm

Jacoby,

mater.

optic

the

ner ve

fascicles

the

border

por-

segregated

bers

continue

dura;

and

optic

cribrosa

the

the

of

connective

and

way

central

the

are

ner ve

cells)

the

the

retina

bundles

with

the

at

limiting

termination

surrounding

mater)

of

of

separated

Arachnoid;

portion

ves-

Willis

that

join

and

(Fig.

cranial

orbital

15.4).

regions,

and

ocular

to

the

the

brainstem,

occipital

lobes,

ipsilateral

nicating

(From

ner ve.

Arch

artery.

posterior

e

cerebral

anterior

artery

cerebral

and

by

a

posterior

anterior

commu-

communicating

arteries are anterior and superior to the chiasm. An internal carotid

artery lies on each lateral side of the chiasm.

Above

third

the

optic

ventricle.

pituitar y

above

including

and

anteriorly

ply

regions,

are

portion. The

rior

posterior

continuous

Astrocytes

prelaminar

course.

is

thickened

posterior

internal

241

Pathway

terminates

the

surrounding

bers

(lower

(black

continuous

is

the

retina

forming

reaching

astrocytes

structures. Branches of the vertebral arteries and basilar artery sup-

the

At

astrocytes

cribrosa

interorbit al

(2).

the

Visual

82:506.)

of

supply

of

fascicles.

the anterior circulation of the internal carotid arteries with the pos-

terior

the

retina.

derived

orbit al

of

membrane

astrocytes.

lamina

Where

astrocytes,

Kuhnt

tissue

the

ner ve

(Gl.M),

Ultrastructure

this

of

surrounding

laminar

(septal

ner ve

border

nerve.

with

between

oligodendrocytes

present

aneurysms.

anterior

(3)

part

astrocytes

optic

specimens,

meniscus

fascicles

(7)

optic

continuity

termination

external

tissue

of

some

central

fascicles

than

Hoyt W.

circle

location

group

are

here

the

D,

Ophthalmol.

e

the

or

orbital

in

stroma. The

the

columns

mantle

surrounding

sels

At

In

the

are

Elschnig

bundles,

connective

(Sep). The

at

of

(1a)

the

of

(5)

ner ve

cells)

layer

(1b).

choroidal

and

(red-colored

thinner

the

Kuhnt

the

myelinated,

a

tissue

part

cells

forming

1000

line),

(drawn

Elschnig

disc,

border

tissue

into

of

and

Müller

15

to

gland,

the

the

and

chiasm

sella

chiasm

is

the

Approximately

the

(Fig.

turcica

hypothalamus

1

cm

below

infundibulum

15.5).

(the

e

fossa

lies

position

in

which

and

the

oor

chiasm

immediately

of

the

the

optic

of

the

is

the

poste-

chiasm

pituitar y

gland

and inferomedial temporal lobes, thus supplying most of the ocular

sits) can var y from being directly above it (in 75% of the popula-

motor

tion)

centers

complete,

the

and

the

anterior

communicating

cortical

visual

cerebral

artery,

and

areas.

arteries

each

are

internal

If

the

circle

joined

carotid

via

of

the

artery

Willis

is

anterior

is

joined

short

to

a

and

gland)

or

position

the

referred

chiasm

postxed

lies

(if

to

as

above

the

optic

prexed

the

(if

anterior

ner ves

are

the

optic

part

long

of

ner ves

the

and

are

pituitar y

the

chiasm

CHAPTER

242

15

Visual

Pathway

A

B

Fig.

is

situated

chiasm

is

toward

the

anteriorly

posterior

part

of

the

pituitar y

displaced

in

approximately

displaced

in

15%.

15.3

gland).

10%

of

e

individ-

Papilledema.

of

the

bers

(which

are

still

the

axons

of

retinal

ganglion

cells)

terminate in the LGN. Fibers from the retinal ganglion cells may

15

uals

and

posteriorly

Posterior

into

on

both

only

to

the

one

the

right

side

optic

and

are

chiasm,

the

le

described

the

sides

branch

visual

of

the

pathway

brain

continues

(the

structures

here).

tures,

destined

e

Tract

optic

in

tract

approximately

is

3.5

a

cylindric,

mm

high

slightly

and

5.1

that

the

same

alternatively,

for

a

specic

cell

sends

some

bers

retinal

structure.

to

various

ganglion

e

aerent

cell

target

axons

bers

of

struc-

may

the

be

pupil-

lomotor reex leave the optic tract before reaching the LGN and

pass

Optic

so

or

attened

mm

long

band

that

of

bers

runs

by

the

way

of

the

midbrain.

nucleus

in

the

superior

Other

brachium

bers

hypothalamus

to

project

and

to

the

to

the

pretectal

the

nucleus

suprachiasmatic

superior

colliculus.

from

7

the

posterolateral

corner

of

the

optic

Anterior

Anterior

chiasm

to

communicating

cerebral

the

LGN.

Most

artery

artery

Optic

nerve

Ophthalmic

artery

1

Optic

∗

chiasm

2

Pituitary

stalk

3

Internal

carotid

Posterior

cating

communi-

artery

Mamillary

Optic

artery

body

tract

Posterior

cerebral

artery

Basilar

Fig.

15.4

circle

Louis:

Relationship

of Willis.

Mosby;

(From

1981 .)

of

the

optic

Harrington

DO.

artery

chiasm

to

The Visual

vessels

Fields,

of

ed

the

5.

St

Fig.

15.5

showing

(2),

Sagittal

its

section

relationship

infundibulum

to

(arrow),

through

the

and

the

optic

hypothalamus

sphenoid

sinus

chiasm

(1),

(3).

(asterisk)

pituitar y

gland

CHAPTER

e

optic

tract

lies

along

the

upper

anterior

and

then

the

15

Visual

243

Pathway

lat-

eral surface of the cerebral peduncle and runs parallel to the pos-

terior

cerebral

capsule

is

arter y.

medial,

e

and

the

globus

pallidus

hippocampus

is

is

above,

below

the

the

internal

optic

K6

tract.

K5

Lateral

Geniculate

Information

system

from

passes

all

Nucleus

the

through

sensor y

the

systems

thalamus

except

before

being

the

olfactor y

transferred

to

the cerebral cortex. Visual information is processed in the LGN,

located

on

relayed

to

the

dorsolateral

higher

cortical

aspect

centers.

of

the

e

thalamus,

LGN

before

resembles

an

being

asym-

metric cone, the rounded apex of which is oriented laterally. e

retinal

LGN

axons

project

e

terminate

to

LGN

the

is

a

here.

visual

layered

Most

of

the

bers

that

leave

the

cortex.

structure.

e

layers

are

piled

on

each

other, with the larger ones draping over smaller ones, and some lay-

ers becoming fragmented and irregular. e cells within a layer are

all of the same type, and three types have been identied according

to size. Magnocellular layers contain large cells, parvocellular layers

contain medium-sized cells, and koniocellular layers contain small

cells.

e

number

of

layers

present

depends

on

the

location

of

the

plane through the structure. In the classic textbook presentation of

the

LGN,

six

layers

are

seen.

Two

magnocellular

layers

are

located

inferiorly and numbered 1 and 2, and the four parvocellular layers

above

these

them

six

are

layers

numbered

lies

a

3,

4,

5,

and

koniocellular

6

(Fig.

layer

15.6).

which

Below

receives

each

of

informa-

26

tion

from

magnetic

layers

short

wavelength

resonance

were

found

cones

imaging

more

(Fig.

(fMRI)

ventral

15.7).

on

and

Using

humans,

medial.

functional

magnocellular

Parvocellular

layers Fig.

15.7

Coronal

section

through

the

lateral

geniculate

nucleus

27

were found dorsally and laterally.

e

LGN

is

not

a

simple

of

relay

station.

It

also

receives

input

a

cellular

from cortical and subcortical centers and reciprocal inner vation

four

from

VA,

ing.

the

It

visual

cortex,

regulates

the

becoming

ow

of

visual

a

center

of

complex

information,

process-

ensuring

that

the

important

e

sule

is

optic

information

tract

lateral,

the

enters

medial

the

is

sent

LGN

to

the

nucleus

e

is

internal

medial,

al s

A,

koniocellular

two

JM.

M

The

editors.

showing

layers,

lateral

Adler's

(K)

and

the

par vocellular

layers.

six

K

this

layers.

geniculate

Physiology

At

the

plane

(From

nucleus.

of

(P),

Eye,

In:

magno-

there

Kaufman

ed

are

Casagrande

10.

St

PL,

Louis:

2003.)

cap-

and

the

inferior horn of the lateral ventricle is posterolateral to the LGN.

e

cr e s t

o

and

layers,

Ichida

Alm

monkey

cortex.

anteriorly.

geniculate

P

(M),

Elsevier;

28

most

macaque

axons

Optic

leave

the

LGN

Radiations

as

the

optic

radiations.

(Geniculocalcarine

Tract)

D

e

6

optic

deep

rior

in

radiations

the

white

bundle

spread

matter

sweeps

of

out

the

anteriorly

fanwise

cerebral

and

as

they

leave

the

hemisphere.

laterally

around

LGN,

e

the

ante-

anterior

5

tip

of

the

temporal

posteriorly

(Meyer

horn

loop)

of

to

the

lateral

travel

4

in

ventricle

the

before

temporal

lobe

turning

en

route

29,30

to

the

occipital

superior

to

the

lobe

(Fig.

temporal

15.8).

horn

e

of

the

middle

lateral

bundle

ventricle.

travels

e

poste-

3 Medial

rior

bundle

travels

within

the

parietal

lobe

lateral

to

the

occipi-

tubercle 2

Lateral

tal

horn

of

the

lateral

ventricle

before

terminating

in

the

striate

horn Hilus

cortex.

1

e

primar y

Fig.

15.6

Laminae

in

the

right

lateral

geniculate

crossed

retinal

projections

projections

terminate

terminate

in

in

laminae

laminae

2,

3,

1,

4,

and

and

5.

6.

involvement

of

one

or

more

of

these

cortex;

optic

radiation

however,

there

bers

are

terminate

some

bers

in

that

the

have

29,31

connections

with

the

extrastriate

cortex

areas.

Un-

Selective

Visual partial

visual

of

nucleus.

direct Crossed

majority

laminae

will

Cortex

pro-

e primary visual cortex (striate cortex or V1), is located almost duce

an

asymmetric

homonymous

visual

eld

defect,

depend-

entirely on the medial surface of the occipital lobe. Just a small poring

on

Visual

the

extent

Fields,

ed

of

5.

laminar

St

Louis:

damage.

Mosby;

(From

1981 .)

Harrington

DO.

The

tion

(perhaps

1

cm

long)

extends

around

the

posterior

pole

onto

CHAPTER

244

15

Visual

Pathway

1

2

Fig.

15.8

The

visual

pathway

from

the

optic

nerve

to

the

Fig.

15.9

rine

ssure

lobe.

laterally

(From

The

before

anterior

turning

Lundy-Ekman

tation,

5th

ed.

St.

optic

radiations

posteriorly

L.

to

Neuroscience:

Louis,

MO:

sweep

travel

to

anteriorly

the

occipit al

Fundamental

Elsevier;

for

surface

(arrow),

the

of

cerebral

cuneus

cortex

gyrus

(1),

showing

and

the

the

calca-

lingual

gyrus

oc(2)

cipital

Medial

of

the

occipital

lobe.

and

lobe.

Rehabili-

2018.)

Cells

are

also

distributed

in

a

vertical

organization,

according

to the eye of origin, forming alternating parallel ocular dominance

columns.

ese

represents

the

columns

are

physiologic

lacking

blind

in

spot

the

area

because

of

this

the

cortex

region

that

receives

information exclusively from one eye. A second system of columns,

the lateral surface. e visual cortex also is called the striate cortex

specic for stimulus orientation, responds on the basis of the direc-

because

tion

37

is

a

white

myelinated

characteristic

of

this

ber

area.

layer,

e

the

white

calcarine

stria

ssure

of

Gennari,

extends

from

of

a

light

slit

or

edge.

Contour

analysis

and

binocular

vision

are two functions of the visual cortex, and such processing is a func-

the parietooccipital sulcus to the posterior pole, dividing the visual

tion

cortex

within the striate cortex are activated only by input from the LGN,

into

an

upper

portion

(the

cuneus

gyrus)

and

a

lower

part

of

both

its

horizontal

and

its

vertical

organization.

e

cells

38–40

(the lingual gyrus) (Fig. 15.9). Most of the primary visual cortex is

although other cortical areas have input into the striate cortex.

buried in the tissue within the calcarine ssure.

e

and

is

pr imar y

visual

organized

into

cor tex

has

hor izont al

a

e

t hickness

layers

and

of

ab out

ver t ical

2

mm

columns.

and

a

striate

the

complete

L ayer I, t he most sup er cial layer, cont ains a fe w s cattered neu-

receives

rons.

tract,

L ayer

cor tical

wit h

II

cont ains

layers.

b ot h

L ayer

ne ar

and

neurons

III

far

t hat

cont ains

cor tical

s end

axons

neurons

on ly

t hat

lo cations.

to

deep er

communicate

L ayer

IV

cont ains

eye

communicates

elds.

retinotopic

well

as

the

for

foveation,

e

map

communication

as

information

tion,

cortex

frontal

the

the

but

control

the

is

of

superior

colliculus,

contralateral

bers

cortex.

perception

and

of

from

striate

with

superior

exiting

It

does

the

not

important

saccadic

eld

of

has

vision,

posterior

analyze

for

eye

colliculus

which

optic

sensor y

visual

orienta-

movements

with

41,42

t he str ia of G ennar i and is sub divided into st rat a, one of w hich

input

receives infor mation f rom t he magno cellular layers of t he LGN

the

and

tribute

ers

of

anot her

of

t he

t he

are as.

ot her

receives

LGN.

pr imar y

L ayer

are as

V

in

L ayer

infor mation

IV

visual

cor tex,

s ends

t he

s ends

axons

brainstem.

f rom

axons

as

to

to

well

t he

L ayer

t he

p ar vo cellular

more

as

sup er cial

ot her

sup er ior

VI

s ends

visual

lay-

are as

cor t ical

collic ulus

proj e c t ions

and

back

frontal

tar y

are

from

to

and

the

lobe,

the

e

of

ocular

cortex

from

the

elds.

bers

e

from

conjugate

to

near

combines

LGN

frontal

striate

eye

cortex

movements.

are

objects

and

and

the

eye

movements

responses

striate

relayed

eye

receive

control

reex

pupillar y

tion

frontal

mediated

(see Ch.

analyzes

transmits

that

B oth

in

this

in

con-

volun-

area,

as

14).

the

this

elds,

visual

informa-

information

to

the

28

to

t he

LGN.

Certain

higher

cortical

regions

are

active

during

motion

stimula-

visual

provide

association

further

areas

interpretation.

(the

ese

extrastriate

areas

(V2,

cortex),

V3,

V4,

which

and

V5)

32

tion,

e

whereas

others

magnocellular

are

active

areas

during

mediate

color

vision

movement

stimulation.

detection

and

low-

surround

the

progressively

spatial-frequency contrast sensitivity, and the par vocellular areas

tex.

mediate

connected

color

and

high-spatial-frequency

contrast

sensitivity,

33–36

although

this

generalization

oversimplies

the

properties.

e

striate

more

visual

to

and

the

cortex

lateral

visual

and

and

are

arranged

anterior,

association

corresponding

within

areas

areas

in

in

in

a

the

one

the

nesting

pattern,

occipital

cor-

hemisphere

other

are

hemisphere

4

through the posterior portion of the corpus callosum.

CHAPTER

Extrastriate

lar Dorsal

objects

areas

and

allow

when

15

Visual

object

objects

are

245

Pathway

recognition

even

transformed,

among

such

as

a

simi-

change

stream

in

size,

stream

rotation,

and

mation

or

dorsal

(Fig.

illumination.

stream,

15.10).

occipitotemporal

temporal

cortex.

ties,

as

e

cortex

is

are

Two

ventral

and

pathway

aids

43

size,

color,

and

in

stream

includes

Ventral

such

pathways,

involved

travels

V2,

in

the

ventral

processing

V4,

and

processing

infor-

through

the

the

inferior

object

quali-

44

shape.

e

dorsal

stream

courses

stream

through

the

temporal

and

occipitoparietal

area).

visually

e

dorsal

guided

cortex

stream

actions,

and

involves

processes

including

position,

43

perception,

BLOOD

Fig.

15.10

Visual

association

areas.

(From

Neuroscience:

Louis,

MO:

Fundamentals

Elsevier;

for

relationships

SUPPLY

TO

between

THE

motion,

depth

44

VISUAL

PATHWAY

Rehabilit ation,

5th

ed.

structures

of

the

visual

pathway

have

an

extensive

blood

sup-

outer

reti-

St.

ply.

Fig.

15.11

nal

layers

shows

many

of

the

involved

vessels.

e

2018.)

receive

nutrition

from

the

choroid,

whereas

Anterior

artery

Anterior

cerebral

artery

Central

retinal

artery

Ophthalmic

carotid

artery

Middle

cerebral

artery

artery

Posterior

communicating

artery

Lateral

(deep

striate

choroidal

Posterior

Middle

Posterior

cerebral

Fig.

15.11

al.

Vascular

Anatomy

of

supply

the

eye

of

and

the

orbit.

artery

choroidal

cerebral

artery

artery

Calcarine

artery

visual

artery

optic )

Anterior

et

medial

objects.

communicating

Internal

(the

information

Lundy-Ekman

e L.

and

V5

spatial

artery

pathway.

In: The

Eye,

5th

From

ed.

Forrester

Elsevier;

JV ,

2021 .

Dick

AD,

McMenamin

PG,

the

inner

CHAPTER

246

retina

the

is

supplied

by

anastomotic

the

ring

and

peripapillary

Fig.

12.3).

15

Visual

central

of

retinal

branches

vessels

Pathway

supply

artery.

of

the

the

e

short

circle

of

ciliary

intralaminar

Zinn,

arteries,

optic

disc

(see

4 45

Capillaries

nonfenestrated

vessels

within

endothelium

perfusing

the

nerve

the

optic

joined

head

by

are

nerve

zonula

part

of

are

composed

occludens,

the

thus

blood-brain

of

the

bar-

15 46

rier.

Pial vessels supply the optic nerve throughout its length. e

intraorbital

from

the

branch

and

canalicular

ophthalmic

of

the

pial

artery.

internal

vessels

e

carotid

are

supplied

superior

artery,

is

by

branches

hypophysial

the

main

artery,

blood

supply

a

to

19

the intracranial optic nerve.

Branches of the ophthalmic and ante-

rior cerebral arteries may also contribute to the distal and proximal

vascular supplies of the intracranial optic nerve, respectively.

e blood supply to the optic chiasm is rich and anastomotic,

with arterioles from the circle of Willis forming capillar y beds at

47

two

48

levels.

cerebral,

e

superior

anterior

network

is

communicating,

supplied

posterior

by

the

anterior

communicating,

and superior hypophyseal arteries, whereas the inferior network

is

supplied

by

the

superior

hypophyseal

and

posterior

com-

49

municating

of

the

arteries.

internal

although

e

carotid,

small

is

anterior

a

branches

choroidal

primar y

from

the

supplier

middle

arter y,

of

the

a

branch

optic

cerebral

tract,

arter y

also Fig.

4

6

15.12

Nerve

ber

pattern

of

the

right

retina.

The

papillo-

25

contribute.

e

blood

supply

to

the

LGN

is

derived

from

the macular bundle (blue) enters the temporal aspect of the optic disc.

anterior

choroidal

arter y

and

the

lateral

choroidal

and

posterior The

6

choroidal

branches

of

the

posterior

cerebral

temporal

disc.

e

anterior

choroidal

group

of

branch

bers

of

cerebral

optic

arter y

the

and

is

by

cerebral

including

are

middle

supplied

middle

arter y,

radiations

the

the

supplied

cerebral

the

lateral

arter y.

by

the

arter y.

branch,

anterior

e

striate

Branches

calcarine

bers

(yellow)

middle

(deep

of

the

optic)

posterior

supply

the

pos-

to

The

the

to

disc

the

these

sal

bers

(green)

temporal

nasal

to

NR,

nasal

the

bers

disc

radiations.

contribute.

is

the

mented

the

to

e

major

by

calcarine

blood

the

posterior

the

central

with

from

branch

supply

posterior

cerebral

visual

temperooccipital

moses

Branches

eld,

of

of

the

temporal

arter y.

branch

branches

for

the

e

may

of

the

middle

the

arter y

cerebral

cortex,

oen

parietooccipital

occipital

have

the

posterior

striate

or

cerebral

a

dual

middle

posterior

pole,

enter

to

Subramanian,

cerebral

the

The

get

(red)

to

enter

PS,

are

the

nasal

superior

to

superior

and

temporal

the

the

the

and

Patel, VR.

Essentials,

inferior

but

optic

must

nasal

disc.

Walsh

Ed

inferior

bers

disc. The

nasal

macula

optic

and

bers

Hoyt's

disc

travel

(Adapted

3. Wolters

temporal

that

are

from

Clinical

Kluwer;

nasal

through

na-

Miller,

Neuro-

2016.)

also

arter y

supple-

branch

of

corresponding

blood

cerebral

that

bers.

Ophthalmology: The

terior

enter

50

arter y.

supply

arter y

as

the

anasto-

arter y.

separated

the

fovea

riorly

by

and

acteristic

temporal

a

horizontal

called

the

inferiorly

arcuate

retinal

line

extending

horizontal

around

patterns

vessels

in

retinal

the

macular

their

usually

through

raphe,

do

course

not

area,

to

cross

the

must

the

the

center

of

arch

supe-

forming

char-

optic

disc.

horizontal

e

raphe

either. e nasal bers can travel directly to the optic disc and are

described as radiating. Nasal and temporal bers are separated by

FIBER

ORIENTATION

AND

VISUAL

FIELDS a

With

one

the

is

eye

able

looking

to

detect

straight

other

ahead

objects

and

xating

around

the

on

point

an

of

object,

regard,

theoretic

vertical

line

passing

through

the

center

of

the

fovea.

e long nerve bers, from the peripheral retina, are more vitread

in

location

than

are

the

short

peripapillary

bers,

with

extensive

51

although

area

is

is

of

the

the

the

by

bers

in

not

pathway.

in

visual

help

resultant

this

processed

location

this

visual

Knowledge

eld

the

of

from

entire

the

orderly

have

of

ber

a

visible

visual

the

extensively

will

cause

patterns

lesion

on

in

the

intermingling

a

the

basis

defect.

Optic

disc,

to

nasal

courses

e

the

retinal

ganglion

bers

cells

form

characteristic

pat-

up

area

papillomacular

temporal

temporal

do

bundle

(Fig.

to

15.12).

the

optic

e

disc

superior

is

called

and

the

inferior

bers,

the

of

to

optic

nasal

to

superior

to

nerve.

(Fig.

the

of

the

inferior

of

retina

retina

one-twentieth

e

cur ve

e

disc,

approximately

15.13A).

disc

superior

pole.

the

bers

radiate

directly

papillomacular

the

temporal

enter

one-third

only

nasal

side

temporal

the

occupy

bers

e

whereas

temporal

inferior

encompasses

the

the

pattern.

disc,

bundle

bundle

bers

the

the

approximately

the

area

specic

from

from

terns in the nerve ber layer. e group of bers that course from

macular

a

side

directly

lomacular

of

prelaminar

Disc

creating

the

Fibers

axons

the

All of the axons in the ner ve ber layer come together at the optic

papillomacular

Retina

e

in

eld

aerent

arrangement

been

pathway

the

location

is

through

and

pathway

aerent

identify

visual

discernible.

Information

and

e

eld.

to

be

eld.

retina

throughout

the

can

may

visual

the

Damage

pathway

of

in

sensor y

studied.

defect

details

termed

taken

visual

the

(see Fig.

arch

pole

of

of

below

the

boundaries

the

the

the

of

the

disc.

papil-

bers

retinal

one-third

15.12).

around

macular

although

bundle

take

macular

area.

the

e

disc,

between

as

each

CHAPTER

up

their

logical

positions:

rior

temporal

optic

rior

temporal

ner ve,

15

Visual

superior

ner ve,

temporal

inferior

247

Pathway

temporal

bers

in

bers

the

in

supe-

the

infe-

ST ST

SN

superior

nasal

bers

in

the

superior

nasal

SN

ner ve, M

and

inferior

nasal

bers

in

the

inferior

nasal

optic

ner ve

M

(Fig.

15.13B).

IN

IT

IN

IT

Optic

In A

15.13

Right

optic

disc

and

nerve

viewed

from

the

crossed

front.

Surface

of

the

optic

disc

showing

the

orient ation

of

the

47.

e

the

as

they

enter

the

disc.

B,

Coronal

section

showing

nasal

of

ner ve

bers

in

the

optic

ner ve

proximal

to

bers

IN,

Inferior

nasal;

IT,

inferior

temporal;

M,

in

the

cross

(decussate).

chiasm

is

e

ratio

approximately

crossing

pattern

depends

on

processes

that

53

occur

macular;

embryological

directing

the

development,

path

taken

by

with

nerve

certain

bers.

molecular

e

majority

the

of chiasm.

bers

the

guides orientation

uncrossed

ner ve

during bers

chiasm,

to

53

to A,

Chiasm

optic

B of

Fig.

the

the

nasal

bers

cross

in

the

paracentral

rather

than

the

cen-

and

then

SN, 54

tral superior

nasal;

ST,

superior

chiasm.

e

inferior

bers

cross

more

anteriorly

temporal.

travel

back

through

the

chiasm

into

the

contralateral

optic

tract

54

(Fig.

set

of

e

bers

bers

are

from

not

the

always

clear-cut

peripheral

in

retina

all

are

parts

more

of

the

pathway.

supercial

than

15.14).

bers

Traditionally,

looped

opposite

1

optic

to

2

mm

nerve

it

was

thought

forward

before

into

turning

that

the

to

the

inferior

terminal

run

back

part

nasal

of

through

the

the

52

those

coming

from

the

central

chiasm.

retina.

e

Wilbrand)

Optic

Nerve

existence

is

of

these

controversial.

anterior

Some

loops

studies

(anterior

show

that

the

knees

of

anterior

knees of Wilbrand are artifacts caused by the prior enucleation in

55

Near

as

the

they

lamina

do

at

the

cribrosa,

disc,

the

but

bers

within

a

have

the

short

same

distance

orientation

the

macular

those studies cited by Wilbrand.

no

junctional

scotoma

in

the

In addition, some studies found

visual

eld

55

bers

move

to

the

center

of

the

ner ve.

Optic

e

rest

of

the

bers

take

of

the

anterior

chiasmal

aer

surgical

Other

clinical

nerve Superior Superior nasal

fibers temporal

fibers

Inferior

nasal

fibers

Inferior

temporal

fibers

Optic

Optic

Fig.

to

chiasm

tract

15.14

through

exit

Fiber

the

in

orientation

chiasm

the

and

exit

contralateral

through

in

optic

the

the

ipsilateral

tract.

optic

optic

chiasm.

tract.

T emporal

Nasal

bers

bers

(solid

(dotted

lines)

sectioning

56

junction.

lines)

cross

in

pass

chiasm

ndings

in

CHAPTER

248

patients

demonstrating

tence

Wilbrand

15

a

Visual

Pathway

junctional

scotoma

support

the

exis-

layers

receives

the

bers

from

the

and

input

from

just

one

eye:

layers

1,

4,

and

6

receive

57–59

of

knees;

however,

in

some

of

the

cases,

the

contralateral

nasal

retina,

whereas

layers

2,

3,

60

association

inferior

ing

has

been

anterior

angle,

and

chiasm

it

is

53

questioned.

make

thought

e

a

that

bers

large,

it

is

which

almost

this

cross

in

90-degree

sharp

angle

cross-

that

makes

5

Most

receive

of

macula,

the

ipsilateral

structure,

contains

all

temporal

including

layers,

retinal

the

although

more

suspectable

compressive

lesion

anteriorly

the

in

to

could

chiasm

4

compression.

aect

the

despite

It

is

inferior

them

wedge

in

54

them

not

also

possible

bers

as

traveling

they

into

that

a

eral

travel

the

con-

aspects,

e

of

the

some

anatomic

monkey,

of

the

layers

structure

so

of

detailed

the

(Fig.

15.16).

representing

far

medial

the

and

lat-

65

merge.

the

maps

57

bers

human

of

the

LGN

is

monkey

similar

LGN

to

have

that

been

67

tralateral optic nerve.

Furthering the controversy, a recent study

applied

using

the

light

a retinotopic map or representation of the contralateral hemield

axons

revealed

anisotropic

inferior,

reecting

but

not

properties

superior,

bers

of

myelinated

arching

toward

of

to

vision.

the

A

human

structure.

retinotopic

map

Each

is

a

layer

of

the

point-to-point

LGN

contains

localization

of

61

the

contralateral

e

they

asm

optic

superior

cross

in

the

in

nerve

nasal

the

before

bers

more

enter

posterior

contralateral

reversing

optic

the

superior

chiasm

tract.

direction.

and

ese

chiasm,

then

bers

the

leave

make

where

the

chi-

shallower

retina.

ese

maps

are

stacked

on

one

another,

such

that

if

a

line (called a line of projection) were passed through all six layers,

perpendicular

to

the

surface,

the

intercepted

cells

all

would

be

carrying information about the same point in the visual eld. is

54

crossing

from

angles

the

than

temporal

do

the

retina

inferior

course

crossing

directly

bers.

back

Fibers

through

the

alignment

layer

is

along

so

the

precise

line

of

that

there

projection

is

that

a

gap

in

each

corresponds

contralateral

to

the

location

68

chiasm

ally

in

into

the

the

optic

chiasm,

tract.

whereas

Temporal

nasal

bers

bers,

are

even

located

aer

later-

crossing

of

the

are

the

are

layers

optic

same

disc.

site

in

us

the

the

visual

bers

eld

of

that

each

carry

eye

information

terminate

in

from

adjacent

54

more

centrally

spread

A

located.

throughout

small

posterior

number

of

the

Nasal

most

of

of

bers

chiasm

macular

the

and

bers

also

cross

and

chiasm.

have

been

enter

the

of

the

LGN,

right

next

to

one

another

(see Fig.

15.16).

e

bers course through the posterior limb of the internal capsule as

identied

that

exit

suprachiasmatic

the

they

leave

the

LGN

to

form

the

optic

radiations.

nucleus

in the hypothalamus. ese bers have a role in synchronization

62–64

of

circadian

Optic

As

the

Tract

bers

uncrossed

from

both

tralateral

tract.

ral

rhythm.

the

retinal

bers,

the

ipsilateral

from

bers

the

chiasm

nasal

the

and

lateral

crossed

in

intermingle.

superior

Fibers

occupy

leave

bers

superior

retina)

inferior

of

optic

temporal

retina

the

to

are

(the

and

nasal

between

con-

of

the

tempo-

retinal

e

and

bers

the

side

inferior

15.15).

located

crossed

medial

(ipsilateral

(Fig.

the

bers

retina

the

inferior

tract

uncrossed,

tract,

superior

move

contralateral

area

and

the

e

bers)

macular

these

two

groups. N G L

Lateral

Geniculate

Fibers

from

medial

aspect

nal

the

quadrants

composing

superior

the

LGN,

terminate

two-thirds

65

the

of

Nucleus

retinal

whereas

in

to

the

quadrants

bers

lateral

terminate

from

aspect.

three-fourths

of

the

the

A

in

inferior

dorsal

LGN,

the

reti-

wedge,

represents

66

macula.

Each

of

the

magnocellular

and

par vocellular

Striate

Lateral

Fig.

15.16

niculate

retina

Fig.

15.15

nerve

SP,

cortex

Medial

Coronal

bers

superior

in

the

section

optic

peripheral.

showing

tract.

IP,

the

inferior

orientation

peripheral;

M,

of

the

macular;

lateral

terminate

(nasal)

originate

in

the

Retinotopic

nucleus

in

in

layers

retina

place

in

representation

Fibers

2,

3,

terminate

neighboring

same

map

(LGN).

the

areas

and

in

of

striate

from

the

5.

layers

all

Fibers

1,

layers

cortex.

of

the

lateral

ipsilateral

4,

of

from

and

the

6.

ge-

(temporal)

the

contra-

Fibers

LGN

that

terminate

CHAPTER

Retinotopic

ose

bers

15

Visual

representation

that

are

adjacent

is

to

present

one

249

Pathway

in

the

another

in

striate

the

cortex.

layers

of

the

LGN project to the same area in the visual cortex (see Fig. 15.16).

at

is,

corresponding

temporal

and

get

visual

in

the

primary

visual

stimulus

in

an

presented

Optic

Optic

15.17

Location

hemisphere.

The

visual

into

Meyer

the

of

the

loops

occipital

optic

pass

radiations

into

the

chiasm

at

xation

tract

in

the

column

the

cells

same

retinas

neighboring

in

point

correspond

COMMENT: Visual

eld

is

tested

point

surrounding

the

temporal

a

cerebral

lobe

before

a

vertical

point

the

lobe.

of

and

Field

monocularly,

responding

xation

and

xation

nasal

The

that

line

a

column

in

to

the

an

(ipsilateral

the

same

locations

tar-

in

correspond

visual

eld,

adjacent

and

point

the

to

in

the

Testing

with

is

a

when

a

the

patient

target

point.

The

eld

can

horizontal

line

that

intersect

seen

by

the

fovea.

The

be

is

looking

seen

straight

divided

at

temporal

anywhere

into

the

four

point

eld

is

in

ahead

the

area

quadrants

of

xation.

slightly

larger

and

superior

reversal

eld

is

of

the

eld

imaged

on

are

the

caused

inferior

by

the

retina

optical

and

the

system

inferior

of

by

The

than

the

eld

eye.

on

the

Radiations superior retina. The nasal eld is imaged on the temporal retina and the temporal

e bers leaving the lateral aspect of the LGN, representing infe-

eld

on

the

nasal

retina

(Fig.

15.18).

This

orientation

is

maintained

in

the

cortex,

where the superior eld is projected onto the visual cortex inferior to the calcarine

rior retina, follow an indirect route to the occipital lobe. ey pass

ssure

into

the

temporal

lobe

and

loop

around

the

tip

of

the

and

where

the

inferior

visual

eld

is

projected

onto

the

cortex

superior

to

temporal the calcarine ssure.

horn

of

form

the

aspect

the

lateral

inferior

of

the

ventricle,

radiations

LGN,

forming

(Fig.

representing

Meyer

15.17).

loops;

Fibers

superior

these

from

retina,

lie

the

bers

medial

superiorly

as

The reader is cautioned to be aware of the difference between visual bers and

visual

elds.

Both

can

be

described

as

nasal,

temporal,

superior,

and

inferior.

they pass through the parietal lobe. e bers from the macula are The

visual

eld

seen

by

the

right

eye

is

nearly

the

same

as

that

eye

the

same

as

the

seen

by

the

left

generally situated between the superior and inferior bers. eye.

the

Striate

The

eld

seen

eld,

the

calcarine

radiations

by

of

the

the

other

eld

eye,

for

one

with

the

is

exception

of

the

far

temporal

temporal

part

of

peripheral

ssure,

terminate

in

called

the

the

region

cuneus

below

g yrus.

the

e

calcarine

inferior

ssure—

which

lingual

g yrus.

us

the

cuneus

g yrus

receives

is

called

the

temporal

crescent.

The

temporal

crescent

is

imaged

on

the nasal retina of one eye but not on the temporal retina of the other because the

depth of the orbit and the prominence of the nose blocks the periphery of the eld

from

imaging

scotoma,

the

part

Cortex

e superior radiations terminate in the area of the striate cortex

above

nasal

the

on

the

temporal

physiologic

retina.

blind

Within

spot,

a

each

result

of

temporal

the

lack

eld

of

is

an

absolute

photoreceptors

on

projections

the optic disc (Fig. 15.19).

from

the

retina.

the

the

and

retina

one-third

occipital

ssure,

of

superior

Only

lobe.

only

occipital

a

e

and

of

the

the

lingual

striate

majority

small

is

portion

posterior

g yrus

cortex

buried

is

on

the

is

from

on

the

the

within

inferior

surface

the

of

calcarine

posterolateral

aspect

Because

the

bers

that

emanate

from

the

nasal

retina

cross

in

the

chiasm,

the

postchiasmal pathway carries information from the contralateral temporal eld

and

the

ipsilateral

nasal

eld.

These

combined

areas

can

be

described

as

the

contralateral hemield (i.e., the right postchiasmal pathway carries information

pole.

from the left side of the visual eld for both eyes). Thus the left side of the eld

Fib ers

f rom

t he

mac ular

are a

ter minate

in

t he

most

p oste-

is

r ior

par t

of

t he

str iate

cor tex,

wit h

t he

sup er ior

mac ular

“seen”

by

the

right

striate

cortex,

paralleling

the

involvement

of

the

right

are a hemisphere in the motor and sensory activities of the left side of the body. Simi-

repres ented

in

t he

c uneus

g yr us

and

t he

infer ior

mac ula

replarly,

res ented

in

t he

lingual

g yr us.

e

mac u lar

proj ec t ion

objects

in

the

right

side

of

the

eld

are

“seen”

by

the

left

striate

cortex

mig ht (see Fig. 15.1). A defect that affects the nasal eld of one eye and the temporal

extend

onto

t he

p osterolatera l

sur face

of

t he

o ccipit al

cor tex. eld

e

mac ular

are a

repres ent ation

o cc upies

a

relat ively

of

of

str iate

cor tex

compared

wit h

t he

small

in

t he

retina.

e

mac ular

cells

are

dens ely

that

b ers

are

small

ca lib er.

B ecaus e

p acked,

mac ular

t he

of

shar p,

str iate

det ai led

cor tex

p er ipheral

is

retinal

vision,

more

t he

mac u lar

extensive

are as.

e

most

t han

cor tex,

t he

t he

p er ipher y

par t

adjacent

to

t he

anter ior

par iet a l

p ar t

of

lob e,

t he

st r i-

A

t he

nas al

retina,

cor resp onding

to

of

eld,

t he

temp or al

cres cent,

t hat

is

s een

by

visual

e ye

only.

of

to

the

the

left

left

eye.

side

of

the

Clinicians

visual

will

eld

refer

to

is

the

not

the

right

same

visual

as

eld

right

side

of

the

eld)

and

the

must

be

left

visual

eld

(meaning

the

left

eld).

eld

defect

of

just

one

eye

caused

by

a

disruption

anterior

to

in

each

prechiasmal

pathway,

or

there

is

a

single

lesion

in

the

chiasm

repres ents

an

are a

the

postchiasmal

t he

pathway,

where

the

bers

for

the

two

eyes

are

brought

of The

pattern

of

the

defect,

as

well

as

associated

contramight

lateral

the

the

together.

visual

eld

the chiasm. If there is a defect in the elds of both eyes, there are two lesions,

or

of

homonymous.

in

repres ent at ion

one

ate

as

and

repres ent at ion

t he

described

f unc t ion side

involves

is

reference

visual

(meaning

mac ular

eye

mac ular

the

are a

other

large

Note

p or tion

the

aid

in

determining

the

location

of

the

damage.

signs

or

a

cells

eld.

Inversion

Optic

All

to

two

represent

loops Optic

passing

at

project

the

that

radiations

Meyer

Fig.

nerve

will

from

nasal)

eld.

CLINICAL

Optic

eld

cortex.

adjacent

visual

points

contralateral

symptoms,

CHAPTER

250

15

Visual

Pathway

B

A

Fig.

15.18

retina.

B,

Orientation

Superior

eld

of

is

an

image

imaged

on

on

the

the

retina.

inferior

A,

Nasal

eld

is

imaged

on

the

temporal

retina.

The optic chiasm brings all the visual bers together. Lesions of the chiasm usually

will show bitemporal defects. The most common cause of a bitemporal eld defect

is

a

pituitary

gland

tumor,

and

a

visual

eld

defect

is

often

the

rst

clinical

sign

(Fig. 15.23). The crossed bers are generally damaged rst in compressive lesions,

54

such as a tumor, because of the large crossing angle of the bers.

bility

the

to

damage

medial

might

portion

of

also

the

be

attributable

chiasm.

to

the

Consequently,

purported

the

weak

crossed

This suscepti-

blood

bers

supply

also

are

of

more

48

susceptible to ischemia in a vascular event.

A

single

lesion

characterized

the

lesion,

This

Fig.

15.19

spot

Central

scotoma

in

visual

the

eld

showing

temporal

eld

of

the

physiologic

both

is

at

by

as

the

an

well

known

as

optic

overall

as

a

a

chiasm

and

depression

superior

junctional

its

in

junction

the

temporal

scotoma.

eld

defect

It

may

with

of

in

the

the

the

occur

optic

eye

on

eld

nerve

the

of

because

might

same

be

side

the

opposite

the

inferior

as

eye.

nasal

blind bers

are

located

bers

have

anteriorly

after

crossing

angle

relative

in

the

chiasm

and

because

the

nasal

eyes. a

large

crossing

to

bers

entering

the

chiasm

from

the

ipsilateral optic nerve.

A homonymous eld defect will be produced by a single lesion in the postchiasmal CLINICAL

COMMENT: Characteristic

Visual

Field

Defects

pathway, as the nasal bers of the contralateral eye join the temporal bers of the Fig.

15.20

depicts

The

regular

examples

of

various

visual

eld

defects.

ipsilateral

related

ber

with

a

orientation

specic

in

pattern

each

of

structure

visual

eld

of

the

loss.

A

visual

lesion

pathway

of

the

can

choroid

be

or

cor-

outer

retina will cause a eld defect that is similar in shape to the lesion and is in the cor-

responding location in the eld (e.g., if the lesion is in the inferior temporal retina,

sufcient

ent

on

eye.

for

the

Visual

20/20

side

accompanying

of

a

acuity

Snellen

the

eld

usually

acuity.

is

In

not

a

contralateral

homonymous

defect

affected

because

postchiasmal

to

can

the

help

lesion,

lesion.

the

one-half

the

Other

eld

signs

diagnostician

the

fovea

loss

or

is

is

pres-

symptoms

determine

more

exactly the site of the lesion.

the defect will be in the superior nasal eld). These lesions can cross the horizontal

A

lesion

involving

the

optic

tract

eventually

will

produce

optic

nerve

atrophy,

or vertical midlines (Fig. 15.21).

which

A

lesion

cation

in

the

and

nerve

ber

conguration

layer

of

the

will

cause

affected

a

eld

nerve

defect

ber

corresponding

bundle.

One

of

to

the

the

lo-

disease

processes that affects the nerve ber layer is glaucoma. It rst affects the temporal

nerve bers as they exit the globe at the superior and inferior optic disc. If temporal

retinal

the

bers

point

of

are

affected,

xation,

starting

nasal

meridian

(Fig.

nasal

step

results

and

an

15.22).

arcuate

at

This

from

the

the

defect

blind

abrupt

can

spot

edge

at

conguration

be

and

the

of

produced

terminating

horizontal

the

that

bers

at

curves

the

meridian

at

the

around

horizontal

is

called

temporal

a

Less

often,

a

lesion

affects

a

nasal

bundle

of

nerves,

producing

a

becomes

evident

as

optic

disc

pallor.

Because

the

optic

tract

is

relatively small in cross section, a lesion often damages all of the bers, causing a

homonymous eld defect that affects the entire half of the eld. If a partial hemi-

anopia

eld

the

results,

are

the

congruent

defect

shapes

defects

if

the

are

will

two

often

defects

dissimilar

be

are

(Figs.

incongruent.

similarly

15.24

and

Defects

shaped

15.25).

and

in

a

are

Because

homonymous

incongruent

crossed

if

bers

outnumber uncrossed bers, a lesion of the complete optic tract may be accompa-

nied by a relative afferent pupillary defect of the contralateral eye.

retinal

A raphe.

usually

lesion

in

the

LGN

will

affect

the

contralateral

eld

and

eventually

cause

optic

wedge-

atrophy. Because of the point-to-point localization in the LGN, lesions here produce shaped defect emanating from the physiologic blind spot into the temporal eld. 69

moderate to complete congruent eld defects.

Injury

to

the

optic

nerve

is

accompanied

by

a

visual

eld

defect,

a

relative

affer-

Damage ent

pupillary

defect,

and

atrophy

of

the

affected

nerve

bers,

which

eventually

the manifested at the optic disc.

to

the

optic

radiations

or

cortex

does

not

normally

cause

atrophy

of

is

optic

nerve

or

a

pupillary

defect

because

it

does

not

involve

the

bers

of

CHAPTER

15

Visual

Pathway

1 2

3

4

5

6

7

8 12

11

9

10

Fig.

15.20

Visual

eld

defects. The

visual

pathway

is

shown,

as

are

the

sites

of

interruption

of

ner ve

-

bers and the resulting visual eld defects. 1, Complete interruption of the left optic ner ve, resulting in com-

plete loss of the visual eld for the left eye. 2, Interruption in the midline of the optic chiasm, resulting in a

bitemporal hemianopia. 3, Interruption of the right optic ner ve at the junction with the chiasm, resulting in

complete loss of the visual eld for the right eye and superior temporal loss in the eld for left eye (because

of

contralateral

inferior

bers

traveling

anteriorly

in

the

chiasm). 4,

Interruption

in

the

left

optic

tract,

caus-

ing an incongruent right homonymous hemianopia. 5, Complete interruption in the right optic tract, lateral

geniculate

of

the

left

greater

right

in

a

ral

in

right

a

striate

Louis:

in

a

radiations,

involving

Interruption

hemianopia

congruous

cortex,

left

Mosby;

of

temporal

the

greater

in

a

left

of

in

9,

a

radiations

8,

hemianopia

12,

in

the

in

homonymous

incongruent

the

of

the

with

left

of

right

macular

WM

Jr,

posterior

of

all

bers

editor.

the

in

hemianopia.

right

parietal

bers

homonymous

Interruption

Hart

left

an

Interruption

Interruption

congruous

(From

total

causing

inferiorly.

bers

hemianopia.

crescent.

loop,

optic

homonymous

Interruption

homonymous

resulting

Meyer

hemianopia.

resulting

sparing. 1 1,

macular

sulting

optic

homonymous

right

crescent

left

7,

homonymous

right

or

radiations

superiorly.

total

sulting

the

nucleus,

optic

the

lobe,

left

in

the

Adler's

Interruption

right

hemianopia

incongruent

striate

Interruption

with

cortex,

an

radiations,

anterior

10,

hemianopia

striate

causing

optic

left

sparing.

6,

homonymous

macular

resulting

anterior

Physiology

of

in

of

a

re-

bers

and

striate

the

resulting

cortex,

in

tempo-

congruous

cortex,

Eye,

ed

9.

re-

St

1992.)

A

B

Fig.

the

that

15.21

left

Visual

eye

does

seen

not

eld

on

defect

fundus

respect

the

associated

with

autouorescence

horizont al

midline

a

(A)

(B).

retinal

lesion.

producing

a

Inferior

superior

temporal

nasal

retinal

visual

eld

scar

in

defect

251

CHAPTER

252

15

Visual

Pathway

Fig.

15.25).

Lesions

more

anterior

in

the

occipital

lobe

will

affect

more

peripheral

visual eld, whereas lesions more posterior will affect macular bers.

When

are

visual

association

involved,

rietal

lobe

carry

out

higher

can

areas

cortical

cause

agnosia

movements),

or

within

visual

the

occipital,

processes

(inability

aphasia

to

may

recognize

(difculty

with

temporal,

be

affected.

objects),

speech).

or

parietal

Lesions

apraxia

Temporal

of

lobes

the

pa-

(inability

lobe

to

lesions

can cause memory impairment, seizures, or aphasia. Injury involving the occipito-

70

temporal cortex can affect object and facial recognition.

Blindsight occurs when

there seems to be some sight in a hemield but there is no conscious awareness

of the sight. That is, a motor reex response can be elicited with the presentation

of an unexpected stimulus in the affected eld, but the patient has no awareness

of the vision. Connections between the LGN and the human motion area in the ex-

trastriate middle temporal cortex (V5), which bypass the visual cortex, are thought

71 72

to be involved in blindsight.

Striate

An

Cortex

early

study

Maps

correlating

the

visual

eld

to

the

striate

cortex

was

73

done

by

W orld

Holmes

W ar

I

and

and

Lister.

ey

attempted

to

studied

match

injured

visual

soldiers

eld

from

defects

with

injuries from shrapnel to the occipital lobe. e Holmes map pro-

Fig.

15.22

Automated

visual

eld

showing

an

arcuate

sco-

vided

toma

and

nasal

step

in

the

visual

eld

of

the

right

a

eld

the

in

eral

is

retinal

ganglion

homonymous

generally

temporal

cells.

eld

lesion

defect.

incongruent

lobe

A

involves

and

the

of

the

Because

may

Meyer

the

affect

loop,

optic

bers

only

a

radiations

are

one

superior

so

causes

spread

quadrant.

eld

If

defect

a

out,

a

will

source

the

defect

of

result.

in

striate

showing

pole

the

cortex.

forward,

anterior

e

the

representation

with

occipital

macular

the

lobe

portion

of

the

visual

periphery

and

the

of

extended

the

eld

uniocular

from

repre-

temporal

crescent in the most anterior aspect of the striate cortex adjacent to

contralat-

lesion

human

posterior

sented

the

detailed

eye.

the

the

parietooccipital

cortex

using

sulcus.

Detailed

electrophysiological

mapping

methods

of

a

monkey

revealed

striate

discrepancies

Pari-

between

monkey

and

human

data.

ese

ndings

suggested

that

41

etal

lobe

lesions

more

commonly

cause

inferior

eld

defects

(see Fig.

15.24).

either

The

characteristic

gruency

(carrying

site

of

depends

the

the

feature

on

same

lesion.

visual

As

of

how

the

a

defect

closely

eld

bers

in

bers

the

from

information)

reach

the

occipital

lobe

is

corresponding

are

positioned

occipital

lobe

and

to

congruency.

points

one

nally

of

another

the

at

striate

monkey

cortex

and

human

cortex

are

not

as

alike

as

believed or that the Holmes map required some modication.

Con-

each

the

T echnologies, such as MRI, have been used to study the human

eye

the

cortex,

allowing

more

direct

correlation

of

a

lesion

with

a

eld

74

cor-

defect.

Some

investigators

suggest

revision

of

the

Holmes

map.

tex, bers emanating from corresponding points in the eld come together to form

e

a

point-to-point

representation

of

the

eld.

Therefore

a

lesion

here

will

cause

primar y

macular

congruent

defect.

Injury

to

the

lingual

gyrus

will

cause

a

superior

visual

eld

change

concerns

the

extent

of

the

area

depicting

a

representation.

A

much

greater

area

of

the

visual

cortex

de-

is

thought

to

be

taken

up

by

macular

projection,

with

the

central

fect. Involvement of the cuneus gyrus will cause an inferior visual eld defect (see

30

A

degrees

of

the

visual

eld

represented

in

approximately

B

Fig.

15.23

imaging

the

Visual

with

eld

contrast

presenting

sign.

defects

showing

associated

a

pituit ar y

with

a

pituitary

adenoma

(A)

tumor.

causing

Sagittal

bitemporal

magnetic

visual

eld

resonance

loss

(B)

as

83%

CHAPTER

15

Visual

Pathway

B

A

Fig.

T2

15.24

Visual

magnetic

radiations

eld

resonance

(A)

resulting

defects

associated

imaging

in

a

left

showing

with

an

incongruous

a

lesion

involving

arteriovenous

homonymous

A

the

malformation

hemianopia

optic

radiations.

involving

the

right

Axial

optic

(B).

B

C

Fig.

15.25

resonance

cates

the

patient

the

Visual

level

of

involving

stroke

macular

eld

imaging

in

the

the

the

sparing

is

defects

(MRI)

axial

left

left

scan

associated

showing

scan

shown

anterior

lingual

caused

by

in

cuneus

gyrus.

the

a

The

second

with

stroke

B.

B,

Axial T2

gyrus.

right

occipital

involving

C, The

inferior

stroke

lobe

the

MRI

right

left

showing

superior

congruous

involving

lesions.

entire

the

left

a

A,

Sagittal

lingual

second

stroke

quadrantanopia

homonymous

anterior

T1

magnetic

gyrus. The

in

is

line

the

caused

hemianopia

cuneus

indi-

same

gyrus.

by

with

253

CHAPTER

254

15

Visual

Pathway

A

B

C

Fig.

15.26

Map

considerable

View

of

lines

ity

the

left

contours

occipital

along

the

2.5

cm

to

showing

the

illustrated

the

of

the

boundar y

right

image A

onto

the

the

of

the

line)

at

between

vertical

occipital

(D)

on

surface. The

lobe,

the

is

the

cortex

the

cortex

but

an

the

cortex.

the

occipital

B,

(V1)

and

pole

to

extend

of

ssure

is

the

by

in

cortex

located

specimens.

transposing

measuring

left

(running

usually

occurs

depicted

meridian

extrastriate

This

A,

Dashed

isoeccentric-

View

calcarine

that

cortex.

horizontal

mark

eld.

ellipse

emphasize

striate

striate

variation

cortex,

is

of

the

visual

shown,

visual

the

to

the

represented.

within

striate

of

of

lines

around

hidden

as

striate

vertical

fovea

the

left

important

exposing

wraps

meridian

is

location

representation

the

mostly

It

and

opened,

cortex

is

size

ssure. The

where

which

cortex.

exact

map. The

striate

hemield

a

eld

calcarine

The

striate

the

ssure

convexity,

(dashed

surface

visual

in

calcarine

cortex,

of

human

visual

of

lateral

striate

the

individuals

degrees.

the

medial

the

in

40

in

the

base

representation

exposed

of

with

the

onto

arrows). The

Projection

map

1

lobe

along

eld

among

coordinates

from

contains

visual

occurs

occipital

the

lobe,

between

C,

the

approximately

approximately

(V2)

of

variation

indicate

runs

D

the

approximately

2

80

×

40

folds

mm

with

around

situated

on

the

the

striate

cortex

region

of

the V4e

lar

of

the

of

lateral

receives

plotted

crescent

region

of

eld

in

with

in

the

to

a

is

C).

human

2500

small

convexity

the

visual

that

map

roughly

pole:

corresponding

isopter

visual

area

exposed

cortex

temporal

stippled

an

occipital

mapped

. The

row

the

cortex.

the

most

indicates

dots

lobe. The

of

the

ipsilateral

meridian.

Arch

dots

the

coordinates

perimeter. The

within

of

between

occipital

only

Horizontal

striate

the

eld

from

Goldmann

HM,

of

visual

input

mm

region

anterior

(From

Ophthalmol.

black

where

the

D,

oval

8%

to

Horton

the

eye's

visual

10%

of

the

blind

to

of

is

the

spot. This

the

striate

Hoyt WF . The

1991;109:816. With

cortex

region

hemield

corresponds

JC,

striate

representation

marks

Right

region

the

foveal

contralateral

eye.

stippled

and

shows

monocu-

cortex

(see

representation

permission.)

74

of

the

closely

15

striate

agree

degrees

of

cortex

with

(Fig.

the

vision

15.26).

Holmes

occupies

Other

map

37%

of

and

the

imaging

show

studies

that

surface

the

area

of

more

central

the

stri-

movements

of

examination,

at

least

3

1

to

the

2

degrees

area

degrees

for

spared

do

occur

within

macular

during

the

sparing

defect

to

be

the

visual

should

eld

involve

conrmed

clini-

75

ate

the

cortex.

lesion

Some

because

discrepancies

an

MRI

may

may

result

from

overestimate

the

the

nature

actual

of

area

cally.

the

Even

in

macular

the

presence

projection

of

area

an

extensive

might

remain

lesion,

some

unaected,

of

either

75

involved

when

edema

is

present.

because

the

extensive

Macular

Macular

Sparing

sparing

occurs

ers

when

an

area

of

central

vision

remains

the

a

ver y

size

large

and

76

within

a

homonymous

eld

defect.

B ecause

xational

eye

glion

posterior

blood

cells.

supply

area.

overlap

pole

or

of

Macular

of

the

because

the

occipital

the

sparing

receptive

lobe

macular

can

also

eld

of

has

such

projection

be

the

explained

retinal

an

cov-

by

gan-

CHAPTER

16.

AGING

WITHIN

THE

VISUAL

cell

death

occurs

SS.

throughout

all

structures

of

the

pressure.

Prog

although

the

extent

varies

signicantly

within

Jonas

Xu

JB,

18.

Age

is

accompanied

by

a

decrease

in

the

the

visual

eld,

caused

both

by

loss

of

cells

and

by

a

L.

Eye

optic

Res.

disc

edema

in

raised

intracranial

Histological

2016;50:108–144.

England).

changes

of

high

axial

myopia.

Eye

2014;28(2):113–117.

Jonas

JB,

Wang

N,

Y ang

D,

etal.

Facts

and

myths

of

cerebrospinal

extent uid

of

Retinal

the

77,78

population.

of

255

Pathway

visual

(London,

pathway,

Pathogenesis

Visual

PATHWAY

17.

Neural

Hayreh

15

pressure

for

the

physiolog y

of

the

eye.

Prog

Retinal

Eye

Res.

decrease 2015;46:67–83.

25,79

in

the

transparency

of

the

ocular

media.

e

ability

to

per19.

ceive

accurately

the

speed

of

moving

objects

declines

with

Caporlingua

and

and

animal

studies

have

identied

an

age-related

A,

Prior

A,

Cavagnaro

MJ,

etal.

e

intracranial

age,

dierence

in

cal

intracanalicular

windows:

optic

endoscopic

ner ve

versus

as

seen

through

transcranial.

dierent

World

surgi-

Neurosurg.

80

temporal processing speed at the level of the visual cortex.

decline

may

in

accurately

contribute

among

the

to

perceiving

the

elderly

higher

the

speed

incidence

of

of

moving

automobile

is

objects

2019;124:522–538.

20.

Liugan

M,

Xu

Z,

subarachnoid

accidents

Ophthalmol.

population.

21.

Kim

the

DH,

optic

ball

Zhang

space

M.

within

Reduced

free

the

canal

optic

communication

in

the

human.

of

the

Am

J

2017;179:25–31.

Jun

J-S,

ner ve

transverse

Kim

sheath

R.

Ultrasonographic

diameter

diameter

in

585

and

its

healthy

measurement

association

with

volunteers.

Sci

of

eye-

Rep.

REFERENCES 2017;7(1):15906.

1.

Hoyt

WF ,

pathway

2.

Polyak

S.

Chicago

3.

Jonas

the

e

L.

ber

Arch

Vertebrate

anatomy

in

Ophthalmol.

Visual

System.

the

infrageniculate

22.

Chicago:

count

University

ratio

of

Sadun

AA,

Tasman

AM,

and

Muller-Bergh

optic

disc

size.

JA,

etal.

Invest

Human

23.

optic

Ophthalmol

Vis

Jaeger

thalmolog y,

5.

Mikelberg

optic

R.

Visual

ed.

chiasm,

with

of

anitetski

M,

in

the

A,

axon

sensor y

M,

of

system.

Clinical

Kim

ASC,

tracts:

In:

MR

etal.

Eugene

e

normal

W .

T-W ,

Sharpe

domain

normal.

Cetković

M,

organisation

Weinreb

RN,

etal.

spectral-domain

J

of

the

Eye

Sanlippo

coherence

brane

PG,

Y ang

glaucoma

H,

of

Assist

and

coherence

Ophthalmol.

12.

Han

JC,

layer

Jonas

and

14.

a

Exp

15.

JB,

of

etal.

the

cal

27.

optic

ner ve.

S,

barrier

Ophthalmol.

Levin

olog y

LA.

of

S,

of

coherence

Optic

parapapil-

29.

Optic

the

Eye,

dis c

etal.

Dist r ibut ion

diameter

p opulat ion.

controls

with

anatomy

30.

Denison

of

patients

the

for

and

J

S,

etal.

Establishment

with

AJNR.

and

c up-to-dis c

Chin

Med

Assoc.

idiopathic

Optic

of

ner ve

norms

sheath

and

intracranial

compari-

hypertension

2012(2):366–369.

TA,

posterior

exact

DO.

RN,

Louis:

Arrigo

Ali

MH.

aspect

macular

J

of

A

restudy

the

buckling.

Vis

the

AT,

and

globe:

Retina

of

the

an

surgi-

essential

(Philadelphia,

Pa).

Elsevier ;

A,

Y acoub

St

Louis:

Mosby ;

Temporal

An

fMRI

1981.

frequency

study

of

the

corti-

E,

etal.

Functional

subdivisions

mapping

of

human

of

the

LGN.

2):358–369.

JM.

eds.

e

primar y

Adler’s

visual

Physiolog y

of

cortex.

the

Eye,

In:

10th

ed.

2003:669.

Calamuneri

Sci.

5.

etal.

humans:

par vocellular

Ichida

Alm

in

ed

H,

2011;11(8).

2014;102(Pt

V A,

Fields,

Strasburger

Vision.

Vu

PL,

A,

Visual

T,

processing

radiations

Párraga

e

Auer

areas.

Casagrande

of

spec-

A,

Mormina

connectivity

in

the

E,

etal.

human

New

insights

brain.

Invest

in

the

Ophthal-

2016;57(1):1–5.

RG,

optic

Ribas

GC,

radiation

Neurosurgery.

Ophthalmolog y.

etal.

Spectral-domain

characteristics

of

Bruch

population.

optical

31.

mem-

Am

Border

lamina

in

tissue

cribrosa

Brain

J

open-angle

morpholog y

defect

and

glaucoma.

S.

Tsukahara

optic

Peripapillar y

ring:

is

J

Welling

and

2012;71(1

LC,

related

Suppl

etal.

bers

Microsurgical

in

anatomy

3-dimensional

Operative):160–171;

images.

discussion

I.

Kuhnt

and

intermediar y

retina.

Graefe

In:

ed.

St

Kaufman

Louis:

PL,

Alm

A,

eds.

2003:603.

Adler’s

Physi-

JD,

DS,

Clark

revealed

CA.

by

Extrastriate

projections

fMRI-informed

in

tractography.

2015;220(5):2519–2532.

Lueck

specialization

Livingstone

and

Hockeld

Acad

Clin

35.

Elsevier ;

Funct.

Watson

neurons

tissue

1976;201(1):57–67.

ner ve.

Struct

S,

radiation

CJ,

in

etal.

A

human

direct

visual

demonstration

cortex.

J

of

Neurosci.

MS,

Hubel

depth:

DH.

anatomy,

Segregation

physiolog y,

of

and

form,

color,

perception.

move-

Science.

1988;240:740.

34.

Arch

Schwarzkopf

1991;11(3):641.

33.

histolog y

2014;92(4):e273–e279.

ner ve

I,

optic

functional

deep-

Am

Zeki

ment,

Ophthalmol.

M,

Alvarez

human

32.

etal.

focal

dropout

the

10th

Constantini

controls.

chromatic

optic

tomogra-

margin

L,

imaging:

El-Mamoun

DV ,

visual

mol

disc

Australian

Panda-Jonas

Ohkuma

between

H,

Kaufman

Vojnos-

2019;203:89–102.

L,

AL

magnocellular

28.

Morphometric

Dierentiation

tomography.

adult

DY ,

with

Acta

healthy

D’Souza

St

normal

Y azar

young

Park

Holbach

correlations.

Okinami

as

E,

microvasculature

Ophthalmol.

13.

JH,

associated

MR

pediatric

Harrington

Tomo-

2016;165:154–163.

Choi

spatially

a

Y-C,

171–172.

Huynh

in

Ko

optic

C hines e

Ben-Sira

on

26.

optic

between

B,

anatomy

and

the

comparison

Comput

optical

etal.

tomography-derived

opening

of

elderly

25.

2012;119(4):738–747.

11.

CJ-L,

2011;31(7):1405–1411.

Ophthal-

2013;120(9):1790–1797.

GP ,

optical

an

topography

human

1976:325–395.

Dimensions

quantitative

and

Anatomy

of

Siam

cal

distribution.

Wol ’s

Saunders;

24.

2015;72(2):132–135.

using

L iu

fac tors

NeuroImage.

Z,

fascicular

with

Shoy

with

In:

Oph-

1994.

diameter

Kucharczyk

atrophy

Vitosević

Pregled.

patients

tral

and

Ophthalmolog y.

Reis

Lippincott;

Philadelphia:

optic

M,

atrophy

phy.

visual

Foundations

1993;17(5):688.

Radunović

Kim

the

Schulzer

and

pathway.

Toledo

lar y

of

Duane’s

SM,

count

JG,

analysis

10.

Drance

Axon

7th

graph.

eds.

Philadelphia:

Orbit,

patients

9.

Anatomy

Parravano

ner ves,

8.

1.

JS.

EA,

1989;96:1325.

War wick

and

7.

FS,

ner ve.

molog y.

6.

vol

in

diameter

Sci.

son

Glaser

W ,

T-M,

2014;77(4):203–208.

2012;33(6):1992.

4.

Kuang

ass o ciated

1962;68:124.

1957.

Schmidt

ber

Visual

primate.

Press;

JB,

ner ve

Osman

of

Sci

S,

Tootell

reveal

USA.

an

Hubel

DH,

geniculate

J

Zaremba

of

S.

Molecular

human

dierences

visual

cortex.

among

Proc

Natl

1990;87(8):3027.

lateral

monkey.

RB,

organization

Livingstone

body

Neurosci.

MS.

and

Color

and

primar y

contrast

visual

1990;10(7):2223.

sensitivity

cortex

in

the

in

the

macaque

CHAPTER

256

36.

Silverman

abnormal

sion.

37.

SE,

in

Invest

Horton

Trick

15

GL,

primar y

JC,

Dagi

LR,

Hart

Jr

Vis

Sci.

McCrane

columns

in

Pathway

WM.

open-angle

Ophthalmol

dominance

Visual

Motion

glaucoma

perception

and

ocular

is

58.

hyperten-

1990;31(4):722.

EP ,

human

etal.

visual

Arch

of

ocular

59.

Ophthalmol.

Lachica

and

EA,

retinal

primate

39.

Press).

Casagrande

axons

lateral

V A.

ending

on

geniculate

e

morpholog y

small

relay

nucleus.

Vis

of

(W-like)

Neurosci.

collicular

cells

of

60.

the

1993;10(3):403.

Boyd JD, Matsubara JA. Extrastriate Cortex. In: Kaufman PL, Alm A,

Catani

tions

41.

M,

in

Horton

Adler’s

42.

Wurtz

JC.

e

RH.

J,

visual

Donato

brain.

central

of

Vision

Invest

Blumb erg

s ee:

DK,

human

Physiolog y

Lecture.

43.

Jones

the

visual

the

for

Eye,

the

G.

recognition

etal.

pathways.

9th

Vis

ed.

t he

of

Sci.

How

in

Occipito-temporal

2003;126(pt

control

Ophthalmol

Kreiman

R,

Brain.

St

In:

Hart

connec-

the

Jr,

ed.

63.

neurons

brain.

J

Kravitz

an

Saleem

expanded

ity.

45.

DJ,

Trends

Jonas

JB,

with

neural

SB.

arterial

secondar y

CI,

Sci.

etal.

for

e

the

help

Clin

ring

of

64.

us

65.

Invest.

ventral

processing

visual

of

pathway :

object

Zinn-Haller

angle-closure

of

qual-

in

circular

normal

glaucoma.

Acta

eyes

peri-

MacKenzie

Can

47.

J

Lao

Y ,

optic

Cio

Ophthalmol.

Francoisa

pathway.

48.

PJ,

J,

and

eyes

Brit

Gao

J

H,

chiasma

Vascular

anatomy

of

the

optic

68.

ner ve

A,

Collette

Ophthalmol.

Zhong

and

Y .

JM.

head.

of

the

optic

1958;42:80.

Vascular

bitemporal

70.

architecture

hemianopia.

of

the

Chin

human

Med

Sci

Salaud

blood

C,

J.

71.

supply

to

S,

the

Bler y

optic

P ,

etal.

Extrinsic

chiasm.

Clin

Anat

and

intrinsic

(New

Y ork,

Luco

C,

Hoppe

vascular

lesions

Psychiatry.

51.

Ogden

N.Y .).

72.

TE.

Ballantyne

Kupfer

optic

Jain

the

lateral

ber

Invest

AJ.

e

M,

etal.

Visual

geniculate

eld

body.

J

defects

Neurol

Soc

the

Ophthalmol

UK.

optic

of

ber

macaque

Vis

Sci.

pattern

retina:

in

the

Neurosurg

retina.

Downer

tract,

and

J,

Trans

lateral

Quantitative

geniculate

Jain

orientations

image

SV ,

histolog y

nucleus

of

man.

of

in

the

ana ly s is .

X,

etal.

human

Inv e s t

Visualization

optic

chiasm

O p ht h a l m o l

Vi s

of

using

S ci.

ner ve

J

Lee

JH,

Surg

56.

Neurol.

with

of

the

optic

S,

Kwon

J-T,

etal.

2006;66(1):11–17;

Zweckberger

tion

ber

K,

Unterberg

optic

ner ve

ner ve

can

sheath

Alvarez-Fernandez

S,

etal.

Junctional

Oalmol.

Malpeli

AW ,

save

Wilbrand’s

discussion

Schick

U.

does

it

JG,

lateral

Louis:

Clin

Neuro

I

in

D,

transec-

scotoma.

A

2019;94(9):445–448.

case

C,

report.

patients

Ferreira

Neurosurg.

Soc

Espanola

J

prechiasmatic

NR,

J

optic

Ophthalmol.

etal.

ner ve

2000;129(6):

Wilbrand

projection

in

in

knee.

Neurol-

mammals:

ganglion-cell

retina.

of

In:

a

com-

photoreceptors.

the

macula

J

J,

editor.

e

2006:195–252.

in

the

lateral

geniculate

1962;54:597.

Variability

body.

Fischbarg

Elsevier ;

Ophthalmol.

RW .

Baker

FH.

geniculate

V A,

PL,

e

body

Ichida

Alm

Elsevier ;

A,

Braga

A,

of

laminar

Comparat

patterns

Neurol.

in

the

1979;

representation

of

of

the

Macacamulatta.

J

visual

elds

Comparat

in

Neurol.

FM.

Balcer

Anatomic

LJ.

Ajina

S,

Bridge

PLoS

Ajina

S,

Biol.

geniculate

Physiolog y

of

nucleus.

the

Eye,

In:

10th

ed.

review

and

Am.

the

of

the

topographic

anterior

(abstract).

diagnosis.

2001;14:1.

Blindsight

and

anatomy

1990;48(4):448

relies

lateral

on

a

functional

geniculate

nucleus,

connection

not

the

pulvi-

2018;16(7):e2005769.

Pestilli

by

lateral

Neuro-Psi.

North

H.

hMT+

e

Adler’s

Microsurgical

Arqu

Clin

JM.

eds.

2003:655.

arter y.

Holmes

G,

F ,

an

Rokem

intact

Lister

with

Horton

A,

etal.

Human

blindsight

geniculo-extrastriate

JC,

Wong

WT.

special

Brain.

pathway.

is

ELife4.

WF .

cortex.

AM,

Sharpe

occipital

J,

Sci.

cells

the

of

vision

cortical

from

cerebral

representation

of

the

JA.

representation

Ophthalmol.

Representation

a

Arch

magnetic

in

a

the

of

the

S.

visual

visual

resonance

Ophthalmol.

humans:

of

eld

in

hu-

1991;109:816.

eld

imaging

in

the

and

peri-

1999;117(2):208.

Nasotemporal

functional

study.

overlap

Invest

of

reti-

Ophthal-

2003;44(4):1568.

Samarawickrama

normal

to

Trauzettel-Klonsinski

ganglion

Vis

e

Arch

cortex:

correlation.

Reinhard

Disturbances

reference

1916;39:34.

Hoyt

striate

Hirose

T,

editors.

optic

C,

Hong

ner ve

Katsumi

Principles

Saunders;

Shehadeh-Mahmalat

Arch

e

geniculate

electrophysiologic

79.

Rodriguez-Balsera

mul-

(Aeolus

T,

head

Jonas

JB,

etal.

parameters.

Measurement

Surv

Ophthalmol.

2012;57(4):317–336.

78.

vision

B.

Am

choroidal

mol

77.

exist?

17.

Pre-chiasmatic

contralateral

meningioma.

knee:

glioblastoma

Neuro-Ophthalmolog y

Am

Amsterdam:

Guiller y

Casagrande

nal

photomicrographic

2015;56(11):

2013;115(12):2426–2431.

57.

lateral

of

Tobias

Multicentric

1973;49:403.

projection

man.

TL,

metric

6734–6739.

55.

e

of

Hickey

human

76.

Wang

Ophthalmol.

2007;454:849–855.

Eye.

human

man

75.

etal.

Harris

Res.

Ehinger

the

C.

macula.

74.

human

1967;101:393.

NS,

73.

retinotopic

1946;66:179.

L,

J

2015.

1983;24:85.

of

the

Phototransduction

M,

of

Kupfer

lesions

layer

ner ve

Chumbley

ner ve,

Anat.

54.

C,

Schweitzer

of

Ner ve

Ophthalmol

53.

M.

mediated

1992;55(1):12.

organization.

52.

A,

of

scotoma.

RA,

Brain

Physiol.

Cour

nar.

2018;31(3):432–440.

50.

La

J

between

Ploteau

C.

neuritis.

Retinohypothalamic

study.

Ophthalmol

1994;9(1):38.

49.

Cercato

optic

junctional

RY .

Berson

St

69.

Vascularization

AG,

Qureshi

Kaufman

G.

prechiasmatic

Am

1975;161:569.

Ophthalmol.

2008;43:308–312.

Neetens

Moore

the

2010;88(8):e317–e322.

46.

the

183:221.

67.

the

Lee

Compression

a

RK,

nucleus

2013;17(1):26–49.

Histomorphometr y

of

scotoma.

2014;82(5):459–460.

Euro

66.

Baker

framework

Cognitive

Jonas

papillar y

KS,

Shin

Biolog y

2010;120(9):3054–3063.

44.

62.

1992:728.

Friedenwald

F ,

JC.

parative

WM

Mosby ;

movement:

cor tical

Compression

junctional

2018;42(2):112–116.

Horton

og y.

1996;37:2310.

human

DM.

a

826–828.

61.

9):2093.

Louis:

Jacobson

produces

mimicking

produces

eds. Adler’ s Physiology of the Eye, 10th ed. St Louis: Elsevier; 2003:686.

40.

Pellegrini

tiforme

1990;108(7):1025.

38.

N,

ner ve

1999;128(2):256–258.

Arrangement

cortex.

Karanjia

optic

Trobe

to

80.

JD,

Testing

Functional

changes:

measurements.

and

Practice

of

In:

psychophysical

Albert

DM,

Ophthalmolog y.

and

Jakobiec

FA,

Philadelphia:

1994:728.

Glasser

and

Mendelson

Vision

O.

Res.

JS.

e

Visual

Inter pretation.

JR,

Wells

EF .

2002;42:695.

Field

Manual:

Gainesville,

Age-related

Fla:

changes

A

Practical

Triad;

in

the

Guide

1983.

visual

cortex.

I N D E X

Page

references

followed

by

“f ” indicate

gure, by

“b” indicate

box, and

Alzheimer

A

A17

amacrine

cells, branching

cells, 127

A18

amacrine

cells, wide-eld

amacrine, 127

Amacrine

AII

Abducens

ner ve, 181

ganglion

sagittal

Accessor y

of

direction, 126

radiation, 47

glands, 21 f, 21–22, 24

Y

Anterior

zonular

suture, 100, 101f

insertion, scanning

Antiangiogenic

factor, production, 122

Apsulopalpebral

release, 124

AMD. See Age-related macular degeneration (AMD)

AQPs.

Amorphous

Aquaporin

ground

fascia

substance, components, 6

See

Aquaporins

channel

Krause, 16, 17f

Anatomic

directions, 1, 3f

Aquaporins

Wolfring, 16, 17f

Anatomic

planes, 1, 3f

Aqueous

chambers, 82

Anchoring

point

reaction

(near-

reaction), 228

(AQPs), 6–7, 44

Aqueous

deciency, 25b

Aqueous

humor, 1

Anisotropic

Aqueous

layer, tear

Aqueous

outow

Annulus

Acetylcholine, 227

of

brils, 38

Zinn

(A

band), 175

(common

tendinous

ring),

167–168, 179

Actin

lm, 23–24

impedance, PAS

Antagonist

myobrils, 175f

Antagonists

myosin

Anterior

(anatomic

Anterior

blepharitis, 22b, 23f

Anterior

border

Anterior

chamber, 1, 82, 153

Arteries, radial

chambers, 89

Arterioles, formation, 150–151

Actin

laments, sets, 175

Action

Active

potential, impact, 6

transport

Adenosine

mechanisms, energ y

triphosphate

usage, 6–7

(ATP), myosin

light

molecules, 46

agonists, actions, 228 f

Adrenergic

antagonists, actions, 229 f

Adrenergic

bers, 227

Adrenergic

neuromuscular

agonist

junction, adrenergic

pathway, 208

accommodation-convergence

reaction, 229

pupillar y

defect, 232b

Aerent

pupillar y

light

pathway, visual

pathway

cataracts, 106f

Age-related

cortical

Age-related

macular

78–7 9,

d e gen e r ati on

( AMD ),

nuclear

Age-related

vitreal

angle

Astrocytes, 6, 119

cataract, 107

changes, 92

Aging

Automated

section, light

micrograph, 83 f

visual

musc le

bers, ganglion

ciliar y

Autonomic

ner vous

branches, 200f

Autonomic

neurotransmitters, action

branching, 200

Autonomic

pathway, 222

rectus

Autonomic

responses

arteries, 200

muscles, relationship, 197 f

ciliar y

veins, 205

agents

epithelium, 64

(proliferation), 153

eye, vitreous

Anterior

iris

epithelial

contraction

knees

of

optic

neuropathy, 198

cell

Basal

cells, 46

Basal

lamina, 4, 31

Bruch

W ilbrand, 247–248

membrane, 77

Basement

membrane, 4

changes

in

uvea, 79

Anterior

lens

capsule, light

Anterior

lens

epithelium, light

Anterior

limbal

(tapering), 59

Benign

Anterior

scleral

Bergmeister

Anterior

segment, peripher y, 82 f

AII

cell

(drugs), 228

(amacrine

All-trans-retinal

Altered

macrophages, 62–63

interruption, 77

micrograph, 98 f

micrograph

of,

98, 98f

cell), 118

isomer, formation, 125

loops, 209

layer, 31, 35f

lamina, 37–38

muscles, 188

sites, 227 f

(alteration), pharmacologic

ner ve

Basal

Anterior

Agonists

chart, 223 f

B

portion, 66f

surface, 65

Anterior

exit, 226

system, ow

myelination, 154

layers, position, 65

ischemic

pathway, 222

relationships, 90 f

folds, 66

Anterior

nasal

Axons, 6

continuation, 64

Anterior

and

(impact), 227

Axenfeld, scleral

aspect, myolaments

eyelids, 26

Agonist

scotoma

eerent

in

manifestations, 105

eld, arcuate

step, 252f

changes

clinical

antagonist, 228

diseases, 25b

Autonomic

epithelial

79f

Age-related

impact, 106–107

Autonomic

apical

cataract, 107

Ascorbate, 47

(relationship), 197f

basal

(parallelism), 229

Age-related

(impact), 82

Astigmatism, 30, 32f

choriocapillaris, ciliar y

Anterior

indication, 231f

Aerent

meshwork

branches, 69f

Autoimmune

Anterior

disruption, 231

eld, 252 f

dissociation,

232

Atropine, adrenergic

Anterior

yield, 7

decrease, 89

visual

pupil, light-near

structure, 82

Anterior

nucleus, 100

Robertson

layer, iris, 62

chamber

structure, determination, 97

Aerent

Arg yll

production, age-related

scotoma, automated

inclusion, 63f

transverse

glycolysis, ATP

Arcuate

importance, 84

actions, 228f

lens, 101f

Aerobic

Aqueous

direction), 1

micrograph, 63f

Anterior

cortex, 101f

Adult

(drugs), 228

lining, 154

Adrenergic

Adult

system, 83f

circumference, trabecular

attachment, 176

Adhesion

aging

muscles, 188

(impact), 65

insolubility, 104

junction, breakage, 176

aponeurosis),

(AQPs)

Anisocoria, 233, 233b, 237f

band

eyelid

proteins, changes, 106–107

of

Accommodation-convergence

(lower

14–15

of

Accommodation, 1, 71

electron

Apoptosis, occurrence, 155

Amacrines, glycine/GABA

ultraviolet

lacrimal

synechia, occurrence, 65

Anterior

micrograph, 102f

types, description, 118

section, 213f

stroma, 35f

Anterior

cells, dierentiation, 147

relays, 126f

nucleus, 217

Absorption

body, 118

information, horizontal

pathway, 217

Abducens

Anterior

cell, 118

cell

VI, 217

table.

disease, 135

damage, 218b

ner ve

“t” indicate

cells, 118

Abducens

cranial

by

layers

Basilar

boundar y, Descemet

foramen, 54

membrane

of, 77f

RPE, 77

Bays

Beta

arter y, vertebral

branches, 241

processes, 72f

anisocoria, 233

papilla, 146b, 147f

proteins, stabilization, 104

257

Index

258

Biomicroscope

Carotid-cavernous

sinus

examination, 57b

Carotid

usage, 4

Caruncle, 10, 57, 57f

Biomolecules, impact, 104

Bipolar

axons, IPL

Bipolar

cells, 115

aerent

membrane, 126

Cation

Caudal

signal, 117–118

neuron, 115

visual

pupillar y

vessels, inner vation, 76

channels, closure, 125

(anatomic

Cavernous

synapse, 120

eld

Choroidal

blood

supply, drawing, 76 f

Choroidal

blood

vessels, parasympathetic

coronal

loss, 250, 252 f

inner vation, 243

cross

direction), 1

sinus, 205

section, 205f

thrombosis, 205

Blood-retinal

wall, trochlear

barrier, 133

supply, 190

Cavernous

sinus

ner ve

Choroidal

neovascularization, 78, 78 f

Choroidal

nevus, 76, 77f

Choroidal

stroma, 75

characteristics, 75

section, 213f

Blepharitis, 22b, 23f

Blood

defect, 232b

surger y, 108

neural

Bitemporal

melanocytes, 75–76

tissue, absence, 144f

physiolog y, 106

migration, 147–148

dendrites

characteristics, 75

formation, 105

information, transfer, 126

Bipolar

stroma

Cataracts, 105–106

termination, 126

dendrites, plasma

second-order

stula, 205

plexus, bers, 222

(entr y), 217

involvement, 217

Choroidal

tissue, absence, 144 f

Choroidal

veins, 75–76

Choroidal

vessels, 76f

blood

ow, 202

cornea, 43

Cell

body, 114–115

of

Cell

cords, palisade

increase, 200

Cell

division, cessation, 143–144

Chromatic

inner vation, relationship, 190

Cell

membrane, 6

Chromophore, photon

eyelids, 22, 24f

to

uveal

Blood

tract, 79

vessels, 22

evidence, 134f

peripher y, 60

aberration, reduction, 128

composition, 6

Chromosomes, 6

uid/solute

Cilia, 11

transport, 6–7

absence, 103

outer

fundus

surface, ridge-like

view, 134b

inner vation, 76

leaet, contact, 7–8

elevations

conditions

(fusion), 7–8

Cilia

absorption, 124

aecting, 11b

(cilium), 114

permeability/barriers, 156

Cell

migration, 46

Ciliar y

arter y, branch, 194–195

sympathetic

Cell

mitosis, location, 98

Ciliar y

body, 1, 62, 79, 151

Cell

proliferation, 46

Blow-out

Blue

fracture, of

cone

Blunt

Body

inner vation, 239f

bipolar

right

cell

orbital

oor, 165 f

synapses, 116

Cells/rods

trauma, 62

Cell

layer, 32, 35f, 46

appearance, 151

Brain

view, 142f

sagittal

Brown’s

Brown

Bruch

processing, occurrence, 208

section, 213f

syndrome, 187f

superior

oblique

membrane

choroid

sheath

(basal

syndrome, 187

lamina), 77, 79 f

section, 111

anterior

Cellular

cytoplasm

Cellular

metabolic

Cellular

organelles, 103

partitions/layers, 71f

functions, 7

section, 200f

supraciliaris, 69

transverse

reex, 129b

meniscus

Central

ner vous

Central

retina, 128

layers, light

Central

retinal

production

of

zonule

Kuhnt, 241 f

system

(CNS), disruption, 232

arter y, 132, 195, 204

cortex, medial

radiations

(location), 249f

Chalazion, 22b, 22f

conjunctiva, 56

Characteristic

examination, 57 b

Chemical

epithelial

Ciliar y

epithelium

visual

layers, light

(ciliar y

micrograph, 75 f

epithelia), 73

micrograph, 75f

(inhibition), drugs

(usage), 88

ganglion, 181

characteristics, 224

surface, 244 f

hemisphere, optic

micrograph, 73 f

bers, 69

Ciliar y

Ciliar y

vessels, atrophy, 153

Cerebral

bipolars, 116

section, light

Central

Cerebral

presence, 76f

aspect, 72f

muscle, 73f

foveal

Central

biomicroscopic

inner

bers

Central

elastic

Bulbar

layer, 63 f

(cytosol), protein

volume, regulation, 104

development, 151

Brush

border

branch, 195

sheet, presence, 151

layers, 111

inclusion, 63f

Cellular

Cell

division, 69

epithelial

(presence), 6

termination, 59, 83f

lateral

(3D

stability, 8

emergence, 152f

information

segments), relationship

drawing), 113f

structures, tissues, 4

Bowman

(outer

components, 73f

damage, 233–234

Ciliar y

muscle, 70

components, 73f

eld

defects, 250–252

contraction, 103

synapses, 124

impact, 72

–

Chlorine

(Cl

Cholesterol

)

ux, importance, 104

molecules, impact, 6

inner vation, 70

longitudinal

bers, contraction, 72

C

Cholinergic

agonists, actions, 229 f

parasympathetic

Cadherins, 8

Cholinergic

antagonists, 228

presence, 73f

Calcarine

Calcium

ssure, 243–244, 249

ion

channels, vesicle

fusion

actions, 229f

facilitation, 124

Cholinergic

bers, 227

Canaliculi, 25f, 25–26

Cholinergic

neuromuscular

Canal

of

Hannover, 89

Choriocapillaris, 76

Canal

of

Petit, 89

basement

Canal

of

Schlemm, 73f, 83

fenestration, 133–134

inclusion, 63f

lumen, presence, 55f

Canthal

tendons, 16

relaxation, 102–103

Ciliar y

junction, 229 f

membrane, interruption, 76–77

network, 132

ner ve

choroidal

Ciliar y

processes

anterior

Ciliar y

network, 76f

Cilioretinal

blood

supply, drawing, 76f

retina

Bruch’s

Capillar y

blood

extension, 75

Circle

of

Capillar y

networks, formation, 130

functions

Circle

of

Capillar y

system, 197f

inner vation, 76f

Capsulopalpebral

Carbonic

fascia, 14–15

anhydrase

inhibitors, usage, 88

layers, histolog y, 75f

posterior

termination, 241f

arter y, 198

entr y, 133

Circadian

beds, formation, 150–151

of, 77

view, 72f

stroma, 70

Capillar y

ow, measurement, 127–128

membrane, 111

entr y, 76f

location, 224

function, maintenance, 122

Choroid, 1, 62, 75, 80, 151

Capillaries, peripapillar y

inner vation, 226 f

rhythm, 123

wake/sleep

cycle, 117

iris, 197f

W illis, optic

chiasm

242f

Circle

of

Zinn, 195–198

formation, 151

(relationship), 241,

259

Index

Circular

furrows, iris, 72f

Connexins, proteins, combination, 9

Circular

receptive

Contact

lenses, 42

Contact

L ens

Cloquet ’s

eld, 127

canal, 91, 91f

formation, 154

Clump

Coats

cells, 62–63

(tunics), 1

Wear, 16b, 17f

Corneal

stromal

Corneal

surface, evaluation

Contralateral

hemield, 249

Corneal

touch

Contralateral

inferior

Corneal

wound

nasal

retinal

bers, 248

Bowman

Cornea, 1, 30, 151

test, 237f

anatomy

Collagen, 92

stroma, 33

precursor, 152f

Contraction, initiation, 227

Cocaine

impact, 228

Corneal

and

Bowman

descemet

histolog y, 30

lamellae, 33, 36 f

of, 30

reex, 227f

repair, 46

layer, 46

membrane, 47

endothelium, 47

layer, 32, 35f

epithelium, 46

bands, sclera, 75

descemet

bers, 6

endothelium, 38, 40f, 41f

Corneoscleral

junction, 59

brils, 56

epithelium, 30

Corneoscleral

meshwork, 82

inner

stroma, 33

Corneoscleral

trabecular

core, 82–83

separation, 6

Collagen

brils, 33

Coloboma, 141b

keyhole

Color

appearance, 144f

vision, area

Columnar

Common

basal

(occupation), 123

cells, 31, 35f

tendinous

ring

(annulus

membrane, 37, 39f, 40f

appearance, 30

Corona

blood

Coronal

supply, 43

of

Zinn), 167–168

ciliaris

Corrugator, 10

central

Cortex

clinical

region, development, 152 f

aging

changes

in, 48

(pars

(anatomic

branches, radiation, 208

composite

cur vature, impact, 3

Cones, 115

stroma, 46

sheets, 85 f

plicata), 69

plane), 2

drawing, 99f

thickness, 103

dimensions, 30

Cortical

functions, 44

cataract, 106

spokes, visibility, 107f

body, 113

absorption

Cortical

regions, activity, 244

cilium, 114

corneal

hydration, 44

Cortical

subcapsular

composition, 113

corneal

metabolism, 45

Cranial

(anatomic

inner

ber, 114–115

corneal

wound

Cranial

cavity

inner

segment, 114

epithelial

Cranial

ner ve

damage, 215

inner vation, 42, 42f, 210f

Cranial

ner ve

III

(oculomotor

layers

Cranial

ner ve

III

palsy, 216f

(trochlear

shape, 115

morpholog y, 115

of

cell

ultraviolet

radiation, 47

repair, 46

replacement, 46

changes, 106 f

direction), 1

(posterior

oor), formation, 159

outer

ber, 114–115

presence, 151

Cranial

ner ve

IV

outer

segment, 113–114

visualization, 4

Cranial

ner ve

VI, abducens

Cranial

ner ve

VII, facial

Cranial

ner ve

VI

membranous

discs, 114f

physiological

aging

renewal, 115

refractive

shortness, 115

removal, 102f

pedicle, 116f

shape, 30

population

stroma

discrimination, 123

increase, 148–149

touch

Congenital

Horner

Cranium

venous

sinus

Cribiform

reex, 227f

drainage, superior

Cr ypts, 65–66

absorption, 105

Cr ypts

of

Henle, 19

Corneal

avascularity, 43

accommodation, 102

Corneal

dimensions, 31f

aging

Corneal

edema, 45

Corneal

endothelium, formation, 151

caruncle, 57

Corneal

epithelial

formation, 155

Corneal

236f

Conjunctiva, 1, 56

blood

vessels, 58

inner vation, 58

basal

lymphatics, 58

cell

middle

layer, wing

plica

surface

layer, 30

stromal

vessels, presence, 55f, 83f

layer, 33 f

clinical

cells, 31

manifestations, 105

capsule, 97

transparency, 97

composite

cells, 31

partitions, 57f

lens, 1

changes, 105

layer

columnar

semilunaris, 57

Cr ystalline

epithelium, 30, 34f

cell

drawing, 99f

cur vature, 103

development, protein

manufacture, 104

dimensions, 97

Corneal

erosion, 31b

divisions, 100

Conjunctival

concretions, 19b, 20f

Corneal

broblasts, 35

elliptic

Conjunctival

fornix, 56

Corneal

guttata, 39b

embr yologic

Conjunctival

goblet

Corneal

hydration, 44

epithelium, 98

Conjunctivitis, 58b

Corneal

injur y, 46

Connecting

Corneal

integrins, 46

glucose, collection, 104

Corneal

lamellae, 33, 37f

histolog y, 97

Corneal

layers, 32f

location, 1

derivation, 155

Corneal

metabolism, 45

metabolism, 104

bers, components, 6

Corneal

neovascularization, 43, 43 f

physiolog y, 103

septa, 178

Corneal

ner ves, 33

slit-lamp

Corneal

opacity, 37

sutures, 100

Corneal

reex, 220b, 227b

Corneal

reshaping, 47–48

Corneal

sensitivity, 42

Connective

circular

cells, 23–24

stalk, 114

tissue, 5

band, 167–168

muscle

connection, 178

sleeves/pulleys

(identication), MRI

(usage), 177–178

sheath, 240

system

cross

section, anterior

orbit, 178 f

cross

section, midorbit, 179f

structure, 97

ber

vascular

Cr ystalline

development, 97

interface, 100

appearance, 100

supply, absence, 99–100

lens

bers, 98

components, 104

assessing, 42

cytoplasm, protein

loss

formation, 104

of, 43

Corneal

sensor y

view, 206 f

plate, 162

arcus, 48, 48f

heterochromia,

ner ve, 219

palsy, 219f

Corneal

syndrome, iris

ner ve), 216

ner ve, 217

bones, 159

wavelength

cataract, 145b

in, 48

(impact), 3

precursor, 152f

synapses, 116f

Congenital

changes

power, cur vature

ner ve), 213

inner vation, 208

concentration, 99

production, continuation, 98

Index

260

Cr ystallins, 47, 99

aggregation, 104

Cuneus

g yrus, projections, 243–244

Cup-to-disc

ratios, variability, 132 f

Cyclopentolate, adrenergic

Eerent

bers, 208

Eerent

parasympathetic

Eerent

pathway, 213

pathway, 229

Elastic

Cyclorotations, 183

dense

limiting

aging

Cytokines, 46

Electron

Cytoplasmic

Electroretinogram

membrane

changes, 190

assessment, 188

bar, extension, 124

blood

(ERG), 123 b

supply, 201t

denseness, 177

concentration, 124

11-cis-retinol, re-isomerization, 125

clinical

decrease, occurrence, 124

Embr yo

enlargement, 189

Cytoplasmic

laments, hairpin

loops, 8

dorsal

surface, 141f

eye, light

Cytosol, protein

eye, section, 153f, 155f

(presence), 6

hyaloid

lens

D

micrograph, 155f

arterial

evaluation, 183–184

evidence, 156f

Cytoskeleton, laments, 8

bers

fatigue

resistance, 177

bers

system, light

micrograph, 145 f

layers, organization, 177

placode, thickening, 144f

sizes, range, 177

orbit, 155f

types, divisions, 177

Dark

adaptation, 127

Embr yonic

ssure, 141

inferior

Dark

current, 124

Embr yonic

nucleus, 100

inner vation, 182t, 188

Decorin, 35–36

Deep

brous

Deep

palpebral

Deep

petrosal

development, 98f

layer, 19

bers, 13

Embr yonic

ner ve, 225–226

Dense

light

connective

Dentate

tissue, 5–6

processes, 72f

Depolarizing

Descemet

bipolar

cells

macroscopic

plate, formation, 140

Emmetropia, 4f

Dendrites, 6

(DBCs), 126

anatomy, 179

origin, 184t

structure, 177

rays, focus, 3

superior

branch, 190

Emmetropization, 154b

Extrastriate

Endoderm, impact, 140

Eyeball, vertical

Endoplasmic

membrane, 35, 37, 39 f, 40f, 47, 48

branch, 190

insertions, 181f, 184t

illustration, 144f

orbicularis

(ELM), 112 f, 119

muscles, 155

action, 184t

bers, 6

coverage, 82–83

cGMP

hordeolum, 22f

External

Extraocular

disruption, 233

antagonist, 228

External

reticulum

(ER)

network, 6

cortex, 244

meridian, 171f

Eyebrow, 10

Endothelial

cells, 38, 39

Eyelashes, 11

evidence, 151

Endothelial

covering, loss, 83

Eyelids

tapering, 59

Endothelium, 4, 38, 40f, 41f, 47

aging

termination, 55f, 59, 82

Entropion, 13b, 13f

assessment, biomicroscope

Epicanthal

blood

Desmosome, 8

appearance, 151–153

Desmosome-like

Developing

fold, 12, 12f

Epicanthus, 12b

attachments, 120

lens, presence

Epichoroidal

(importance), 154

Epidermal

changes

supply

of

external

skin, 16

features, 10

margin, 11

topography,

Epimysium, 175

eyelid

Diabetes-related

Episclera, 55

palpebral

Diuse

cone

Dilation

Dilator

bipolar

cells, types, 116

connective

lag, 237f

muscle, 64

presence, 64, 69f

termination, 64

Direct-acting

adrenergic

Direct-acting

agonist, 228

Direct-acting

cholinergic

Disc

agonists, 228

agonist, 228

components, radiolabeled

amino

acids

pulse

(application), 115

Disc

(anatomic

(anatomic

Dorsal

tegmentum, injur y, 232

Dorsonasal

canthal

glands

Epithelial

cells

replacement, 46

orbital

classication, 5

retractor

lateral

superior

membranes, connection, 98

tissue, 4

sheets, 4

of

lower

tarsal

muscle

tarsal

plate, 16

apex

position, 65

interface

palpebral

(EFI), 100

(mitosis), 145

tarsal

plates, 18

Ethmoid

arteries, 194–195, 198

inner vation

Ethmoid

bone, 159

lacrimal

of, 22

system, 23, 26

lacrimal

nasolacrimal

D ura

plate, 165

Excyclorotation, 183

Exocrine

movements, 183f

mater, periosteal

tear

glands, 5

major

Exophthalmos, 172–173

layer, 170

External

carotid

ow

chart, 203f

terminal

adnexa

supply, 202f

branch, 202

Ectropion, 13b, 13f

External

collectors, 73f

Edinger-Westphal

External

features, of

nucleus, eerent

parasympathetic

Edinger-Westphal

Eector

pathway, 229

preganglionic

sites, neurotransmitter

cells, 223–224

(binding), 227

lm, 23, 24f

functions, 10

division, 12

eyelids, 10

eyelid

margin, 11

eyelid

topography, 11

palpebral

ssure, 10

topography, 11

Eye

movements, 182

control, 219

direction, 188f

result, 182–183

Eyes

accommodation, 71

adduction, 184

system, 24

drainage

ptosis, 216f

ocular

Ectoderm, impact, 140

secretor y

margin, 11, 21f

arter y, 202

branches

E

muscle, 14

conjunctiva, 18

orbital

eye

levator

Müller, 14f, 15, 15f

skin, 16

impact, 165

D uctions, 183

of

features, 16

Drusen, 77, 77f

eye, 25b

eyelid, 14

glands, 20

Drugs, impact, 228

Dr y

muscle, 12, 13 f

palpebral

histological

drawing, 99f

oculi

septum, 14f, 16

muscles, 18

to

Equator, cells

mydriasis, 228b

eyelids, 16, 17f

orbicularis

Epithelium-ber

arter y, 194, 201

tendons, 16

of

adaptation, 5

apex

ssure, 10

anatomy, 12

cell

layers, 64

direction), 1

branch, 201

Drug-induced

gross

Epithelial

composite

direction), 1

Dorsal

layer, 55

Epithelium, 30, 46

margins, atness, 132

Distal

tissue

Episcleritis, 55b

Epithelial

(usage), 4

of, 22, 24f

eyelid

Dextroversion, 183

cataract, 107

in, 26

eversion, 16b

stars, 73f

layer

(palpebrae), 155

system, 25, 25 f

Index

anatomic

anterior

blood

blunt

features, 1

chamber, 1

F lat

bipolars, 116

F lat

midget

supply, 197f

bipolar

trauma, 62

cell, invaginating

cell

midget

(comparison), 116

F loor, 163

chambers, 1

ciliar y

Gaze

bipolar

circulation, horizontal

section, 199 f

coats/tunics, 1

muscles, cardinal

Genetic

implications, 156

Geniculocalcarine

Genome, 6

characteristics, 163

Germinative

out

(F

), inclusion, 88

positions, 189 f

Gaze, positions, 183

apex, relationship, 163

F low

261

Giant

cone

tract

(optic

radiations), 243

zone, 98

bipolar

cell, name

(derivation), 116

out

duction, movement, 183f

F luid

early

F luorescein

full

development, 142f

thickness, photomicrograph, 75 f

human

embr yo, light

micrograph, 155 f

accumulation, 18b

serial

Glands, 20

angiography, 198

fundus

F luorescein

of

photos, 201f

eyelids, 16, 17f

secretion

dye, 30, 33f

Glands

of

classication, 5

Moll, development, 155

layers, 1

Foramen

ovale, 162

neural

Foramen

rotundum, 162

drugs, usage, 88

Foramen

spinsoum, 162

surgical

optical

outer

layer, 111

components, image

connective

posterior

primar y

tissue

focus, 3

coat, appearance, 30

chamber, 1

Foramina, presence, 166

Forced

position, 187f

duction

Forehead

proptosis, 173f

secondar y

Fossa, 163

positions, movements, 185

slit-lamp

Fourth

examinations, 92

sympathetic

layer, 1

vitreous

chamber, 1

supply, 58

surgical

cells, proliferation, 146

tissue, band, formation, 154

Globe

palsy, 217f

zone, 129

capillar y-free

Fovea

(fovea

muscles, division, 175

centralis), 128

orbital

outside, assessment, 4

Foveal

region, light

posterior

micrograph, 131 f

Glucose, 45

diameter, 128

Facial

ner ve

maturation, 148–149

Free

pathway, 219

Facial

nuclei

Fascia

bulbi

Fascial

Fat

(facial

radicals

Frontal

capsule), 56

Frontal

bone

eye

Fenestrations, presence, 151

Frontalis

Fetal

Frontal

ssure, 141

closure, 150–151

Fetal

lenses, 101f

Fetal

nucleus, 100, 101f

Fiber

Chievitz, 147, 149 f

orientation, visual

elds

(relationship), 246

muscle, 10

components, 104

network, 83

epithelium

interface, 100

(usage), 4

Ganglion

Fibroblasts, 6

Schwalbe, 66–67

refractive

acid

processes, 62

petrosal

wing, projection, 162

Gross

(GABA), inhibitor y

orbital

tarsal

tarsal

information, 123

sclera, 75

classication, 116

layer, 64f

of

eyelids, 16, 17f

oculi

muscle, 12, 13 f

septum, 14f, 16

superior

cells, dierentiation, 147

eyelids, 12

tendons, 16

retractor

cells, 116

ner ve, 225–226

anatomy, of

orbicularis

axon, 117

presence, 92

index, 99

Greater

proteins, stabilization, 104

amacrine

organs, 177

Greater

neurotransmitters, 124

Gamma

tonometr y, performing, 88

disease, hyperthyroidism, 189

glands

membranes, interdigitation, 104

of

the

lower

palpebral

muscle

of

eyelid, 14

levator

muscle, 14

Müller, 14f, 15, 15f

plate, 16

Ground

substance, 35–36

Growth

factors, presence, 104

layer, 112f, 120

layer, 19

establishment, 148

tissue, radial

projections, 60

axes, 182

neural

signal, 117–118

population, apoptosis

position, 187f

movement, 185f, 186f

illustration, 183f

apparatus, function, 82

Fissures, 167

Gradient

eye), 198f

Gamma-aminobutyric

junctions, 104

Filtration

tendon

G

interruption, 251f

globe

Golgi

canthal

formation, 104

eyes, secondar y

apparatus, 6, 111

Gonioscopy, 84–85

examination, ophthalmoscope

of

applanation

Golgi

Graves

(right

neurotransmitters, 124

cells, 19, 19f

Goldmann

dystrophy, 41f, 45

Furrows

elastic-like

Fibrovascular

Goblet

ner ve, 182, 211

photograph

agent, 105

Glycosaminoglycans, 35–36

Fundus

Fibers, 98

Fick’s

elds, 244

presence, 69f

Fuchs

layer

supercial

reducing

Glycine, inhibitor y

location, 182

inclusion, 100

Fibrous

impact, 106–107

Fuchs’ cr ypts, 65–66

Fiber

branching

release, 124

Glutathione, 47

impact, 162

cells, 6

neurotransmitter, 124

receptors, 125

formation, 159

expansions, 181

(Glu)

excitator y

byproduct, 103

nucleus), 219

(Tenon

of

Glutamate

accumulation, impact, 106

illustration, 219f

portion, 210f

veins, drainage, 204f

Foveola, 128

arter y, 202

VII, 219

apex, 180f

development, stages, 148

Facial

ner ve

length, 240

movement, 185f, 186f

zone, 129

layers, presence, 131f

cranial

(postluminar)

side, 179f

Foveal

F

Face, bones, 162

segment, peripher y, 63 f

intraorbital

lateral

annular

inhibitors, usage, 88

Glial

anterior

ner ve

anhydrase

procedures, 89

Glial

Fovea

inner vation, 236f

vascular

bers), 211

bers, 211

Fornices, branch

ner ves, supply, 208

carbonic

(sensor y

muscles, 10, 10f

sensor y

protection, 1

sensor y

aspect

treatment, 89

treatment, 88

test, 189

Forehead, lateral

movements, 183

Glaucoma, 88

thinning, 148f

Gap

junctions

appearance, 151–153

(occurrence), 155

H

Hair

follicles, development, 155

Haller’s

layer, 75–76

Hassall-Henle

bodies, 39b

Head

formation, 9

blunt

proteins, 105

circulation, 193

trauma, 62

Index

262

Hemidesmosomes, 8–9, 31, 46

Incyclorotation, 183

impact, 31

Herpes

zoster, 210

Interphotoreceptor

Indirect-acting

adrenergic

agonists, 228

carrier

Indirect-acting

agonist, 228

formation, 122

Heterochromia, 68

Indirect-acting

cholinergic

passive

High

Induction, 141–142

intraocular

Histologic

pressure, 45

features, 4

glands, 20

Inferior

(anatomic

Inferior

extraocular

muscles, 18

conjunctiva, 18

Inferior

tarsal

Holocrine

Inferior

glands, 5

Homonymous

congruent

muscles, sheaths,

Intracellular

Intracranial

eyelids, 200

eld, 249

defects, 250

incongruent

defects, 250

oblique

muscle, 182

communication, network, 127–128

involvement, 217

Intraocular

lens

Intraocular

optic

Intraocular

pressure

bers, 214

uctuations, 88

insertion, 182

impact, 88

ophthalmic

Horizontal

Inferior

orbital

ssure, 169

Intrinsic

communication, 126

Inferior

orbital

margin, formation, 167

Invaginating

information

Inferior

palpebral

Inferior

rectus

rectus

Horizontal

retinal

muscles, 184

raphe, 246

Horner

muscle, 13, 16, 170–171

Horner

pupil, iris

Horner

syndrome, 235b–236b

heterochromia, 235 b–236b

vein, 205

current, 104

Information

test, 237f

miosis, presence, 236f

presenting

anisocoria, 237f

cellular

Human

embr yo

eye, light

micrograph, 155f

light

arterial

muscle, 15, 15f

structure, 248

system, 145

processing, occurrence, 208

Ipsilateral

Infraorbital

ner ve, 211

Iris, 1, 62, 79, 153

Infraorbital

vein, 205

anterior

message, passage, 126

zone, 77

layers, 64f

segment, light

epithelial

Inner

ber, 114–115

ciliar y

Inner

limiting

arterial

coloboma, 144f

Inner

neuroblastic

layer, 71

layer, vitread

nonpigmented

nuclear

Hyaloid

channel, 91

Inner

plexiform

Weigner), 90

layer

portion

(cell

portion, light

color, 67

dilator

(INL), 112 f, 120

(IPL), 112 f, 120

inner vation, 225f

sympathetic

stimulation, 222

equilibrium, 225b

Inner

retinal

surface, 91

Inner

segment, 114

congenital

Hyaloid

system

Inner

synaptic

Horner

vitreous

Hyaloid

Hydrogen

acid

(HA)

(hyaluronan), 92

ions, 45

Hydrophobic

blood

layer, 6

eyelids, 22

light

to

uveal

location, 62

protein

Intermediar y

contribution, 153

space, acid-rich

Intermediate

tissue

of

circle

arcades, 66f

components, 7

test, 237f

correction, 3

micrograph, 63f

minor

junctions, 7

Intercellular

(farsightedness), 4f

features, 62

of

impact, 228

mucoprotein, 8

Kuhnt, 154

mioisis/mydriasis, movement, 63–64

posterior

zone, 91

surface, radial

Intermuscular

septa, 178–179

pupillar y

margin, 62

Intermuscular

transverse

pupillar y

portion, 66f

Hyperpolarizing

Internal

Hyperthyroidism

Hypophyseal

cells

(HBCs), 126

(Graves’ disease), 189

fossa

(sella

turcica), 159

I

ligament, 14 f, 14

arter y, 193

removal, 102f

atherosclerosis, 193

root, tissue

branches, ow

sphincter

chart, 203f

stroma, 62

lateral

surface

wall, 217–218

A, 19

conduction

speed, myelinization

(impact), 6

Incongruent

right

homonymous

hemianopia, 251 f

layer, 62

surfaces, 69f

Internal

collector

Internal

hordeolum, 22f

Iris

Internal

limiting

Isolated

fundus

movement, 65–66

muscle, 62

entr y, 145–146

location, 205f

Immunoglobulin

Impulse

carotid

folds/circular

furrows,72f

Hyperpolarization, magnitude, 124–125

bipolar

syndrome, 236 f

location, 235b–236b

layers, 69f

Inner vation

tract, 79

Horner

pupil

Inner vation

Intercellular

Hydroxyamphetamine

Hyperopia

histologic

supply, relationship, 190

Integrins, 7

lipid

heterochromia, 68

layer, 120

Inner vation, 190

development/regression, 146 f

vasculature, formation, 146

Hyaluronic

components, displacement, 148

sympathetic

Hyaloid

vessels, atrophy, 146f

micrograph, 69 f

cross-section, 69f

epithelium, growth,

layer

micrograph, 63 f

circle, formation, 151–153

arteries, branches, 63–64

membrane, 120

Inner

layer, 62

anterior

Inner

arter y, persistence, 147 f

bers,

retina, termination, 248 f

anterior

151–153

(of

border

collagenous

Hyaloid

retinal

absence, 62

Inner

Inner

temporal

(temporal)

Iridectomy, 64b

micrograph, 145f

ligament

inferior

tissue, 6

248

dierentiation), 147

Hyaloideocapsular

Ipsilateral

groove, 163

Hyalocytes, 92

Hyaloid

(imaging), 250 f

Inion, 159

physiolog y, review, 6

LGN, anatomic

eld

muscle

Infraorbital

Inhibitor y

orbit, 155f

Human

arter y, 132

formation, 205

ptosis, presence, 236f

Human

Invagination, synapses, 124

Ionic

cocaine

midget

(comparison), 116

channels, opening, 176

tarsal

responses, 227

cell, at

Ionic

Inferior

heterochromia, 236f

cell

bipolar

Involuntar y

anisocoria, 237f

iris

length, 240

location, 182

retina, superior

hydroxyamphetamine

midget

bipolar

muscle, 182

retinal

diagnosis, 235b–236b

(postlaminar)

muscles, pharmacologic

bers, 214

Inferior

test, 237f

Intraorbital

sulcus, 11, 12 f

Inferior

dierential

(IOP)

measurement, 88

Inferior

Horizontal

ner ve, 241f

decrease, 103

Hordeolum, 22b, 22f

transfer, 118

(IOL), insertion, 108

action, 185

origin, 182

cells, 118

neurons

processes, 127

aponeurosis, sheaths, 171–172

plates, 18

force, 112

Interplexiform

direction), 1

171–172

skin, 16

(IPM), 112

provision, 112–113

occurrence, 141–142

eyelids, 16

palpebral

agonist, 228

matrix

proteins, transport, 125

channel

(of

Sondermann), 84

membrane, 120

view, 121b

synechiae, 65

process, presence, 55f

agonist

Isotropic

band

model, 183–184

(I

band), 175

263

Index

J

Junctional

complexes, 9f

Juxtacanalicular

connective

Juxtacanalicular

tissue

Lateral

palpebral

arteries, 195

Lateral

palpebral

ligament, orbital

relationship, 170–171

tissue, 83

( JCT ), 87–88

Lateral

sicca, 25b

muscle, 178–179, 181

path, cellular

rays, neural

superior

Limbal

area, light

Limbal

blood

Limbal

conjunctiva, formation, 55 f

Limbal

histologic

Limbal

stem

Limbal

stroma, location/composition, 83 f

border, 181

wall, 166

L eft

cells, opsin

Brown’s

proptosis, 173f

L eft

Kuhnt, tissue

syndrome, 187f

incongruous

homonymous

hemianopia, MRI

anterior

blood

arter y, 195

vessels, 60

features, 59

boundar y, components, 59

micrograph, 59f

vessels, lymphatics, 60

biconvexity, 97

corneoscleral

capsule, 97, 103

drawing, 83f

transparency, 97

Lacrimal

histologic

junction

illustration, 55f

branch, 194–195

cortex, thickness, 103

stem

continuation, 195

cur vature, 103

transition, 59, 59f

location, 181

development, protein

Lacrimal

bone, 162

diameter, 97

Lacrimal

gland, 24

dimensions, 97

inner vation, 225

manufacture, 104

cell

deciency, 60b

transitional

Lingual

MRI

scan, 253f

Lipid

development, 156

epithelium, 98

Lipids

parasympathetic

equator, 97

bilayer, ion

ber

interface, 100

double

membranes, cholesterol

inner vation, 226 f

inner vation, 239f

zone, 59

g yrus, 243–244

divisions, 100

sympathetic

location, 59

features, 59

cells, bands, 101f

autonomic

conguration, 1

micrograph, 59 f

cells, deciency, 60 b

area, light

L ens, 141

L

organelles, 103

signal

Limbus, 1, 59

scan, 253f

tissue, 154

(formation), 154

(sensitivity), 124

eye

Keratocytes, 35

Kuhnt, intermediar y

transformation, 111

dissociation, 233b, 233f

Light

Keratoconus, 36b, 38f

Keratoplasty, 47

energ y

Light

L-cone

bers, 6

Keratoconjunctivitis

adaptation, 127

Light

Light-near

characteristics, 166

Keratan, 35–36

Keratin

rectus

Light

contraction, abduction, 184f

Lateral

K

septum,

layer, tear

lm, 23–24

movement

(facilitation), 6–7

layer, 6

Lacrimal

lake, 10

ber

Lacrimal

ner ve, 181, 211

glucose, collection, 104

L ong

ciliar y

arteries, anastomosing, 151–153

Lacrimal

papilla, 12, 25

metabolism, 104

L ong

ciliar y

ner ve, 210f

Lacrimal

punctum, 12, 25

optic

Lacrimal

sac, 26

fossa, anterior/posterior

crest, 167 f

isolation, 170–171

Lacrimal

secretor y

Lacrimal

system, 10

Lacrimal

system, in

lacrimal

nasolacrimal

tear

system, 24

system, 25, 25 f

lm, 23, 24f

L oose

L ower

connective

sensor y

Lymphatic

vascular

tunic, formation, 145–146

protection, ascorbic

refractive

acid

(impact), 105

power, 97

Lymphoid

ligament

of, 102

MA.

vascular

Macaque

Lamellae, 33

vesicle

synapses, 152f

Laminae

crossed

retinal

selective

projections, termination, 243 f

partial

uncrossed

involvement, 243 f

retinal

projections, termination, 243 f

Lamina

fusca

(suprachoroid

Lamina

papyracea, 165

Lateral

(anatomic

Lateral

canthal

Lateral

canthus, 10

Lateral

geniculate

anatomic

blood

layered

relay

direction), 1

tendon, 16

(LGN), 243, 248

section, 243f

structure, 243

station, 243

map

L ens

cortex, ber

L ens

bers, 98

cells

of, 99, 100 f

(scanning

representation, 248 f

cross-sectional

cytoplasm, protein

lutea, 128

proles

micrograph), 100 f

concentration, 99

terminolog y, 128b

Macular

region, capillar y

Macular

sparing, 254

resonance

imaging

Mastoid

cells, 6

Matrix

process, 159

metalloproteinases, 46

L evator

action, 14

Maxillar y

arter y, 203

L evator

aponeurosis, 14, 15f, 18, 18f

Maxillar y

bone

Lid

wiper

epitheliopathy, 19b, 19f

frontal

process, 167

wiper

region, 18

orbital

plate, 163

horn, 14

Lid

Lateral

orbital

Ligand-gated

stimulants, 6–7

(MRI), usage,

252–254

Mast

wings, projection, 159

bed, 130 f

occurrence, 254

Magnetic

UVR

absorption, 105

(MO), 7–8

areas

bers, termination, 249

production, continuation, 98

L esser

(MA), 8

occludens

process, complexity, 104

Lateral

margin, 167

adherens

Macula

Macular

electron

nucleus

terminolog y, 128b

arrangement, 103

cells, hexagonal

(MA)

geniculate

section), 243f

Macula

Macula

formation, 104

structure, 248

retinotopic

brunescence, 105

junctions, 104

nucleus

adherens

monkey, lateral

alteration, 62–63

(diagram), 97 f

components, 104

supply, 246

coronal

L ens

lamina), 75

Macula

Macrophages, 6

micrograph, 145f

zonule, relationship

perforations, 240

See

(coronal

light

impact, 54b

scleral

supply, absence, 99–100

formation, 142–143

cribrosa, 54, 56f

tissue, 19

appearance, 100

Lagophthalmos, 11b, 11f

Lamina

lining, 83–84

Lysosomes, 6

M

Lamellar

cell

drainage, 205

Lymphatics, 60

thickness, 97

(impact), 226

inner vation, 211f

thickening, 144f

sutures, 100

stimulation

tissue, 5–6

Lumen, endothelial

posterior

ligament), 171

eyelid, 14–15, 21f

formation, 144f

suspensor y

(increase), parasympathetic

(suspensor y

formation, 208

physiolog y, 103

slit-lamp

distribution, 25, 25f

Lacrimation

section, 100

placode, 142–143

eyelids, 23, 26

drainage

L ockwood

paradox, 105

system, 24

secretor y

content, 104

Maxillar y

ner ve

formation, 212

Index

264

Medial

(anatomic

Medial

canthal

area, structures, 208

direction), 1

Müller

bers, appearance, 148

Medial

canthal

tendon, 13, 13 f, 16

hypertrophy, 135

Medial

canthus, 10, 11f

per vasiveness, 118

Medial

orbital

structure, 119f

Medial

palpebral

wall, bones, 166 f

arteries, 194–195, 200

Müller

branches, 200

Medial

rectus

muscle, 178–179, 181

Multilobed

Muscle

bers, 214

number/distribution, 121

characteristics, 165

glands, 16

model, 176

illustration, 176f

formation, ethmoid

bone

(impact), 165

oblongata, 217–218

Muscle

movement, line

Neural

ectoderm, invagination, 70–71

Neural

fold, growth, 141f

Neural

groove, invagination, 141 f

Neural

retina, 147

Neural

signals, 123

Neural

tube

(relationship), 187 f

formation, 141f

Muscles, eyelids, 18

inner

surface, indentations, 140

Meibocytes, 20

Muscle

spindles, 177

Neuroblastic

Meibomian

Muscle

tissue, 6

Neuroglia, 6

glands, 11, 12f, 20, 20f, 24

development, 155

Meibomian

glands

classication, 6

(tarsal

glands), 16

Muscular

Meibum, 20

Myasthenia

granules

choroidal

processes, 62–63

stroma, 75

bers, 6

anisotropic

Melanosomes, 111

Membrane-bound

isotropic

organelles, degradation,

104

band

band

(I

(A

band), 175

proteins, 7

Myopia

Mesenchyme, 141

divisions

(separation),

82

transport

cells, 6, 119

properties, 6

eye, result, 142–143

Microtubules, 6, 104

Midbrain

NSC.

attachment, 176

Nuclear

tegmentum, injur y, 232

lesion, impact, 232

Miosis, 63–64

bones, impact, 162

O

Nasal

direction-adduction, 184

O blique

Nasal

bers, travel, 246

Nasal

step, 250

Nasociliar y

Nuclear

sclerotic

presence, 236f

cataract

tear

eld, 252f

ner ve, 212f

bone, 159

impact, 159

Occipital

lobe

striate

drainage

system, 25, 25 f, 156

sac, 26

and

muscles, 184

visual

cortex, 244f

pathway, 244f

Occludin, 7–8

duct, 26, 25f

canaliculi, 25

drainage, 26

Occluding

OCT .

See

Ocular

junction, 7–8

Optical

coherence

duct, 26, 25f

development, 155

Nasolacrimal

system, 156

lymphatic

glands, 16, 20–21, 21f

Motor

control

Motor

ner ves, eerent

Motor

nucleus

Mucin

of

layer, tear

of

lid

line

the

muscle, 22

pathway, 213

facial

ner ve, 219

lm, 23–24

junction, 18, 18 f, 57

margin, 18

of

Mar x, 11, 12f

Müller

(orbital

Müller

(tarsal

Near-point

reaction

(accommodation-convergence

muscle), 172

muscle), development, 155

Near

pupillar y

response, 230f

Neck

circulation, 193

internal

carotid

Ocular

albinism, 150b

Ocular

arter y

branches,

circulation

aging, eect, 206

arter y, contact, 193

(NFL), 112f, 120

physiolog y, 201

ber

layer

Ner ve

ber

orientation, 246f

Ner ve

tissue, 6

Ocular

ischemic

types, 6

Ocular

motility

Ocular

movement

Ner vous

carotid

202f

Ner ve

cell

(OCT )

drainage, 206f

supply, external

reaction), 228

orbicularis

of

Mucocutaneous

(MO)

tomography

adnexa, 10

Nasolacrimal

dot, 146b

Moll

(NSC), 92

complexity, 190

Mittendorf

occludens

(NSC)

involvement, 217

Mitochondria, 6, 111

Macula

cataract

section, 106f

sclerotic

Occipital

visual

nasolacrimal

puncta

See

epithelium

pumps, location, 6–7

Nasal

lacrimal

plane), 2

MO.

ciliar y

cataracts, 106, 106f

Nucleus

Nasolacrimal

cell, 116

(anatomic

See

Nuclear

formation, 210

nucleus, 213

bipolar

Nonpigmented

optical

bers, 6

automated

Midsagittal

See

junction, breakage, 176

Na/K/ATPase

Midget

(fundus

Nucleus, 6

loops, passage, 251f

oculomotor

retinopathy, OD

release, 228f

ATP

Meyer

Microphthalmic

diabetic

recycling, 227

NPE.

mechanisms, site, 98

Microglia, phagocytic

limiting

photo), 121f

actin

Myosin

(NPE), 71

membrane, 89

myobrils, 175f

trabeculae, components, 82

epithelium

(NPE)

N

dorsal

epithelium, internal

(nearsightedness), 4f

Metamorphopsia, 129

Microglial

ciliar y

Nonpigmented

in, 53

Mesoderm, impact, 140

Metabolic

Nonpigmented

Myosin

proliferation/migration, 141, 153

Meshwork, anatomic

basal/basolateral

Norepinephrine, 227

changes

correction, 3

layers, 142f

cells,

Nonproliferative

Myopia

scleral

cells, alignment, 153

replication, 228

aspects,71

band), 175

types, 175

sheath, 194

(comparison), 6

keratitis, 43

Nonpigmented

Myolaments, proliferation, 153

Membrane-spanning

Mesenchymal

Neurotrophic

cells, 20–21

Myobrils

pigment, derivation, 150b

Meshwork

ner ve

Myoepithelial

number

bodies/processes, 118

Neurotransmitters, 124, 227

Myelinization, impact, 6

branching

cell

action, drug

Myelinated

Melanocytes

cells, 118

Neurons, 6

Myelin, 6

production, 150b

covering

gravis, 176

layers, formation/completion, 147

number, neuron

Neuronal

Mydriasis, 63–64

density, 67–68

Meningeal

Neuroglial

arteries, 194–195, 200

variation, 200

Melanin

cells

separation, 141f

inner vation, 239f

ratchet

crest

dierentiation, 151–153

contraction

sliding

cells

death, 255

Neural

initiation, 227

wall, 165

Medulla

Neural

muscle, 15

sympathetic

contraction, abduction, 184f

Medial

cells, 118

system, 208

Ocular

development/mutation, RAX

156

syndrome, 193 f, 193

testing, 188

terminolog y, 183 t

(impact),

265

Index

Ocular

cupping, 54b

Orbital

connective

development, 140

structures

damage, 168

Orbital

cranial

embr yologic

formation, 143f

Orbital

fat, 172

genetic

derivation, 140b

implications, 156

parasympathetic

head, 130

pathway, 223

surfaces, three-dimensional

pathway, 240

inferior

sympathetic

system

intraocular

Oculocardiac

reex, 212

mapping, 4

branch, 214

section, 240

longitudinal

section, 196f

foramina/ssures, 167

Orbital

lobe, 24

Orbital

margins, 167

Orbital

muscle

Orbital

optic

of

Müller, 172

damage, 215

meningeal

Oculomotor

foramen, 180

passage, 54

Orbital

periosteum

Oculomotor

ner ve

visual

Orbital

plate, 163

Orbital

portion

ner ve

III, 213

exit, 214

nuclei, lateral/dorsal

views, 214 f

sheaths, 240

Orbital

Oculomotor

cranial

pathway, 244f

Optic

neuritis, 232b

Optic

pits, 140

Optic

radiations

pathway, 214

anterior

regeneration, aberration, 215

divisions, 246

sagittal

bers, middle

section, 213f

Oculomotor

midbrain

nucleus, 213

posterior

result, 251f

bipolars, 125

OFF

cells, designations, 125

Optic

longitudinal

ON

cells, designations, 125

agonist

agents, 228

Ophthalmic

antagonist

Ophthalmic

arter y, 181, 194

agents, 228

branches, 194–195

Ophthalmic

instrumentation, 3

Ophthalmic

ner ve

oculi

septal

septum, 14f, , 170

lateral

margin, 170–171

angular

view, 143f

sinus

sections, 143f

Orbit, separation, 166

strut, 167–168

O uter

collagenous

Optic

tract, 242, 248

O uter

ber, 114–115

O uter

neuroblastic

O uter

nuclear

O uter

plexiform

coronal

section, 248f

vesicle

coherence

Ora, bays/dentate

Ora

tomography

(OCT ), 4

linear

processes, 72 f

O uter

O vernight

retina, peripheral

micrograph, 75f

termination, 130

membrane, continuity, 77

Opsin, formation, 124

Orbicularis

action, 13

Optic

Orbicularis

ciliaris

Orbicularis

muscle, motor

Orbicularis

oculi

bers

exit, 247–248

sagittal

third

orbital

section, 242f

of

circle

of

W illis, relationship, 242 f

cup, 141

cell

inner

surface, views, 143f

layer, basement

internal

membrane, 146–147

corneal

swelling, 45

stress, UVR , relationship, 105

O xygen, 45

of, 22

portion, 13

action, 13

changes, 173

P

Painless

chalazion, 22f

Palatine

bones, 162

Palisades

of

Vogt, 60

brovascular

Palpebrae

tissue, radial

Palpebral

conjunctiva, 18, 56

Palpebral

ssure, 10

arrangement, 170

Palpebral

inner vation, 23f

blow-out

Palpebral

ligaments.

Palpebral

lobe, 24

portion, of

fracture, 163

bones, anterior

view, 164f

projections, 60

(eyelids), 155

See

Canthal

Palpebral

Papilledema, 132b, 133f, 204, 242f, 240

lip, elongation, 153

drainage, 204f

Papillomacular

longitudinal

fascial

Parafoveal

section, 143f

layer, pigment

(evidence), 156 f

cells, 142–143

tissue, 170

system

horizontal

vertical

section, 172f

section, 171f

disc, 130, 246

lateral

view, 204f

assessment, 132b

lateral

wall, formation, 159

glial

ner ves, 169f

tissue, 147f

ophthalmic

peripapillar y

section, 155f

retinal

elements, absence, 130

surface, ner ve

Optic

ber

orientation, 247 f

ssure, 141

closure, 143f

Optic

ner ve, 1, 154, 240, 247

capillaries, 245–246

choroid, connection, 75

arter y, branches, 194 f

shape, 163

sinuses, relationship, 169–170

veins, 203

vessels, 169f

Orbital

apex, 180f

globe, removal, 215f

Orbital

oculi

muscle, 13

bund le, 246

areas, 129

sinuses, 169

location, 170f

Parasympathetic

ow

inner vation, 103

chart, 223f

impact, 241f

margins, atness, 132

adhesion, 90

Paranasal

orbicularis

tendons

connective

surface, glial

entr y, 145–146

O xidative

composition, 163

Optic

arter y

layer, 120

pathway, resistance, 87

layers, apposition, 146–147

outer

carotid

control

muscle, 10, 12, 13 f, 18, 18f

Orbit, 155, 163

aging

layers, 141

inferior

orbicularis

(OPL), 112 f

plana), 69

portion, 13

palpebral

ventricle, oor, 241–242

vessels

Optic

(pars

division, 12–13

orientation, 247f

(ONL), 119

layer

arrangement, 149f

synaptic

light

basement

layer, components, 148 f

layer

occurrence, 120

serrata

RPE

zone, 77

synapses

orbit, 209f

supply, 246

relationship, 163f

cavities, location, 170f

formation, 211

chiasm, 240

ligament, relationship,

walls, 163

O utow

blood

system, 172

palpebral

choroid, connection, 77

Ophthalmoscope, usage, 4

inner vation, 208

Optic

Optic

muscle, 13

Orbital

ssure, closure, 150–151

Optical

branch, 200–201

orbicularis

Orbital

evagination, 140

origin, order, 195t

terminal

contracts, 14

of

Orbital

buckling, 141

orbit, view, 194f

orbicularis

medial

fetal

Ophthalmic

of

sensor y

stalk

transverse

(periorbita), 170

Orbital

arter y, branches, 246

buckling, 141

bipolars, 125

sclera, 53

ner ve, 241f

170–171

ON

of

tract), 243, 249

group, 246

cerebral

Oligodendrocytes, 6

Opacity

(geniculocalcarine

radiations, 246

location, 213

OFF

structures, 177

derivation, 155

sympathetic

supply, 222

tissue

ner ves, 209t

cellulitis, 170, 170f

Parasympathetic

root, 224

Parasympathetic

stimulation

lacrimation, increase, 226

pupillar y

constriction, 224

Parasympathetic

system, 222

activation, 229–230

Pars

plana

ciliar y

(orbicularis

epithelial

extension, 69

ciliaris), 69

layers, light

micrograph, 75 f

Index

266

Pars

plicata

cuboidal

PAS.

See

PAX2

(corona

ciliaris), 69

cells, 71

Peripheral

anterior

synechia

(PAS)

Posterior

ciliar y

Posterior

commissure, 229

Posterior

(gene), mutations, 156

Pericytes

(Rouget

Perifoveal

cells), ability, 76–77

Posterior

lens

Perimysium, 175

periosteum), 170

choriocapillaris, 195–198

Peripapillar y

chorioretinal

anterior

Peripheral

layers, position, 65

granules, shedding, 67

cr ypts, 65–66

Posterior

lens

Peripheral

fundus, 134f

Posterior

limiting

Peripheral

retina, 129

Posterior

precortical

Peripheral

retinal

degeneration, 130 b

Posterior

sclera, 56f

Peripheral

retinal

traction, 93

Petrous

P2

vision, 128

pupillar y

portion

ganglion

membrane, 153 b

(temporal

bone), 159

Pharmacologically, dilated

subcapsular

Posterior

pupil, 235 b

foramen, optic

cataract

vascular

vitreal

Photon, light

Posterior

Y

(changes), 124

vision, 123

ner ve

passage, 54

(PSC), 106, 107

cells, 111, 119

ganglion

absence, 132

skull

margin

involvement, 65

tunic, formation, 145–146

detachment, 93, 93 f

sutures, 100

Postganglionic

bers

Postganglionic

Potassium

Zinn, 180f

Red

corneal

erosion, 31b, 35f

eye, 200

pain, 211

Reex

blepharospasm, 14

Reex

blink, 13–14

Reex

tearing, 24

conditions, 3

examples, 4f

exit, 222

neural

Recurrent

Refractive

Relative

entr y, 235b–236b

illustration, 114f

of

display, 215f

Referred

synechia, pupillar y

Posterior

origin, 179

annulus

scleral

conguration, 127

muscles

insertions, 180

pockets, 90–91

portion, 210f

Posterior

Posterior

Photoreceptor

lamina, 37

Posterior

Photokeratitis, 47

Photopic

Rectus

photograph, 107f

cell, termination, 116

elds, 127

center-surround

vitreous

(slowness),

(gene), impact, 156

Receptive

surface, attachment, 97

globe, posterior

substances, turnover

103–104

RAX

pigment

(PAS), 65

folds, iris, 72f

Radiolabeled

lamina, 37–38

Persistent

Radial

iris, 63f

Posterior

Peripheral

R

surface, 66

atrophy, 135

synechia

cells, elongation, 144 f,

epithelium, 65

epithelial

Peripapillar y

Peripheral

membrane, 153b

persistence, 153

bers, relationship, 100

Posterior

(orbital

epithelial

Pupillar y

144–145

areas, 129

Periorbita

arteries, 195

aerent

pupillar y

defect

(RAPD)

application, 231–232

parasympathetic

bers, 224

left

eye

(RAPD

OS), 232f

+

signal, 117–118

Photoreceptors

Preganglionic

activation, 125

dark

channels

(K

channels), 6–7

bers, dorsal

column

Preganglionic

neuron, location, 223–224

Premacular

glutamate, release, 124

Prematurity, retinopathy, 151b

hyperpolarization, 125

Presbyopia, 103, 105

light

Preseptal

stimulation, absence, 124

Presynaptic

migration/maturation, 147–148

Pretectal

(PRK), 47–48

Phototransduction, 124

photon, change, 124

Physiological

blind

Physiological

cup, 132

blind

eld

spot, 132

visual

plots), 250f

cholinergic

agonist,

229f

Pig

micrograph, 156 f

dispersion

cholinergic

impact, 229f

photograph, 58f

adenoma, MRI

scan, 252 f

P lasma

membrane

surface

epithelial

cells, 30

P leomorphism, inclusion, 135

P lexiform

P lica

layers, appearance, 148

Point-to-point

circuitr y, knowledge, 123–124

position, 188

bers, 97, 100

coloboma, 144f

visual

degenerations, 122b

cortex

(striate

cortex), 243, 249

location, 243–244

Procerus

muscle, 10

ow

chart, 149f

function, 121

ganglion

(anatomic

direction), 1

Pter ygia, 58b

cells, axons

growth, 143f

pattern, 246

hemorrhages, 133b

tissue, 58b

image, orientation, 250f

Pter ygium, overgrowth, 58b

layers, 112f, 119

Pter ygoid

process, 162

light

energ y

Pter ygoid

venous

light

micrograph, full-thickness

light

microscopy, imager y, 111

plexus, 205

fossae, 162

ner ve

Pter ygopalatine

formation, passage, 212

ganglion, 212, 226

and

canaliculi, 25

transformation, 111

ner ve

ber

pattern, 246f

tissue, 1

peripheral

termination, 129

photoreceptor

layer, 112f

processing, 127

Poles, 97

Pupillar y

bers, 229

receptive

Pons, groove, 217–218

Pupillar y

light

regions, 128

gaze, 183

extraocular

muscles, inner vation, 188

Posterior

(anatomic

direction), 1

Posterior

cerebral

Posterior

chamber, 1, 89

arter y, branches, 246

pathway, 229

elds, arrangement, 127

illustration, 231f

stages, 148f

understanding, 229

synapses, 117f

Pupillar y

light

response, 231b

Pupillar y

margin, 62

involvement, 65

view, 119 f

metabolism, 127

neural

presence, 236f

Puncta

map), 248

development, 148f

constriction, 224

of

(retinotopic

detachment, 112b

Pupillar y

Positions

localization

ow, 127–128

lens

Ptosis, 15b, 15f

semilunaris, 10, 11f, 25, 57, 57f

blood

Primar y

maxillar y

of

supply, 132

capillar y

Primar y

Pter ygopalatine

P lasmalemma, 115

changes, 134

blood

cells, 117f

connective

tissue, 58b

lamina, 4

gaze, 219f

Proximal

agonist, 228

Pingueculae, 58b

Pituitar y

nucleus, 229

Proteoglycans, 35–36

syndrome, 67

Pilocarpine, direct-acting

connective

(impact), 6

Proptosis, 173f

embr yo, light

Pigmentar y

aging

potential

organization, 244

Physostigmine, indirect-acting

OD), 232f

deturgescence, 44

Primar y

Primar y

(central

corneal

Retina, 1, 246

movements, 183

spot, scotoma

Relative

(usage), 232

(RAPD

accommodation, 71

membrane, action

olivar y

eye

Reticular

cellulitis, 171

location, 129

keratoplasty

bursa, 90–91

(determination), swinging-ashlight

test

right

depolarization, 125

Physiologic

exit,

235b–236b

current, 125f

Photorefractive

presence

ten-layered

arrangement, 119

tissue

absence, 144f

267

Index

vertical

connections, 126

Riolan

vessels, 150

capillar y-free

visible

muscle, 13, 18, 18f, 20

Scleritis, 55b

Rods, 115

zone, relationship, 133

Scotopic

bipolar

changes, 135b

cell, 115

cells

Retinal

blood

supply, 132

body, 115

Retinal

cells, 117f

Retinal

degenerations, 122b

Retinal

detachment, 112b

Retinal

function, 121

Retinal

ganglion

Retinal

outer

segments, relationship

(3D

drawing),

113f

cilium, 114

vision, 123

Sebaceous

glands, 16

Sebaceous

Zeis

glands, 20

Secondar y

bers, Y-suture

Secondar y

lens

Secondar y

positions, 187f

movements, 185

composition, 113

Secondar y

density, increase, 121

Second-order

hemorrhages, 133b

inner

ber, 114–115

Sella

Retinal

histologic

inner

segment, 114

Sensor y

inner vation, 211f

Retinal

layers, 119

junction, 114f

Sensor y

root, 224

Retinal

metabolism, 127

width, 115

Septa

Retinal

neurons, ON/OFF

Retinal

pigment

cells, axons

(patterns), 246

features, 111

cells, 125

epithelium

light

(RPE), 71, 79 f, 111,

apical

portion, 111

basement

illustration, 122f

fundus

outer

segment, 113–114

Short

ciliar y

location, 224

spherule, 116f

Sinus

synapses, 116f

Skin

agent, production, 150

Rough

endoplasmic

melanosomes, 111

Rough

ER, impact, 6

neuroretinal

RPE.

interface, 112

See

Retinal

of

reticulum, 111

Retinal

pigment

extracellular

segments

(3D

sensor y

pigment

epithelium

(RPE)

epithelium

relationship), 113f

(RPE)

cells

space, 112

Retinal

processing, 127

Retinal

receptive

Retinal

synapses, 117f

Retinal

tissue

venous

Retinal

ow, 127–128

tree, retina

Retinal

venous

Retinal

vessels, 150

branch

pacemaker

ner ve

ber

pattern

Retractor

zone, relationship, 133

mechanisms, 201–202

of

prematurity

map

of

Retrobulbar

lower

optic

localization), 248

eyelid, 14

space

tract, 91

(of

of

upper

view, 161f

lateral

posterior

laments, arrangement, 176 f

reticulum, calcium

ion

release, 176

canal, 73f, 82, 83

diameter, 88

posterior

view, 160f

tissue

Smooth

ER, impact, 6

muscle

concentration, increase, 107

inclusion, 63f

Space

inner

Spectacles, 36b

endothelium, 87

lesser

cells, 6

wing, 166

wings, projection, 159

projection, 159

absence, 6

Sphenoid

Sclera, 1, 53, 151

bone, coronal

Sphenopalatine

changes

in, 54

Sphincter

supply, 54

muscle, 62

parasympathetic

Spiral

of

rectus

broblasts, 75

muscles, impact, 181f

Spontaneous

canals, 54

venous

Squamous

cell

formation, 53

Squamous

corneal

histologic

Squamous

portion

normal

photograph, 198f

inner vation, 54

fundus, 121f

opacity

papilledema, 133f

fundus, photo, Stargardt ’s

macular

dystrophy, 123f

Right

lateral

Right

orbital

Right

superior

geniculate

nucleus, laminae, 243 f

oor, blow-out

fracture

(coronal

CT ), 165f

oblique

of, 53

changes, in

Scleral

ectasia, 53

Scleral

ner ve

Scleral

spur, 53, 73f, 82

collagen

myopia, 53

bone), 159

dystrophy, right

fundus

induced

cataract, 108

surger y, 189

of

Axenfeld, 209

sheets, endothelial

(loss),83

(temporal

macular

Strabismus, 189

Stratied

Striate

corneal

cortex

bers, presence, 55f

trabecular

dysfunction, 217 f

Steroid

Scleral

loops

epithelium, 59

(photo), 123f

posterior, 56f

proptosis, 173f

Right

Stargardt ’s

pulsation, 204

layer, 30, 35f

Right

features, 53

inner vation, 226 f

Tillaux, 180

Ribosomes, 6

fundus

section, 205 f

ganglion, 226

location, 64

bands, 75

and

bone, 159

greater

line, 38

tissue, 6

ller, 5–6

Sphenoid

lumen, presence, 55f

foramina

eye

system, 172

Sorbitol

wall, 83

bone

(impact), 159

Smooth

detachment, 73f

manufacture, 6

divisions, entr y, 212

(formation), occipital

derivation, 154

collagen

granules, protein

aspect

Slings, connective

color, 54

(RNA)

view, 160f

ophthalmic/maxillar y

cross-sectional

blood

Berger), 90

view, 162f

oor, 161f

eyelid, 14 f

layer, 75–76

aging

synapses, 124

acid

plane), 2

extension, 175–176

Schwann

neuritis, 179

Retrolental

Ribonucleic

section

Schwalbe

(ROP), 151 b

(point-to-point

Retrolental

Ribbon

occlusion, 195

pigmentosa, 122b

Retinotopic

Sagittal

Schlemm

inner vation, absence, 201–202

capillar y-free

Retinopathy

(anatomic

Sattler’s

branches, location, 204

autonomic

anterior

division, 159

Sagittal

thick/thin

(relationship), 246f

Retinitis

S

Sarcoplasmic

vascular

bers, 208, 211

bones, unication, 159

Sarcomere

elds, arrangement, 127

blood

of, 16

base, disarticulated

phagocytosis, 122

capillar y

layer

eyelid, 16

Skull

physiolog y, 121

rods/cells, outer

cavities, location, 170f

epidermal

characteristic, 163

melanin-related

photos, 201f

ner ves

damage, 233–234

Roof, 163

layers, 112f

fossa), 159

presence/orientation, 178–179

Serial

junction, 114f

(proposal), 121–122

neuron, 115

(hypophyseal

location, 178–179

width, 115

transport, model

turcica

ber, 114–115

membrane, 77

laments, merging, 77

vitreous, development, 154

outer

continuity, 77

ion

detection, 123

morpholog y, 115

119, 146

(meeting), 145

bers, 98, 100

epithelium, 30

(primar y

visual

cortex),

243, 249

covering

maps, 252

visual

information, combination, 244

Index

268

Striated

muscle

connective

Suspensor y

tissue

network, 175f

of

sheath, relationship, 175

light/dark

L ockwood), 171

Trabecular

test, 235b–236b

response, 232f

anatomy, 175

Sympathetic

hypothalamus

travel, 222

Sympathetic

Stroma, 46

ow

Transient

sheets, pigment/debris

ber

Transporting

bers

tissue, 6

scan, 253f

separation, 82

visibility, 154

lens, 102, 102f

photomicrograph, 176f

Stroke, MRI

(of

tissue, 171–172

Swinging-ashlight

bands, 175

microscopic

ligament

connective

trans

control, 222

inner vation, 236f

chart, 223f

layer

of

epithelia, polarization, 6–7

retinol, uptake, 125

Transverse

(anatomic

Transverse

tubules

plane), 2

(T

tubules), ion

Trigeminal

ganglion, bers

Trigeminal

ner ve

layer, 64

Sympathetic

ner ves, plexus, 195

activation, irritation, 226

sphincter

muscle, location, 64

Sympathetic

pathway

divisions, 212f

of

palpebral

Styloid

process, 159

Stylomastoid

Submucosa

Substantia

foramen, 159

of

palpebral

propria

Subsurface

conjunctiva, 19

of

conjunctiva, 19

palpebral

conjunctiva, 19

vesicles, 19

Supercial

conjunctival

Supercial

temporal

terminal

Superior

colliculus, 244

Superior

eyelids, 200

Superior

nasal

Superior

oblique

direction), 1

chiasm

linear

ophthalmic

vein, 203

veins, connection, 203

ssure, 169, 218

Trochlear

damage, 217

Synaptic

contacts, occurrence, 120

Trochlear

ner ve

Synaptic

densities, 120

Synaptic

vesicles, neurotransmitter

edge, 167–168

muscle

of

plates, 16, 18

Tarsal

smooth

drainage, 26

Tear

lm, 23, 24f

Tropicamide, adrenergic

antagonist, 228

complex, calcium

(binding), 176

Tunics

(coats), 1

Two-layered

basal

epithelium

lamina

basis, 152f

separation, 152f

uid, 25

U

Teenagers, right

Superior

orbital

Superior

palpebral

bone

margin

ridge

(formation), frontal

(impact), 163

levator

musc le, 14

bones, 159

lifetime

composition, 159

aponeurosis, 14, 15f

squamous

rectus

sulcus, 11, 12 f

muscle, 181

contraction, Fick’s

axes

(globe

crescent, 249

Temporal

eld

visual

Tendinous

bers

insertion, 182

Tendinous

ring, 179

retinal

arter y, 132

Tenon

Superior

retinal

quadrants, bers

Superior

tarsal

Superior

transverse

(termination),

248

ligament

Suprachoroidal

( W hitnall

ligament),

levator

plots), 250f

lamina), 76 f

lamina

Tertiar y

in

suprachoroidea, 76f

lamina), 69

sclera, detachment, 73f

Upper

arter y, 194–195, 199

origin, 199

Tonic

section

of, 14f

aspect, sensor y

muscles, sensor y

sensor y

bers, 211

bers, 211

inner vation, 211f

Uvea, 1, 151

bar, zonula

occludens/adherens, 111

aging

vitreous, stretching, 154

changes

in, 79

structures, 1

myobrils, 175

of

power, 97

bers, 6

eyelids

lateral

tract, 62

myobrils, 175

Tissue

lens, refractive

ner ve

eyelid, 10, 11

sagittal

bulbi, 56

ree-layered

of, 47

ring, diameter

passage, 240

location, 59–60

ick

fusca, 75

(supraciliar y

Unmyelinated

Upper

episclera, connection, 55

Terminal

(suprachoroid

Unaccommodated

aponeurosis, 18

piercing, 171

space, 75

Suprachoroidea

eld

spot), scotoma

formation, 55f

14, 14f

ciliar y

(decrease), 103

blind

capsule, 56, 83f, 171

fascia

muscle, 15, 15f

of

stress, relationship, 105

radiation, absorption

Unaccommodated

(physiologic

(central

(UVR), 105

absorption, 105

exposure, 107

Ultraviolet

portion, 159

Temporal

movement), 185 f

radiation

ber

oxidative

portion, 159

inner vation, 182

Superior

Ultraviolet

Temporal

levator

palpebral

fundus), 121 f

lens

petrous

Superior

(normal

arteritis, 202

action, 14

Superior

eye

Temporal

levator

endothelium, separation, 152 f

Uveal

blood

Uveal

tract, 62

Kuhnt, formation, 154

blood

pupil, 233–234, 234b

vessels, 197f

supply

inner vation

to, 79

to, 79

Tonolaments, 8

Torsions, 183

Supratrochlear

arter y, 194, 200

Supratrochlear

notch, 167

Supraversion, 183

lens

section, 213f

nucleus, 216

Troponin-tropomyosin

muscles, 22

Tear

IV, 216

pathway, 216

Müller, 14f, 15, 15f

Tarsal

Tear

separation, 166

ectoderm, 140

covering

ner ve

entr y, 216

sagittal

roof

Surface

release, 124

Trochlear

Tearing, 26

Supraorbital

cranial

distribution, 25, 25f

posterior

Supraciliaris

origin, 182

complexes, appearance, 148

ner ves/vessels, entr y, 169f

lamina

division, 208

attachment, 163

arrangement, 149f

assessment, 24b

edges, 170

Suprachoroid

ophthalmic

Trochlea

development, 155

angular/supraorbital

division, 212

division, 211

Synaptic

Tarsal

trochlea, impact, 182

medial

system, 222

T

muscle, 182

origin, 182

orbital

root, 224

Sympathetic

entr y, 248

length/width, 182

Superior

maxillar y

Synkinesis, 228–229

bers, superior

action, 184–185

Superior

mandibular

origination, 222

Sympathetic

of, 19

branch, 202

(anatomic

formation, 212

disruption, 235

Synapses, 6

cell, surface

arter y, 202

Superior

damage, 235b–236b

spread, 175

(exit), 212

epithelial

Stroma

deposits, 88

Chievitz, 147, 149 f

layers, 142f

vesicle, separation, 144–145

V

movement, questions, 183

Trabeculae, prominence, 69f

Valve

Trabecular

Vascular

meshwork, 73f, 82

conguration

(change), ciliar y

contraction

inclusion, 63f

(impact), 71

musc le

of

Hasner, 25f, 26

endothelial

growth

factor

impact, 122

overproduction, 122

Vascularized

connective

tissue, 19

( VEGF), 43, 92

269

Index

Vascular

primar y

vitreous, 146 f

Vasomotor

sympathetic

VEGF .

Vascular

See

inner vation, 24

endothelial

growth

factor

Y

second-order

Y oke

vascular

branches, 69f

V isual

Venous

branches, location, 204

Venous

channel, 83–84

Venous

sinus

Ventral

(anatomic

neuron, 115

structures, anatomy, 240

( VEGF)

Veins, radial

illustration, 239f

pathway, 241f, 245f

pigments

view, 206 f

V isual

Z

direction), 1

Zeis

system, 2f

information

joining, 75–76

V itreal

attachments, 90

V itreal

function, 92

V idian

(versions), 183

rectus

musc les, 185

ner ve, pter ygopalatine

retinal

A

ganglion

entr y,

ZO.

deciency, 19b

V itreomacular

areas, 245f

attachment, 90

V itreous

cells, location, 92

RPE

cortex, 243

V itreous

chambers, 1, 82, 90

V isual

evoked

V itreous

composition, 91

V isual

eld, 4

V itreous

cortex, 91

V itreous

humor, 1

V itreous

physiolog y, 92

V itreous

zones, 91

visual

pathway, display, 251f

orientation, relationship, 246

striate

cortex, schematic, 254f

Voltage-gated

testing, 249

V isual

Voluntar y

information, striate

cortex

(combination),

Vortex

244

V isual

Zonular

pupillar y

Zonular

bars, 111

attachments, composite

lamella, 98

Zonular

length, increase

Zonule

tissue, 6

vitreous, stretching, 146 f

Zonular

229

development, 154

veins, 75–76, 76f, 204

Zonules

Water-soluble

blood

W hitnall’s

cr ystallins, decrease, 105

ligament, level, 178 f

cells/synapses, 239–240

W ide-eld

display, 251f

W ing

bers, indication, 230f

alpha

amacrine

cells, 35f, 31

formation, 152f

cells

(diagram),

97f

cycle, 117

aging, 255

supply, 245

point, 72f

lens, relationship

W

Wake/sleep

(absence), 103

bers, 69

attachment

pathway, parallelism,

drawing,

bers

tertiar y

stimulants, 6–7

muscle

cells, connection, 133–134

insertion, 98

drainage, 204

light

(ZO), 7–8

99f

pathway

aerent

bars, 111

occludens

terminal

V isual

ber

(ZO)

junctions, 30

V itreous

association

defects, 250–252

occludens

evidence, 151–153

V isual

response, recordation, 159

Zonula

adherens, 8

terminal

Zonula

traction, 91f, 91

presence, 112

changes, 135b

See

Zonula

V itreous, 154

225–226

V isible

Zinn, zonules, 102

specialization, 127

V itamin

glands, 16, 20, 20f

development, 155

collection, 1

formation, 150–151

Vergences

positions, 189f

sutures, 100

activation, 124

Venules

Vertical

Y

location, 124

drainage, superior

muscles, 189

cardinal

(A17

cells), 127

Zonules

of

Zinn, 102

Zygomatic

bones, 163

Zygomatic

ner ve, 211–212

bypass, 226

Zygomatic

process, 159