The Human Eye

Structure and Function

Clyde W. Oyster
The University of Alabama
at Birmingham

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Sunderland, Massachusetts

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Brief Contents
Preface xxiii
Acknowledgments xxviii
Prologue A Brief History of Eyes 1

PART ONE
Ocular Systems 55
1 Formation of the Human Eye 57
2 Ocular Geometry and Topography 77
3 The Orbit 111
4 The Extraocular Muscles 133
5 The Nerves of the Eye and Orbit 191
6 Blood Supply and Drainage 247
7 The Eyelids and the Lacrimal System 291

PART TWO
Components of the Eye 323
8 The Cornea and the Sclera 325
9 The Limbus and the Anterior Chamber 379
10 The Iris and the Pupil 411
11 The Ciliary Body and the Choroid 447
12 The Lens and the Vitreous 491
13 Retina I: Photoreceptors and Functional Organization 545
14 Retina II: Editing Photoreceptor Signals 595
15 Retina III: Regional Variation and Spatial Organization 649
16 The Retina In Vivo and the Optic Nerve 701

Epilogue Time and Change 753

Glossary G –1
Historical References and Additional Reading HR–1
Index I –1
vii
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Contents
Preface xxiii
Acknowledgments xxviii

Prologue A Brief History of Eyes 1

The Antiquity of Eyes and Vision 1
Thinking about the eye gave Charles Darwin “a cold shudder” 1
The history of the eye is embedded in the history of animals and
molecules 2
Several of the eye’s critical molecules are ancient 3
Eyes were invented by multicellular animals almost 600 million years
ago 5
Eyes arose not once, but numerous times, in different animal groups 6
Eyes are most common in groups of motile animals living in lighted
environments 8

The Diversity and Distribution of Eyes 9

The first step in vision is an eye that can sense the direction of incident
light 9
At least ten types of eyes can be distinguished by differences in their
optical systems 11
Vertebrates always have simple eyes, but invertebrates can have
compound eyes, simple eyes, or both 13

Paths and Obstacles to Perfection 16

Simple eyes improve as they become larger 16
Elaborate simple eyes may have evolved rapidly 18
Compound eyes have inherent optical limitations in their
performance 19

An Ocular Bestiary: Fourteen Eyes and Their Animals 21

I. Compound eye—focal apposition, terrestrial variety: Honeybee
(Apis mellifica) 21
II. Compound eye—focal apposition, aquatic variety: Horseshoe crab
(Limulus polyphemus) 23
III. Compound eye—afocal apposition: Monarch butterfly (Danaus
plexippus) 26

ix
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x Contents

IV. Compound eye—apposition with neural The primitive lens is the first ocular structure to exhibit
superposition: Housefly (Musca domestica) 29 cell differentiation 68
V. Compound eye—refracting superposition: Firefly All future growth of the lens comes from the early lens
(Photuris spp.) 31 cells, some of which are “immortal” stem cells 69
VI. Compound eye—reflecting superposition: The precursors of the future retina, optic nerve, lens, and
Crayfish 33 cornea are present by the sixth week of gestation 69
VII. Compound eye—parabolic superposition: Crabs 36 In general, the eye develops from inside to outside 70
VIII. Simple eye—pinhole: Nautilus 37
Failures of Early Development 71
IX. Simple eye—refracting, aquatic variety: Octopus 38
“If anything can go wrong, it will” 71
X. Simple eye—refracting, aquatic variety: Goldfish 40
One or both eyes may fail to develop completely 71
XI. Simple eye—refracting, terrestrial variety: Pigeon
(Columba livia) 43 Congenital absence of the lens may be an early
developmental failure 71
XII. Simple eye—refracting, terrestrial variety: Jumping
spiders (Metaphidippus spp.) 45 Incomplete closure of the choroidal fissure can produce
segmental defects in the adult eye 74
XIII. Simple eye—reflecting: Scallops 48
XIV. Simple eye—refracting, terrestrial variety: Humans VIGNETTE 1.1 The Eye of Mann 72
(Homo sapiens) 50
Chapter 2 Ocular Geometry and
PART ONE Topography 77
Ocular Systems Elements of Ocular Structure 77
The human eye is a simple eye 77
Chapter 1 Formation of the Human Eye 57 The outermost of the three coats of the eye consists of
Some Developmental Strategies and Operations 57 cornea, limbus, and sclera 78
The middle coat—the uveal tract—includes the iris,
Embryogenesis begins with cell proliferation, cell ciliary body, and choroid 78
movement, and changes in cell shape 57
The eye’s innermost coat—the retina—communicates
Specialized tissues are formed by collections of cells that with the brain via the optic nerve 79
have become specialized themselves 58
Most of the volume of the eye is fluid or gel 81
Proliferation, movement, and differentiation in a cell
group may require communication with other cells 58 Image Quality and Visual Performance 82
Embryonic Events before the Eyes Appear 59 Images of point sources are always small discs of light
whose size is a measure of optical quality 82
The blastocyst forms during the first week of
embryogenesis 59 The amount of smear or spread in the image of a point
source is related to the range of spatial frequencies
The inner cell mass becomes the gastrula, which is transmitted by the optical system 83
divided into different germinal tissues 60
The contrast sensitivity function specifies how well
Neurulation begins the development of the nervous different spatial frequencies are seen by the visual
system 62 system 86
Formation of the Primitive Eye 64 We can see flies when their images subtend about one
minute of visual angle 87
Ocular development begins in the primitive forebrain 64
The optic vesicle induces formation of the lens 64 The Anatomy of Image Formation 90
The quality of a focused image is affected by pupil size,
Elaboration of the Primitive Eye 65 curvatures of optical surfaces, and homogeneity of the
The optic cup and the lens form from different germinal optical media 90
tissues by changes in cell shape 65 Defocusing produces large changes in the modulation
The optic cup is initially asymmetric, with a deep groove transfer function 92
on its inferior surface 67 The major anatomical factors that determine the
Closure of the choroidal fissure completes the optic refractive power of the eye are the curvatures of the
cup 67 cornea and lens and the depth of the anterior
chamber 93
The lens vesicle forms in synchrony with the optic cup 67
Schematic eyes are approximations of the eye’s optically
relevant anatomy 95

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 Contents xi

Eye Shape and Size 97 All structures in the orbital cavity are lined and
interconnected with connective tissue 125
Vertebrate eyes vary considerably in shape 97
Abnormal development of the connective tissue may
Both the cornea and the sclera are aspheric 97 affect movement of the eyes 125
On average, the adult human eye measures twenty-four Fat fills the spaces in the orbital cavity that are not
millimeters in all dimensions 100 occupied by other structures 126
Axial lengths and other anatomical features vary among The septum orbitale prevents herniation of orbital fat into
individuals, but most eyes are emmetropic 101 the eyelids 127
Most refractive error is related to relatively large or small
axial lengths 102 Development of the Orbital Bones 127
Many bones form first as cartilage templates 127
The Eye’s Axes and Planes of Reference 103
Most orbital bones do not have cartilaginous
The eyes rotate around nearly fixed points 103 templates 127
Like the head, the eyes have three sets of orthogonal The orbital plates begin to form during the sixth week of
reference planes 104 gestation 130
The pupillary axis is a measure of the eye’s optical The capacity of bone for growth, repair, and remodeling
axis 106 lasts many years 130
The line of sight differs from the pupillary axis by the The eyes and orbits rotate from lateral to frontal positions
angle kappa 107 during development 130
The angles kappa in the two eyes should have the same Most developmental anomalies of the orbital bones are
magnitude 107 associated with anomalies of the facial bones 131
Eye position is specified by the direction of the line of
VIGNETTE 3.1 Sovereign of the Visible World 116
sight in a coordinate system whose origin lies at the
eye’s center of rotation 108 BOX 3.1 Visualizing the Orbit and Its Contents In
VIGNETTE 2.1 The Medieval Eye 80 Vivo 122
BOX 2.1 Evaluating Visual Resolution 88 VIGNETTE 3.2 The Anatomy of Vesalius 128

VIGNETTE 2.2 Fundamentum Opticum 98

Chapter 4 The Extraocular Muscles 133
Chapter 3 The Orbit 111 Patterns of Eye Movement 133
The Bony Orbit 111 Our eyes are always moving, and some motion is
necessary for vision 133
The orbits are roughly pyramidal 111
Large, rapid eye movements are used for looking around,
The large bones of the face form the orbital margin and for placing retinal images of interest on the fovea 135
much of the orbit’s roof, floor, and lateral wall 112
Slow eye movements are used to track or follow movement
The sphenoid bone fills the apex of the orbital pyramid and to compensate for changes in head and body
and contributes to the lateral and medial walls 114 position 136
The lacrimal and ethmoid bones complete the medial Eye movement velocities may vary by a factor of 105 137
wall between the maxillary bone in front and the
sphenoid in back 118 Since the eyes have overlapping fields of view, their
movements must be coordinated 137
Three major and several minor foramina permit blood
vessels and nerves to enter or exit the orbital cavity 118 Slow movements of the eyes in opposite directions help
keep corresponding images on the foveas in both
Blowout fractures of the orbit are a consequence of the retinas simultaneously 138
relative weakness of the orbital plates 119
Strabismus is a misalignment of the two visual axes
Abnormal positioning of the eye relative to the orbital under binocular viewing conditions 139
margin may indicate local or systemic pathology 120
Infection and tumors can enter the orbital cavity through Control of Eye Position 139
the large sinuses that surround the orbit 120
The extraocular muscles are arranged as three
Connections between the Eye and the Orbit 121 reciprocally innervated agonist–antagonist pairs 139
The eyes are stationary when the opposing forces exerted
Connective tissue lines the interior surface of the by the extraocular muscles are in balance 141
orbit 121
Imbalanced forces produce eye rotations 142
Connective tissue surrounds the eye and extraocular
muscles 121 Muscle force is related to muscle length 143
Check ligaments connect Tenon’s capsule to the Most of the force that maintains eye position is passive
periorbita 124 force 144

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xii Contents

Equilibrium muscle lengths and forces for different gaze Passive extraocular muscle stretch may produce
positions are functions of the innervational bradycardia 167
command 145 Sensory endings in extraocular muscles probably do not
Different patterns of innervation are required for fast and convey information about eye position 167
slow eye movements 146 Sensory signals from the extraocular muscles may be
Extraocular motor neurons are located in three involved in motor learning, motor plasticity, and
interconnected nuclei in the brainstem 146 development 168
Motor commands are the result of interactions between
visual and nonvisual inputs to the motor control
Actions of the Extraocular Muscles 168
centers 147 All of the extraocular muscles except the inferior oblique
A copy of the innervational command is used to verify have their anatomical origins at the apex of the
the system’s operation 148 orbit 168
Extraocular motor neurons receive inputs from premotor The anatomical origin of the inferior oblique and the
areas in the brainstem to generate appropriate signals functional origin of the superior oblique are anterior
for saccadic eye movements 148 and medial in the orbit 169
The pathways for smooth pursuit movements and for The four rectus muscles are arranged as horizontal and
vergences go through the cerebellum, but vergences vertical pairs, all inserting onto the anterior portion of
have a separate control center near the oculomotor the globe 170
nucleus 149 The horizontal recti rotate the eye in the horizontal plane
around a vertical axis 170
Extraocular Muscle Structure and Contractile
The vertical recti are responsible for upward and
Properties 153 downward rotations of the eye 171
Muscle fibers are the units from which muscles are The recti define a muscle cone within the orbital cavity
constructed 153 that contains most of the ocular blood vessels and
Striated muscle fibers have a parallel arrangement of nerves 172
contractile proteins that interleave to cause The oblique muscles constitute a third functional pair,
contraction 154 inserting onto the posterior portion of the eye 172
Striated muscle fibers differ in structural, histochemical, Extraocular muscle actions cannot be measured
and contractile properties 155 directly 174
The extraocular muscles contain muscle fiber types not The classic description of action of the extraocular
found in skeletal muscles 156 muscles is based on the geometry of their origins and
Thick and thin extraocular muscle fibers differ in their insertions 174
contractile properties 156 Boeder diagrams attempt to describe the actions of the
Different muscle fiber types are not randomly distributed extraocular muscles completely 176
within the muscles 157 The presence of Tenon’s capsule and muscle pulleys
Different muscle fiber types may receive different invalidates the geometric model of extraocular muscle
innervational commands 158 actions 178
Extraocular muscles have very small motor units 159 “There is no simple way to describe the action of these
muscles on the eye!” 180
Acetylcholine at the neuromuscular junctions depolarizes
the cell membrane by opening sodium channels 161 A realistic model of the extraocular muscle system is
The spread of depolarization along the sarcolemma may important for the diagnosis and treatment of muscle
differ among muscle fiber types, producing different paresis 182
contractile properties 161
Development of the Extraocular Muscles 183
Extraocular muscles exhibit high sensitivity to agents
that mimic or block the action of acetylcholine 162 Each muscle develops from several foci in the mesoderm
surrounding the optic cup 183
Extraocular muscles often exhibit early symptoms of
myasthenia gravis 163 The extraocular muscles appear after the optic cup, but
before the orbital bones 185
Neurotoxins that interfere with acetylcholine action can
be used to alleviate strabismus and blepharospasm 163 Different muscle fiber types form late in gestation and
continue to develop postnatally 185
Sensory Endings in Extraocular Muscles and Tendons 165 Most developmental anomalies are associated with the
Skeletal muscles have two major types of sensory connective tissue of the muscles or with their
organs 165 innervation 186
Human extraocular muscles have anatomically The oculomotor system is not fully operational at
degenerate sensory organs and exhibit no stretch birth 186
reflexes 166
BOX 4.1 Detecting Ocular Misalignment 140

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 Contents xiii

BOX 4.2 Changing the Effects of Extraocular Muscle All somatosensory information from the eye is conveyed
Contraction 152 by the nasociliary nerve to the ophthalmic division of
the trigeminal 213
VIGNETTE 4.1 Locating the Extraocular Muscles 164
Sensory nerve fibers from the cornea, conjunctiva,
VIGNETTE 4.2 In the Service of the Eye 184 limbus, and anterior sclera join to form the long ciliary
nerves 213
Stimulation of corneal or conjunctival nerve endings
Chapter 5 The Nerves of the Eye and elicits sensations of touch or pain, a blink reflex, and
Orbit 191 reflex lacrimation 215
Other sensory fibers from the eye are conveyed by the
Elements of Neural Organization 191 short ciliary nerves and the sensory root of the ciliary
The brain deals with information about the external ganglion 215
world and the body 191 Most other branches of the ophthalmic nerve carry
Neurons are the anatomical elements of neural somatosensory fibers from the skin of the eyelids and
systems 191 face 215
Neural circuits consist of neurons linked mostly by A few branches of the maxillary nerve pass through the
unidirectional chemical synapses 193 orbit from the facial skin and the maxillary sinus 217
The direction of neural information flow distinguishes Lesions in the branching hierarchy of the ophthalmic
between sensory and motor nerves 194 nerve produce anesthesia that helps identify the lesion
site 218
Motor outputs are divided anatomically and functionally
into somatic and autonomic systems 194 Viral infection of the trigeminal system can produce
severe corneal damage 219
The autonomic system is subdivided into the
sympathetic and parasympathetic systems 194 The Extraocular Motor Nerves 219
The Optic Nerve and the Flow of Visual Information 195 The three cranial nerves that innervate the extraocular
muscles contain axons from clusters of cells in the
In the optic nerve, the location of axons from retinal brainstem 219
ganglion cells corresponds to their location on the
retina 195 Cells in different parts of the oculomotor nerve nucleus
innervate the levator, the superior and inferior recti, the
Axons from the two optic nerves are redistributed in the medial rectus, and the inferior oblique 219
optic chiasm 198
Axons destined for different muscles run together in the
The decussation of axons in the chiasm is imperfect 199 oculomotor nerve until it exits the cavernous sinus just
Spatial ordering of axons changes in the optic tracts 200 behind the orbit 221
In the lateral geniculate nuclei, which are primary targets The oculomotor nerve contains parasympathetic fibers
of axons in the optic tracts, inputs from the two eyes are bound for the ciliary ganglion 224
separated into different layers 200 Cells in the trochlear nerve nucleus innervate the
Axons terminating in the lateral geniculate nuclei are contralateral superior oblique 224
spatially ordered 201 Abducens nerve cells innervate the ipsilateral lateral
Some axons leave the optic tracts for other rectus 225
destinations 203 All of the oculomotor nerves pass through the cavernous
Axons terminating in the superior colliculi form sinus on their way to the orbit 225
discontinuous retinotopic maps 204 The extraocular motor nerves probably contain sensory
Axons forming the afferent part of the pupillary light axons from muscle spindles and tendon organs 226
reflex pathway terminate in the pretectal nuclear
complex 204 Innervation of the Muscles of the Eyelids 226
Retinal inputs to the accessory optic system may help Three sets of muscles are associated with the eyelids 226
coordinate eye and head movement 205
The orbicularis is innervated by the facial nerve 227
Retinal axons may provide inputs to a biological
The superior and inferior tarsal muscles are innervated
clock 205
by the sympathetic system 227
Lesions of the optic nerves and tracts produce defects in
Ptosis may result from either oculomotor or sympathetic
the visual fields 207
lesions 228
Lesions in the secondary visual pathways can be
observed only as motor deficits 212 Autonomic Innervation of Smooth Muscle within
the Eye 228
The Trigeminal Nerve: Signals for Touch and Pain 212
The superior cervical ganglion is the source of most
Two of the three trigeminal divisions carry signals from sympathetic innervation to the eye 228
the eye and surrounding tissues 212

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Sympathetic fibers enter the eye in the short ciliary Spinal neurons in peripheral nerves can regenerate after
nerves 230 being damaged 242
Sympathetic innervation of the dilator muscle acts at Central nervous system neurons do not regenerate
alpha-adrenergic receptors to dilate the pupils 230 following major damage 242
The arterioles in the uveal tract receive sympathetic Corneal nerve endings will regenerate following local
innervation that produces vasoconstriction 231 damage 243
Horner’s syndrome is the result of a central lesion in the Neuronal degeneration can affect other, undamaged neu-
sympathetic pathway 231 rons 243
Parasympathetic fibers entering the eye originate in the VIGNETTE 5.1 The Integrative Action of the Nervous
ciliary or the pterygopalatine ganglion 231
System 196
Axons from cells in the ciliary ganglion innervate the
sphincter and the ciliary muscle 232 BOX 5.1 Tracing Neural Pathways: Degeneration and
Axons from the pterygopalatine ganglion cells innervate Myelin Staining 206
vascular smooth muscle in the choroid 233 VIGNETTE 5.2 Seeing One World with Two Eyes:
Accommodation and pupillary light reflexes share The Problem of Decussation 210
efferent pathways from the Edinger–Westphal nuclei to
the eyes; pupillary reflexes are mediated by retinal BOX 5.2 Tracing Neuronal Connections: Axonal
signals reaching the Edinger–Westphal nuclei through Transport Methods 222
the pretectal complex 233
Deficient pupillary reflexes may be associated with
midbrain lesions 234 Chapter 6 Blood Supply and Drainage 247
Innervation of the Lacrimal Gland 235 Distributing Blood to Tissues 247
Axons from cells in the pterygopalatine ganglion reach Arteries control blood flow through capillary beds, and
the lacrimal gland via the zygomatic and lacrimal veins regulate blood volume 247
nerves 235 Blood flow through capillary beds can be controlled
The efferent pathway for lacrimal innervation begins in locally or systemically 248
the facial nerve nucleus 235 Capillary beds in a tissue may be independent or
Basal tear production may require tonic innervation of interconnected 251
the lacrimal gland 236 The interchange between blood and cells depends partly
on the structure of the vascular endothelium 252
Some Issues in Neural Development 236 Capillary endothelium is renewable, and capillary beds
Specialized growth cones guide the extension of axons can change 253
and dendrites 236 Neovascularization is a response to altered functional
Pathfinding by growth cones depends on recognition of demands 253
local direction signs 237 Structurally weakened capillaries may be prone to
Target recognition and acquisition may require specific excessive neovascularization 254
markers produced by the target cells 238
The Ophthalmic Artery and Ophthalmic Veins 255
Many early neurons are eliminated as mature patterns of
connectivity are established 238 The ophthalmic artery distributes blood to the eye and its
Adult connectivity patterns are not always complete at surroundings 255
birth, and postnatal development is subject to Blood supplied to tissues by the ophthalmic artery is
modification 239 drained to the cavernous sinus by the ophthalmic
Ocular albinism is associated with a pathfinding error in veins 257
the development of optic nerve axons 239
Supply and Drainage of the Eye 260
Anomalous innervation of the extraocular muscles
may be the result of pathfinding or target recognition Muscular arteries supply both the extraocular muscles
errors 240 and the anterior segment of the eye 260
Some forms of amblyopia may be related to problems The anterior ciliary arteries contribute to the episcleral
with postnatal establishment and maintenance of and intramuscular arterial circles 261
synaptic connections 240 The conjunctiva and corneal arcades are supplied by
Innervation of the extraocular muscles begins early in branches from the episcleral arterial circle and drained
gestation, sensory innervation much later 241 by the episcleral and anterior ciliary veins 262
The system of episcleral veins drains the conjunctiva,
Postnatal Neuron Growth and Regeneration 241 corneal arcades, and limbus 263
Most postnatal neuron growth is interstitial growth 241
Neurons do not undergo mitosis postnatally 242

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 Contents xv

The posterior ciliary arteries divide into long and short Chapter 7 The Eyelids and the Lacrimal
posterior ciliary arteries that supply different
regions 264 System 291
The intramuscular and major arterial circles are formed Structure and Function of the Eyelids 291
in the ciliary body by branches from the anterior and
long posterior ciliary arteries 265 Structural rigidity of the lids is provided by the tarsal
plates 291
Blood supply to the anterior segment is redundant, but
there is some segmentation in supply to the iris 268 The tarsal plates are made of dense connective tissue in
which glands are embedded 292
The short posterior ciliary arteries terminate in the
choriocapillaris, which supplies the retinal The palpebral fissure is opened by muscles inserting onto
photoreceptors 269 or near the edges of the tarsal plates 294
The short posterior ciliary arteries contribute to the The palpebral fissure is closed by contraction of the
supply of the optic nerve through the circle of Zinn 272 orbicularis 296
The short posterior ciliary arteries sometimes contribute Blinking may be initiated as a reflex response or as a
to the supply of the inner retina 274 regular, spontaneous action 298
The central retinal artery enters the eye through the optic Lid movements during spontaneous blinks move tears
nerve and ramifies to supply the inner retina 275 across the cornea 299
The central retinal vein exits the eye through the optic Overaction of the orbicularis may appear as
nerve 277 blepharospasm or as entropion 299
The vortex veins drain most of the uveal tract 277 Paresis of the orbicularis produces ectropion and
epiphora 300
The vortex veins have segmented drainage fields, but
they are heavily anastomotic 278 Other glands in the lids are associated with the
eyelashes 301
Supply and Drainage of the Eyelids and Surrounding The skin on the lids is continuous with the conjunctiva
Tissues 279 lining the posterior surface of the lids and covering the
anterior surface of the sclera 302
The lacrimal gland is supplied by the lacrimal artery and
drained by lacrimal veins 279 The orbital septum is a connective tissue sheet extending
from the orbital rim to the tarsal plates 303
The eyelids are supplied by branches of the lacrimal,
ophthalmic, facial, and infraorbital arteries 279 The shape and size of the palpebral fissure vary 304
The terminal branches of the ophthalmic artery leave the The overall structure of the lids consists of well-defined
orbit to supply the skin and muscles of the face 282 planes or layers of tissue 306
The infraorbital artery runs under the orbital floor 283 Tear Supply and Drainage 307
The orbital veins are connected to the veins of the face,
the pterygoid plexus, and the nose 283 Most of the tear fluid is supplied by the main lacrimal
gland 307
Development of the Ocular Blood Vessels 284 Secretion by the lacrimal gland is regulated by autonomic
inputs operating through a second-messenger
Primitive embryonic blood vessels appear very early in
system 308
the eye’s development 284
The composition of the lacrimal gland secretion varies
Several parts of the early ocular vasculature are transient
with the secretion rate 309
and do not appear in the mature eye 284
Dry eye may result from a decreased amount of tears,
The anterior ciliary system forms later than the posterior
abnormal tear composition, or both 310
ciliary system 287
Tears are drained off at the medial canthus and deposited
Remnants of normally transient, embryological
in the nasal cavity 311
vasculature may persist in the mature eye 287
Pressure gradients created by contraction of the
VIGNETTE 6.1 Circulation of the Blood 256 orbicularis during blinks move tears through the
canaliculi into the lacrimal sac 312
BOX 6.1 Tracing Hidden Blood Vessels: Vascular
Casting 270 Formation of the Eyelids and the Lacrimal System 315
VIGNETTE 6.2 Blood Vessels inside the Eye 280 The eyelids first appear as folds in the surface ectoderm,
which gives rise to the lid glands 315
The lacrimal gland and the lacrimal drainage system
derive from surface ectoderm 316
Most developmental anomalies in the eyelids and
lacrimal system are problems in lid position or blockage
of the drainage channels 318
Anomalous innervation can produce eyelid movements
linked to contraction of muscles in the jaw 318

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xvi Contents

PART TWO Corneal Healing and Repair 365

Components of the Eye The epithelium heals quickly and completely 365
Corneal healing may require limbal transplants 368
Chapter 8 The Cornea and the Sclera 325 Repair of damage to the stroma produces translucent scar
tissue 368
Components and Organization of the Cornea and
The endothelium repairs itself by cell expansion and
Sclera 325 migration 369
The cornea, sclera, and limbus are made primarily of Corneal graft incisions are repaired by the normal
collagen fibrils 325 healing processes 369
Collagen is embedded in a polysaccharide gel that forms Radial keratotomy incisions are repaired by epithelial
the extracellular matrix 326 hyperplasia and collagen formation 370
The fibroblasts in the corneal and scleral stroma Photorefractive keratectomy ablations are healed mostly
constitute a small fraction of the stroma’s volume 327 by the epithelium 371
Collagen fibrils in the cornea are highly organized; those
in the sclera are not 328 Growth and Development of the Cornea 371
The structure of the corneal stroma is altered in The epithelium and endothelium are the first parts of the
Bowman’s layer 331 cornea to appear 371
Corneal transparency is a function of its regular The stroma is derived from neural crest cells associated
structure 332 with the mesoderm 372
Collagen organization in the stroma and corneal The regular arrangement of the stromal collagen appears
transparency depend on intact epithelium and soon after collagen production begins 372
endothelium 334 Corneal growth continues for a few years
The corneal epithelium is a multilayered, renewable postnatally 374
barrier to water movement into the cornea 335 Anomalous corneal development can produce misshapen
The corneal endothelium is a single layer of or opaque corneas 375
metabolically active cells 339
BOX 8.1 Biomicroscopy of the Cornea 342
The endothelial cell tiling changes with time because
cells that die cannot be replaced 340 VIGNETTE 8.1 The Invisible Made Visible 350
Descemet’s membrane separates the endothelium from BOX 8.2 Some Reservations about Corneal Refractive
the stroma 345
Surgery 362
Nerve endings in the cornea give rise to sensations of
touch or pain, a blink reflex, and reflex lacrimation 347 VIGNETTE 8.2 The Art of William Bowman 366
The epithelium contains a dense array of free terminals
of nerve fibers from the long ciliary nerves 347
Chapter 9 The Limbus and the Anterior
Corneal sensitivity can be measured quantitatively 349
Chamber 379
The dense innervation of the cornea makes it subject to
viral infection 349 The Anterior Chamber and Aqueous Flow 379
The Cornea as a Refractive Surface 349 The anterior chamber is the fluid-filled space between the
cornea and the iris 379
The optical surface of the cornea is the precorneal film
covering the surface of the epithelium 349 The angle of the anterior chamber varies in
magnitude 380
The cornea’s outline is not circular, its thickness is not
uniform, and its radius of curvature is not constant 351 Aqueous is formed by the ciliary processes and enters the
anterior chamber through the pupil 381
The shape of the cornea is determined by comparison to
a sphere 353 Aqueous drains from the eye at the angle of the anterior
chamber 383
The cornea does not have a single, specifiable shape 354
Intraocular pressure depends on the rate of aqueous
Contact lenses can affect corneal shape and structure production and the resistance to aqueous outflow 385
directly or indirectly 356
The shape and optical properties of the cornea can be The Anatomy of Aqueous Drainage 390
permanently altered 358 The scleral spur is an anchoring structure for parts of the
Surgically reshaped corneas may change with time 359 limbus and the ciliary body 390
Corneal shape can be changed by removing tissue 360 The trabecular meshwork is made of interlaced cords of
Stromal reshaping leaves the epithelium intact 361 tissue extending from the apex of the angle to the
margin of the cornea 392
Corneal grafts are used to repair optically damaged
corneas 361 Schwalbe’s ring separates the trabecular meshwork from
the cornea 393

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 Contents xvii

The trabecular cords have a collagen core wrapped with Structure of the Iris 420
endothelial cells 393
The pupils in the two eyes are normally the same size
The major source of outflow resistance is the juxta- and are decentered toward the nose 420
canalicular tissue separating the canal of Schlemm from
the trabecular spaces 395 The iris is constructed in layers and regional differences
in the iris are related to the different muscles within
The canal of Schlemm encircles the anterior chamber them 421
angle 395
The anterior border layer is an irregular layer of
Aqueous enters the canal of Schlemm by way of large melanocytes and fibroblasts interrupted by large
vacuoles in the endothelial lining of the canal 397 holes 422
Aqueous drains out of the canal into venous plexuses in The iris stroma has the same cellular components as the
the limbal stroma 399 anterior border layer, but loosely arranged 423
Pilocarpine reduces intraocular pressure, probably by an Small blood vessels run radially through the stroma,
effect of ciliary muscle contraction on the structure of anastomosing to form the minor arterial circle and
the trabecular meshwork 400 supply the iris muscles 425
An effective way to reduce intraocular pressure seems to The sphincter and dilator occupy different parts of the
be to increase the uveoscleral outflow 402 iris and have antagonistic actions 426
Surgery for glaucoma aims to increase aqueous The sphincter is activated by the parasympathetic
outflow 402 system, the dilator by the sympathetic system 427
The outer surface of the limbus is covered with episcleral The anterior pigmented epithelium is a myoepithelium,
tissue and a heavily vascularized conjunctiva 403 forming both the epithelial layer and the dilator
muscle 428
Development of the Limbus 405
The posterior epithelial cells contact the anterior surface
The anterior chamber is defined by the iris growing of the lens 430
between the developing cornea and lens 405
Surgery for closed-angle glaucoma often involves the iris
The angle of the anterior chamber opens during rather than the limbus 432
development as the root of the iris shifts
posteriorly 406 Some Clinically Significant Anomalies of the Iris and
The trabecular meshwork develops between the fourth Pupil 432
and eighth months 408
Changes in iris color after maturity are potentially
Most developmental anomalies in the limbus are pathological 432
associated with structural anomalies that affect other
parts of the anterior chamber 408 Differences between the two eyes in pupil size or
pupillary responses to light are commonly associated
BOX 9.1 Through the Looking Glass: Gonioscopy 382 with neurological problems 433
BOX 9.2 Estimating the Pressure Within: Anisocoria and unresponsive pupils are often associated
Tonometry 388 with defects in the efferent part of the innervational
pathways 435
Clinically useful drugs affecting pupil size fall into four
Chapter 10 The Iris and the Pupil 411 functional groups 437

Functions of the Iris and Pupil 411 Development of the Iris 440
The iris is an aperture stop for the optical system of the The iris stroma forms first by migration of
eye 411 undifferentiated neural crest cells 440
The entrance pupil is a magnified image of the real The epithelial layers and the iris muscles develop from
pupil 412 the rim of the optic cup and are therefore of
neuroectodermal origin 440
Variation of pupil size changes the amount of light
entering the eye, the depth of focus, and the quality of The pupil is the last feature of the iris to appear 442
the retinal image 413 Most postnatal development of the iris is an addition of
Pupil size varies with illumination level, thereby helping melanin pigment 443
the retina cope with large changes in illumination 414 Segmental defects and holes in the iris result from
Pupil size varies with accommodation and unsynchronized or failed growth of the optic cup rim 443
accommodative convergence 416 An ectopic pupil is improperly centered in an otherwise
The pupillary near response is smaller in children than in normal iris 445
adults 417 A persistent pupillary membrane may be the result of
The pupil is in constant motion, and it reacts quickly to either insufficient tissue atrophy or tissue
changes in retinal illumination 418 hyperplasia 445
Decreased iris pigmentation in ocular albinism affects the
optical function of the iris 419

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xviii Contents

Chapter 11 The Ciliary Body and the The choriocapillaris is heavily anastomotic but has local
functional units 479
Choroid 447 The choriocapillaris varies in capillary density and in the
Anatomical Divisions of the Ciliary Body 447 ratio of arterioles to venules 480
Capillaries in the choriocapillaris are specialized for
The ciliary processes characterize the pars plicata 447
ease of fluid movement across the capillary
The ciliary muscle extends through both pars plicata and endothelium 481
pars plana 449
Bruch’s membrane lies between capillaries and
The Ciliary Processes and Aqueous Formation 449 pigmented epithelium in both the choroid and the pars
plana of the ciliary body 481
The ciliary processes are mostly filled with blood
vessels 449 Development of the Ciliary Body and Choroid 482
The capillaries in the ciliary processes are highly The ciliary epithelium arises from the optic cup, the
permeable 451 ciliary muscle from neural crest cells 482
Two layers of epithelium lie between the capillaries and Formation of the ciliary epithelium may be induced by
the posterior chamber 452 the lens 483
Aqueous formation involves metabolically driven Formation of the ciliary muscle may be induced by the
transport systems 452 ciliary epithelium 484
The ciliary epithelium is anatomically specialized as a The ciliary muscle begins to form during the fourth
blood–aqueous barrier 454 month and continues to develop until term 485
Ions are transported around the band of tight junctions to The muscles associated with the eye originate from
produce an osmotic gradient in the basal folds of the different germinal tissues 486
unpigmented epithelium 455
The ciliary processes form in synchrony with the vascular
Aqueous production varies during the day and declines system in the ciliary body 486
with age 456
The zonule is produced by the ciliary epithelium 486
The major classes of drugs used to reduce aqueous
The choroidal vasculature has two developmental
production interact either with adrenergic membrane
gradients: center to periphery and inside to outside 488
receptors or with the intracellular formation of
bicarbonate ions 458 VIGNETTE 11.1 The Source 470
The pars plana is covered by epithelial layers that are
continuous with the epithelial layers of the pars
plicata 459 Chapter 12 The Lens and the Vitreous 491
The Ciliary Muscle and Accommodation 461 Structure of the Lens 492
The ciliary muscle has three parts with a complex Some unusual proteins, the crystallins, are the dominant
geometry 461 structural elements in the lens 492
Contraction of the ciliary muscle produces movement Dense, uniform packing of the crystallins within lens
inward toward the lens so that the muscle behaves like cells is responsible for lens transparency 494
a sphincter 463 Crystallins are highly stable molecules, making them
The zonule provides a mechanical linkage between some of the oldest proteins in the body, but they can be
ciliary muscle and lens 465 changed by light absorption and altered chemical
Accommodation is a result of ciliary muscle environments 494
contraction 468 a-Crystallins may play a special role in maintaining
The primary stimulus to accommodation is retinal image native crystallin structure over time 496
blur 469 The lens is formed of long, thin lens fibers arranged in
Accommodative amplitude decreases progressively with concentric shells to form a flattened spheroid 497
age 472 Lens fibers in each shell meet anteriorly and posteriorly
Presbyopia is not a consequence of reduced innervation along irregular lines 498
to the ciliary muscle 473 Lens shells are bound together with miniature locks and
Aging of the ciliary muscle is unlikely to be a significant keys, a kind of biological Velcro 499
factor in presbyopia 474 The anterior epithelium is the source of new cells for the
lens 501
The Choroid 477 Elongating epithelial cells at the equator become long
The choroidal stroma consists of loose connective tissue lens fibers that form new shells in the lens 503
and dense melanin pigment 477 The size of the lens and the number of lens fibers
Blood vessels that supply and drain the capillary bed increase throughout life 503
supplying retinal photoreceptors make up the main Each new lens shell has one more fiber than the previous
part of the choroid 478 shell and about five new shells are added each year
after the age of five 504

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 Contents xix

An aged lens has about 2500 shells and 3.6 million lens Most developmental anomalies in the vitreous represent
fibers 505 incomplete regression of the hyaloid artery system 541
The lens capsule encloses the lens shells and VIGNETTE 12.1 Putting the Lens in Its Proper
epithelium 507
Place 512
The locations at which the zonule inserts onto the lens
change with age 510 BOX 12.1 Cataract Surgery 528

The Lens as an Optical Element 513

The refractive index of the ocular lens varies from one
Chapter 13 Retina I: Photoreceptors and
part of the lens to another 513 Functional Organization 545
Lens transparency is related not only to protein
regularity but also to water content, which is
The Retina’s Role in Vision 545
maintained by ion pumping in the epithelium 514 The retina detects light and tells the brain about aspects
The lens contains several different optical zones 515 of light that are related to objects in the world 545
The lens surfaces are parabolic and therefore flatten Objects are defined visually by light and by variations in
gradually from the poles to the equator 516 light reflected from their surfaces 546
Both anterior and posterior lens surfaces become more The retina makes sketches of the retinal image from
curved with accommodation, but the anterior surface which the brain can paint pictures 547
change is larger 519
Functional Organization of the Retina 549
The lens thickens with age and its curvatures increase, but
unaccommodated lens power does not increase with Photoreceptors catch photons and produce chemical
age 520 signals to report photon capture 549
The increased lens surface curvatures in accommodation Photoreceptor signals are conveyed to the brain by
are primarily a consequence of tissue elasticity 522 bipolar and ganglion cells 551
The presbyopic lens is aging, fat, and unresponsive 523 Lateral pathways connect neighboring parts of the
retina 552
Presbyopia is largely, if not solely, associated with age-
related changes in the lens 525 Recurrent pathways may assist in adjusting the
sensitivity of the retina 554
Cataracts, most of which are age-related, take different
forms and can affect any part of the lens 526 The retina has anatomical and functional layers 555

The Vitreous 530 Catching Photons: Photoreceptors and Their

The vitreous is the largest component of the eye 530
Environment 560
The primary structural components of the vitreous are Each photoreceptor contains one of four photopigments,
collagen and hyaluronic acid 530 each of which differs in its spectral absorption 560
The external layer of the vitreous—the vitreous cortex— Color vision requires more than one photopigment 562
attaches the vitreous to surrounding structures 532 The photopigments are stacked in layers within the outer
Inhomogeneity of the vitreous structure produces segments of the photoreceptor 564
internal subdivisions in the vitreous 533 Light absorption produces a structural change in the
The vitreous changes with age 533 photopigments 565
Shrinkage of the vitreous gel may break attachments to Structural change in the photopigment activates an
the retina 536 intracellular second-messenger system using cGMP as
the messenger 566
Altered activity of cells normally present in the vitreous
or the introduction of cells from outside the vitreous A decrease in cGMP concentration closes cation channels,
may produce abnormal collagen production and scar decreases the photocurrent, and hyperpolarizes the
formation 537 photoreceptor 568
Vitrectomy removes abnormal portions of the Absorption of one photon can produce a detectable rod
vitreous 538 signal 570
Photocurrent in the outer segment decreases in
Development of the Lens and Vitreous 539 proportion to the number of absorbed photons 572
The lens forms from a single cell line 539 Photopigments activated by photon absorption are
Most failures of lens development are manifest as inactivated, broken down, and then regenerated 573
congenital cataracts 540 Photoreceptor sensitivity is modulated by intracellular
The primary vitreous forms around the embryonic Ca2+ 575
hyaloid artery 541 Changes in photoreceptor sensitivity account for less
The secondary vitreous, initially acellular, forms outside than half of the retina’s sensitivity increase in the dark
the vasa hyaloidea propria 541 and sensitivity decrease in the light 578

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xx Contents

The tips of photoreceptor outer segments are surrounded The effects of neurotransmission depend on postsynaptic
by pigment epithelial cell processes 579 receptors 620
The pigment epithelium and the interphotoreceptor Amacrine cell connections centering on the AII amacrine
matrix are necessary for photopigment regeneration 580 cells illustrate difficulties in understanding amacrine
Both rods and cones undergo a continual cycle of cell operations 621
breakdown and renewal 583
Ganglion Cell Signals to the Brain: Dots for the Retinal
The inner segments of photoreceptors assemble the Sketches 624
proteins to construct the outer segment membranes 585
The inner segments form tight junctions with Müller’s Most ganglion cells are midget or parasol cells 624
cells; these junctions are the external limiting The small region of the world seen by a ganglion cell is
membrane 586 its receptive field 628
Photoreceptors signal light absorption by decreasing the The concentric organization of excitation and inhibition
rate of glutamate release from their terminals 590 makes ganglion cells sensitive to contrast rather than to
Glutamate release from a photoreceptor is subject to average light intensity 630
modification by activity in other photoreceptors 592 Ganglion cell receptive fields can be thought of as filters
that modify the retinal image 631
VIGNETTE 13.1 “Everything in the Vertebrate Eye
Sensitivity functions of ganglion cell receptive fields
Means Something” 558 differ in size and in the strength of their inhibitory
components 636
Chapter 14 Retina II: Editing Photoreceptor Ganglion cell signals differ in their reports on stimulus
duration and on the rate of intensity change 637
Signals 595 Midget ganglion cells have wavelength information
The Editing Process 595 embedded in their signals, but only small bistratified
cells are known to convey specific wavelength
Interactions among Photoreceptors, Horizontal Cells, and information 639
Bipolar Cells 597 Axons from midget and parasol ganglion cells go to
Horizontal cells integrate photoreceptor signals 597 different layers in the lateral geniculate nucleus 642
Horizontal cells receive inputs from photoreceptors and Ganglion cell responses are the elements of retinal
send signals of opposite sign back to the photoreceptor sketches 643
terminals, using GABA as the neurotransmitter 601
VIGNETTE 14.1 The Retina Comes to Light 612
Horizontal cell connections emphasize differences in
illumination between different photoreceptors 602 VIGNETTE 14.2 The Shoemaker’s Apprentice 626
Different glutamate receptors on cone bipolar cells cause BOX 14.1 Studying Individual Neurons 632
increases and decreases in light intensity to be reported
by ON and OFF bipolar cells, respectively 605
Signals from both red and green cones go to midget Chapter 15 Retina III: Regional Variation
bipolar cells, which are specific for cone type, and to and Spatial Organization 649
diffuse bipolar cells, which are not cone specific 606
Blue cones have their own bipolar cells 608 Making Retinal Sketches out of Dots: Limits and
Rods have sign-inverting synapses to rod bipolar cells, Strategies 649
which do not contact ganglion cells but send signals to The detail in a sketch is limited by dot size and spacing,
the cone pathways through an amacrine cell 608 and cones set the dot size in the central retina 649
Interactions among Bipolar Cells, Amacrine Cells, and The entire retinal image cannot be sketched in great
detail 652
Ganglion Cells 610
Most retinas are organized around points or lines 653
Bipolar cell terminals in the inner plexiform layer release
glutamate at synapses to amacrine or ganglion cells and Retinal sketches should be continuous, with no
receive inputs from amacrine cells 610 unnecessary blank spots 654
Bipolar cells terminate at different levels within the inner Tilings do not need to be regular, and tiles do not have to
plexiform layer, thereby creating functional be the same size 657
sublayers 611 Tilings formed by axonal or dendritic arbors at different
Amacrine cells vary in the extent over which they levels of the retina need not match precisely 659
promote lateral interactions among vertical pathways
and in the levels of the inner plexiform layer in which
Spatial Organization of the Retina 660
they operate 616 The fovea is a depression in the retina where the inner
Amacrine cells exert their effects mainly at glycine and retinal layers are absent 660
GABA synapses, while several other neurotransmitters
or neuromodulators play subsidiary roles 618

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 Contents xxi

The spatial distribution of a pigment in and around the The problem of understanding how the retina works can
fovea is responsible for entoptic images associated with be reduced to the problem of understanding its
the fovea 661 sampling units 698
Photoreceptor densities vary with respect to the center of The central representation of a sampling unit depends on
the fovea, where cones have their maximum density the number of ganglion cells it contains 698
and rods are absent 663
BOX 15.1 Locating Species of Molecules: Immunohisto-
The human retina varies from center to periphery in
terms of the spatial detail in the retinal sketch 664 chemistry 670
Maximum cone densities vary among different retinas by
a factor of three 666 Chapter 16 The Retina In Vivo and
The human retina has about 4.5 million cones and 91
million rods 666
the Optic Nerve 701
Blue cones have a different distribution than red and green Electrical Signals and Assessment of Retinal Function 702
cones have: the center of the fovea is dichromatic 667
A difference in electrical potential exists between the
There are more red cones than green cones, and more vitreal and choroidal surfaces of the retina and between
green cones than blue cones 668 the front and back of the eye 702
The distribution of different types of cones is neither The electroretinogram measures a complex change in
regular nor random 668 voltage in response to retinal illumination 702
Cone pedicles probably tile the retina in and near the The a-wave and off effect are generated by the photo-
fovea, but rod spherules probably never form a single- receptors, the c-wave by the pigment epithelium 703
layered tiling 672
The b-wave is either a direct reflection of ON bipolar cell
The pedicles of cones in and near the fovea are displaced activity or is indirectly related to their activity by a
radially outward from the cone inner segments, but secondary potential arising from Müller’s cells 704
spatial order is preserved 674
The ERG is useful as a gross indicator of photoreceptor
The density of horizontal cells is highest near the fovea function 706
and declines in parallel with cone density 675
Multifocal ERGs provide assessments of retinal function
Neither H1 nor H2 horizontal cells form tilings 676 within small areas of the retina 707
All types of cone and rod bipolar cells are distributed like
their photoreceptor types 676 The Retinal Vessels and Assessment of Retinal Health 708
The different types of bipolar cells provide different The retina in vivo is invisible 708
amounts of coverage with their dendrites 678 Since the choroidal circulation is usually not directly
All bipolar cell terminals form tilings at different levels in visible, irregularities and nonuniformities on the
the inner plexiform layer 679 fundus are commonly indicators of pathology 711
AII amacrine cells tile the retina, varying in density as The central retinal artery is an end-arterial system 712
ganglion cells do 681 The capillaries supplied by the central retinal artery
Medium- and large-field amacrine cells are low-density ramify in the inner two-thirds of the retina 713
populations whose processes generate high coverage Retinal detachment separates photoreceptors from their
factors 682 blood supply 714
Ganglion cell density declines steadily from the The foveal center lacks capillaries 715
parafovea to the periphery of the retina 685
Retinal capillaries are specialized to create a blood–retina
Midget and parasol ganglion cell dendrites tile at barrier 715
different levels in the inner plexiform layer 687
Retinal blood flow is autoregulated 717
Spatial resolution is limited by cone spacing in the fovea
and parafovea and by midget ganglion cells elsewhere The arterial and venous branches on the retinal surface
in the retina 690 can be distinguished ophthalmoscopically 717
Drainage of the inner retina is segmental 718
A Final Look at Three Small Pieces of Retina: Dots for the
Retinal Sketches 691 The Optic Nerve 719
A sampling unit is the smallest retinal region containing All ganglion cell axons and all branches of the central
at least one representative from each type of ganglion retinal artery and vein converge at the optic nerve
cell 691 head 719
Sampling units are smallest at the foveal center and are The nerve head and the optic nerve consist primarily of
dominated by cone signals 692 axon bundles separated by sheaths of glial cells and
connective tissue 719
Rods and blue cones become significant in the parafoveal
sampling units 694 The blood supply and drainage differ between the pre-
and postlaminar portions of the nerve head 721
Rods and rod pathways dominate in peripheral sampling
units 695

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xxii Contents

Ganglion cell axons form a stereotyped pattern as they Fusion of the optic stalks produces the optic chiasm,
cross the retina to the optic nerve head 722 where pioneering axons must choose the ipsilateral or
Axons from many widely separated ganglion cells are contralateral path 746
collected in bundles in the nerve fiber layer 723 The last stages of development in the optic nerve are
Axon bundles have an orderly arrangement in the nerve axon loss and myelination 746
head 724 The inner retina seems relatively immune to congenital
Scotomas observed in advanced stages of glaucoma anomalies 748
correspond to those produced by lesions along the The most common developmental anomalies are failures
superior and inferior temporal margin of the nerve to complete embryonic structures or eliminate transient
head 727 structures 748
The lamina cribrosa is weaker than the rest of the BOX 16.1 Fluorescein Angiography and the Adequacy
sclera 727
of Circulation 710
Field defects in glaucoma may be due to blockage of
axonal transport secondary to deformation of the
lamina cribrosa 728 Epilogue Time and Change 753
Ganglion cell loss in experimental glaucoma does not
appear to be selective by cell type or axon diameter 730 Postnatal Growth and Development 753
Development of the Retina and Optic Nerve 732 The newborn eye increases in overall size for the next 15
years 753
The retina develops from the two layers of the optic Refractive error is quite variable among newborn infants,
cup 732 but the variation decreases with growth 754
Retinal development proceeds from the site of the future Visual functions mature at different rates during the first
fovea to the periphery 733 6 years of life 756
Retinal neurons have identifiable birthdays 733 Changes in the lens and vitreous that begin in infancy
Ganglion cells, horizontal cells, and cones are the first continue throughout life 758
cells in the retina to be born 733
As distance from the fovea increases, the firstborn cells
Maturation and Senescence 759
appear at progressively later dates 735 The average refractive error is stable from ages 20 to 50,
Synapse formation has a center-to-periphery gradient but the eye becomes more hyperopic and then more
superimposed on a gradient from inner retina to outer myopic later in life 759
retina 736 Although the gross structure of the eye is stable after the
The location of the future fovea is specified very early; age of 20, tissues and membranes are constantly
the pit is created by cell migration 737 changing 760
Foveal cones are incomplete at birth 737 Retinal illuminance and visual sensitivity decrease with
age 761
Photoreceptor densities are shaped by cell migration and
retinal expansion 739 Visual acuity declines after age 50, largely because of
optical factors 763
Ganglion cell density is shaped by migration, retinal
expansion, and cell death 740
The spatial organization of the retina may depend on Historical References and Additional
specific cell–cell interactions and modifications of cell
morphology during development 741
Reading HR–1
Retinal blood vessels develop relatively late 743
Developing vessels are inhibited by too much Glossary G –1
oxygen 744
The optic nerve forms as tissue in the optic stalk is
replaced with developing ganglion cell axons and glial
Index I –1
cells 745

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