The Human Eye: Structure and Function - Sinauer Associates

ContentsPreface xxiiiAcknowledgments xxviiiPrologue A Brief History of Eyes 1The Antiquity of Eyes and Vision 1Thinking about the eye gave Charles Darwin “a cold shudder” 1The history of the eye is embedded in the history of animals andmolecules 2Several of the eye’s critical molecules are ancient 3Eyes were invented by multicellular animals almost 600 million yearsago 5Eyes arose not once, but numerous times, in different animal groups 6Eyes are most common in groups of motile animals living in lightedenvironments 8The Diversity and Distribution of Eyes 9The first step in vision is an eye that can sense the direction of incidentlight 9At least ten types of eyes can be distinguished by differences in theiroptical systems 11Vertebrates always have simple eyes, but invertebrates can havecompound eyes, simple eyes, or both 13Paths and Obstacles to Perfection 16Simple eyes improve as they become larger 16Elaborate simple eyes may have evolved rapidly 18Compound eyes have inherent optical limitations in theirperformance 19An Ocular Bestiary: Fourteen Eyes and Their Animals 21I. Compound eye—focal apposition, terrestrial variety: Honeybee(Apis mellifica) 21II. Compound eye—focal apposition, aquatic variety: Horseshoe crab(Limulus polyphemus) 23III. Compound eye—afocal apposition: Monarch butterfly (Danausplexippus) 26© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.ix

ContentsxiiiBOX 4.2 Changing the Effects of Extraocular MuscleContraction 152VIGNETTE 4.1 Locating the Extraocular Muscles 164VIGNETTE 4.2 In the Service of the Eye 184Chapter 5 The Nerves of the Eye andOrbit 191Elements of Neural Organization 191The brain deals with information about the externalworld and the body 191Neurons are the anatomical elements of neuralsystems 191Neural circuits consist of neurons linked mostly byunidirectional chemical synapses 193The direction of neural information flow distinguishesbetween sensory and motor nerves 194Motor outputs are divided anatomically and functionallyinto somatic and autonomic systems 194The autonomic system is subdivided into thesympathetic and parasympathetic systems 194The Optic Nerve and the Flow of Visual Information 195In the optic nerve, the location of axons from retinalganglion cells corresponds to their location on theretina 195Axons from the two optic nerves are redistributed in theoptic chiasm 198The decussation of axons in the chiasm is imperfect 199Spatial ordering of axons changes in the optic tracts 200In the lateral geniculate nuclei, which are primary targetsof axons in the optic tracts, inputs from the two eyes areseparated into different layers 200Axons terminating in the lateral geniculate nuclei arespatially ordered 201Some axons leave the optic tracts for otherdestinations 203Axons terminating in the superior colliculi formdiscontinuous retinotopic maps 204Axons forming the afferent part of the pupillary lightreflex pathway terminate in the pretectal nuclearcomplex 204Retinal inputs to the accessory optic system may helpcoordinate eye and head movement 205Retinal axons may provide inputs to a biologicalclock 205Lesions of the optic nerves and tracts produce defects inthe visual fields 207Lesions in the secondary visual pathways can beobserved only as motor deficits 212The Trigeminal Nerve: Signals for Touch and Pain 212Two of the three trigeminal divisions carry signals fromthe eye and surrounding tissues 212All somatosensory information from the eye is conveyedby the nasociliary nerve to the ophthalmic division ofthe trigeminal 213Sensory nerve fibers from the cornea, conjunctiva,limbus, and anterior sclera join to form the long ciliarynerves 213Stimulation of corneal or conjunctival nerve endingselicits sensations of touch or pain, a blink reflex, andreflex lacrimation 215Other sensory fibers from the eye are conveyed by theshort ciliary nerves and the sensory root of the ciliaryganglion 215Most other branches of the ophthalmic nerve carrysomatosensory fibers from the skin of the eyelids andface 215A few branches of the maxillary nerve pass through theorbit from the facial skin and the maxillary sinus 217Lesions in the branching hierarchy of the ophthalmicnerve produce anesthesia that helps identify the lesionsite 218Viral infection of the trigeminal system can producesevere corneal damage 219The Extraocular Motor Nerves 219The three cranial nerves that innervate the extraocularmuscles contain axons from clusters of cells in thebrainstem 219Cells in different parts of the oculomotor nerve nucleusinnervate the levator, the superior and inferior recti, themedial rectus, and the inferior oblique 219Axons destined for different muscles run together in theoculomotor nerve until it exits the cavernous sinus justbehind the orbit 221The oculomotor nerve contains parasympathetic fibersbound for the ciliary ganglion 224Cells in the trochlear nerve nucleus innervate thecontralateral superior oblique 224Abducens nerve cells innervate the ipsilateral lateralrectus 225All of the oculomotor nerves pass through the cavernoussinus on their way to the orbit 225The extraocular motor nerves probably contain sensoryaxons from muscle spindles and tendon organs 226Innervation of the Muscles of the Eyelids 226Three sets of muscles are associated with the eyelids 226The orbicularis is innervated by the facial nerve 227The superior and inferior tarsal muscles are innervatedby the sympathetic system 227Ptosis may result from either oculomotor or sympatheticlesions 228Autonomic Innervation of Smooth Muscle withinthe Eye 228The superior cervical ganglion is the source of mostsympathetic innervation to the eye 228© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

xivContentsSympathetic fibers enter the eye in the short ciliarynerves 230Sympathetic innervation of the dilator muscle acts atalpha-adrenergic receptors to dilate the pupils 230The arterioles in the uveal tract receive sympatheticinnervation that produces vasoconstriction 231Horner’s syndrome is the result of a central lesion in thesympathetic pathway 231Parasympathetic fibers entering the eye originate in theciliary or the pterygopalatine ganglion 231Axons from cells in the ciliary ganglion innervate thesphincter and the ciliary muscle 232Axons from the pterygopalatine ganglion cells innervatevascular smooth muscle in the choroid 233Accommodation and pupillary light reflexes shareefferent pathways from the Edinger–Westphal nuclei tothe eyes; pupillary reflexes are mediated by retinalsignals reaching the Edinger–Westphal nuclei throughthe pretectal complex 233Deficient pupillary reflexes may be associated withmidbrain lesions 234Innervation of the Lacrimal Gland 235Axons from cells in the pterygopalatine ganglion reachthe lacrimal gland via the zygomatic and lacrimalnerves 235The efferent pathway for lacrimal innervation begins inthe facial nerve nucleus 235Basal tear production may require tonic innervation ofthe lacrimal gland 236Some Issues in Neural Development 236Specialized growth cones guide the extension of axonsand dendrites 236Pathfinding by growth cones depends on recognition oflocal direction signs 237Target recognition and acquisition may require specificmarkers produced by the target cells 238Many early neurons are eliminated as mature patterns ofconnectivity are established 238Adult connectivity patterns are not always complete atbirth, and postnatal development is subject tomodification 239Ocular albinism is associated with a pathfinding error inthe development of optic nerve axons 239Anomalous innervation of the extraocular musclesmay be the result of pathfinding or target recognitionerrors 240Some forms of amblyopia may be related to problemswith postnatal establishment and maintenance ofsynaptic connections 240Innervation of the extraocular muscles begins early ingestation, sensory innervation much later 241Postnatal Neuron Growth and Regeneration 241Most postnatal neuron growth is interstitial growth 241Neurons do not undergo mitosis postnatally 242Spinal neurons in peripheral nerves can regenerate afterbeing damaged 242Central nervous system neurons do not regeneratefollowing major damage 242Corneal nerve endings will regenerate following localdamage 243Neuronal degeneration can affect other, undamaged neurons243VIGNETTE 5.1 The Integrative Action of the NervousSystem 196BOX 5.1 Tracing Neural Pathways: Degeneration andMyelin Staining 206VIGNETTE 5.2 Seeing One World with Two Eyes:The Problem of Decussation 210BOX 5.2 Tracing Neuronal Connections: AxonalTransport Methods 222Chapter 6 Blood Supply and Drainage 247Distributing Blood to Tissues 247Arteries control blood flow through capillary beds, andveins regulate blood volume 247Blood flow through capillary beds can be controlledlocally or systemically 248Capillary beds in a tissue may be independent orinterconnected 251The interchange between blood and cells depends partlyon the structure of the vascular endothelium 252Capillary endothelium is renewable, and capillary bedscan change 253Neovascularization is a response to altered functionaldemands 253Structurally weakened capillaries may be prone toexcessive neovascularization 254The Ophthalmic Artery and Ophthalmic Veins 255The ophthalmic artery distributes blood to the eye and itssurroundings 255Blood supplied to tissues by the ophthalmic artery isdrained to the cavernous sinus by the ophthalmicveins 257Supply and Drainage of the Eye 260Muscular arteries supply both the extraocular musclesand the anterior segment of the eye 260The anterior ciliary arteries contribute to the episcleraland intramuscular arterial circles 261The conjunctiva and corneal arcades are supplied bybranches from the episcleral arterial circle and drainedby the episcleral and anterior ciliary veins 262The system of episcleral veins drains the conjunctiva,corneal arcades, and limbus 263© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

ContentsxvThe posterior ciliary arteries divide into long and shortposterior ciliary arteries that supply differentregions 264The intramuscular and major arterial circles are formedin the ciliary body by branches from the anterior andlong posterior ciliary arteries 265Blood supply to the anterior segment is redundant, butthere is some segmentation in supply to the iris 268The short posterior ciliary arteries terminate in thechoriocapillaris, which supplies the retinalphotoreceptors 269The short posterior ciliary arteries contribute to thesupply of the optic nerve through the circle of Zinn 272The short posterior ciliary arteries sometimes contributeto the supply of the inner retina 274The central retinal artery enters the eye through the opticnerve and ramifies to supply the inner retina 275The central retinal vein exits the eye through the opticnerve 277The vortex veins drain most of the uveal tract 277The vortex veins have segmented drainage fields, butthey are heavily anastomotic 278Supply and Drainage of the Eyelids and SurroundingTissues 279The lacrimal gland is supplied by the lacrimal artery anddrained by lacrimal veins 279The eyelids are supplied by branches of the lacrimal,ophthalmic, facial, and infraorbital arteries 279The terminal branches of the ophthalmic artery leave theorbit to supply the skin and muscles of the face 282The infraorbital artery runs under the orbital floor 283The orbital veins are connected to the veins of the face,the pterygoid plexus, and the nose 283Development of the Ocular Blood Vessels 284Primitive embryonic blood vessels appear very early inthe eye’s development 284Several parts of the early ocular vasculature are transientand do not appear in the mature eye 284The anterior ciliary system forms later than the posteriorciliary system 287Remnants of normally transient, embryologicalvasculature may persist in the mature eye 287VIGNETTE 6.1 Circulation of the Blood 256BOX 6.1 Tracing Hidden Blood Vessels: VascularCasting 270VIGNETTE 6.2 Blood Vessels inside the Eye 280Chapter 7 The Eyelids and the LacrimalSystem 291Structure and Function of the Eyelids 291Structural rigidity of the lids is provided by the tarsalplates 291The tarsal plates are made of dense connective tissue inwhich glands are embedded 292The palpebral fissure is opened by muscles inserting ontoor near the edges of the tarsal plates 294The palpebral fissure is closed by contraction of theorbicularis 296Blinking may be initiated as a reflex response or as aregular, spontaneous action 298Lid movements during spontaneous blinks move tearsacross the cornea 299Overaction of the orbicularis may appear asblepharospasm or as entropion 299Paresis of the orbicularis produces ectropion andepiphora 300Other glands in the lids are associated with theeyelashes 301The skin on the lids is continuous with the conjunctivalining the posterior surface of the lids and covering theanterior surface of the sclera 302The orbital septum is a connective tissue sheet extendingfrom the orbital rim to the tarsal plates 303The shape and size of the palpebral fissure vary 304The overall structure of the lids consists of well-definedplanes or layers of tissue 306Tear Supply and Drainage 307Most of the tear fluid is supplied by the main lacrimalgland 307Secretion by the lacrimal gland is regulated by autonomicinputs operating through a second-messengersystem 308The composition of the lacrimal gland secretion varieswith the secretion rate 309Dry eye may result from a decreased amount of tears,abnormal tear composition, or both 310Tears are drained off at the medial canthus and depositedin the nasal cavity 311Pressure gradients created by contraction of theorbicularis during blinks move tears through thecanaliculi into the lacrimal sac 312Formation of the Eyelids and the Lacrimal System 315The eyelids first appear as folds in the surface ectoderm,which gives rise to the lid glands 315The lacrimal gland and the lacrimal drainage systemderive from surface ectoderm 316Most developmental anomalies in the eyelids andlacrimal system are problems in lid position or blockageof the drainage channels 318Anomalous innervation can produce eyelid movementslinked to contraction of muscles in the jaw 318© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

xviContentsPART TWOComponents of the EyeChapter 8 The Cornea and the Sclera 325Components and Organization of the Cornea andSclera 325The cornea, sclera, and limbus are made primarily ofcollagen fibrils 325Collagen is embedded in a polysaccharide gel that formsthe extracellular matrix 326The fibroblasts in the corneal and scleral stromaconstitute a small fraction of the stroma’s volume 327Collagen fibrils in the cornea are highly organized; thosein the sclera are not 328The structure of the corneal stroma is altered inBowman’s layer 331Corneal transparency is a function of its regularstructure 332Collagen organization in the stroma and cornealtransparency depend on intact epithelium andendothelium 334The corneal epithelium is a multilayered, renewablebarrier to water movement into the cornea 335The corneal endothelium is a single layer ofmetabolically active cells 339The endothelial cell tiling changes with time becausecells that die cannot be replaced 340Descemet’s membrane separates the endothelium fromthe stroma 345Nerve endings in the cornea give rise to sensations oftouch or pain, a blink reflex, and reflex lacrimation 347The epithelium contains a dense array of free terminalsof nerve fibers from the long ciliary nerves 347Corneal sensitivity can be measured quantitatively 349The dense innervation of the cornea makes it subject toviral infection 349The Cornea as a Refractive Surface 349The optical surface of the cornea is the precorneal filmcovering the surface of the epithelium 349The cornea’s outline is not circular, its thickness is notuniform, and its radius of curvature is not constant 351The shape of the cornea is determined by comparison toa sphere 353The cornea does not have a single, specifiable shape 354Contact lenses can affect corneal shape and structuredirectly or indirectly 356The shape and optical properties of the cornea can bepermanently altered 358Surgically reshaped corneas may change with time 359Corneal shape can be changed by removing tissue 360Stromal reshaping leaves the epithelium intact 361Corneal grafts are used to repair optically damagedcorneas 361Corneal Healing and Repair 365The epithelium heals quickly and completely 365Corneal healing may require limbal transplants 368Repair of damage to the stroma produces translucent scartissue 368The endothelium repairs itself by cell expansion andmigration 369Corneal graft incisions are repaired by the normalhealing processes 369Radial keratotomy incisions are repaired by epithelialhyperplasia and collagen formation 370Photorefractive keratectomy ablations are healed mostlyby the epithelium 371Growth and Development of the Cornea 371The epithelium and endothelium are the first parts of thecornea to appear 371The stroma is derived from neural crest cells associatedwith the mesoderm 372The regular arrangement of the stromal collagen appearssoon after collagen production begins 372Corneal growth continues for a few yearspostnatally 374Anomalous corneal development can produce misshapenor opaque corneas 375BOX 8.1 Biomicroscopy of the Cornea 342VIGNETTE 8.1 The Invisible Made Visible 350BOX 8.2 Some Reservations about Corneal RefractiveSurgery 362VIGNETTE 8.2 The Art of William Bowman 366Chapter 9 The Limbus and the AnteriorChamber 379The Anterior Chamber and Aqueous Flow 379The anterior chamber is the fluid-filled space between thecornea and the iris 379The angle of the anterior chamber varies inmagnitude 380Aqueous is formed by the ciliary processes and enters theanterior chamber through the pupil 381Aqueous drains from the eye at the angle of the anteriorchamber 383Intraocular pressure depends on the rate of aqueousproduction and the resistance to aqueous outflow 385The Anatomy of Aqueous Drainage 390The scleral spur is an anchoring structure for parts of thelimbus and the ciliary body 390The trabecular meshwork is made of interlaced cords oftissue extending from the apex of the angle to themargin of the cornea 392Schwalbe’s ring separates the trabecular meshwork fromthe cornea 393© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

ContentsxviiThe trabecular cords have a collagen core wrapped withendothelial cells 393The major source of outflow resistance is the juxtacanaliculartissue separating the canal of Schlemm fromthe trabecular spaces 395The canal of Schlemm encircles the anterior chamberangle 395Aqueous enters the canal of Schlemm by way of largevacuoles in the endothelial lining of the canal 397Aqueous drains out of the canal into venous plexuses inthe limbal stroma 399Pilocarpine reduces intraocular pressure, probably by aneffect of ciliary muscle contraction on the structure ofthe trabecular meshwork 400An effective way to reduce intraocular pressure seems tobe to increase the uveoscleral outflow 402Surgery for glaucoma aims to increase aqueousoutflow 402The outer surface of the limbus is covered with episcleraltissue and a heavily vascularized conjunctiva 403Development of the Limbus 405The anterior chamber is defined by the iris growingbetween the developing cornea and lens 405The angle of the anterior chamber opens duringdevelopment as the root of the iris shiftsposteriorly 406The trabecular meshwork develops between the fourthand eighth months 408Most developmental anomalies in the limbus areassociated with structural anomalies that affect otherparts of the anterior chamber 408BOX 9.1 Through the Looking Glass: Gonioscopy 382BOX 9.2 Estimating the Pressure Within:Tonometry 388Chapter 10 The Iris and the Pupil 411Functions of the Iris and Pupil 411The iris is an aperture stop for the optical system of theeye 411The entrance pupil is a magnified image of the realpupil 412Variation of pupil size changes the amount of lightentering the eye, the depth of focus, and the quality ofthe retinal image 413Pupil size varies with illumination level, thereby helpingthe retina cope with large changes in illumination 414Pupil size varies with accommodation andaccommodative convergence 416The pupillary near response is smaller in children than inadults 417The pupil is in constant motion, and it reacts quickly tochanges in retinal illumination 418Decreased iris pigmentation in ocular albinism affects theoptical function of the iris 419Structure of the Iris 420The pupils in the two eyes are normally the same sizeand are decentered toward the nose 420The iris is constructed in layers and regional differencesin the iris are related to the different muscles withinthem 421The anterior border layer is an irregular layer ofmelanocytes and fibroblasts interrupted by largeholes 422The iris stroma has the same cellular components as theanterior border layer, but loosely arranged 423Small blood vessels run radially through the stroma,anastomosing to form the minor arterial circle andsupply the iris muscles 425The sphincter and dilator occupy different parts of theiris and have antagonistic actions 426The sphincter is activated by the parasympatheticsystem, the dilator by the sympathetic system 427The anterior pigmented epithelium is a myoepithelium,forming both the epithelial layer and the dilatormuscle 428The posterior epithelial cells contact the anterior surfaceof the lens 430Surgery for closed-angle glaucoma often involves the irisrather than the limbus 432Some Clinically Significant Anomalies of the Iris andPupil 432Changes in iris color after maturity are potentiallypathological 432Differences between the two eyes in pupil size orpupillary responses to light are commonly associatedwith neurological problems 433Anisocoria and unresponsive pupils are often associatedwith defects in the efferent part of the innervationalpathways 435Clinically useful drugs affecting pupil size fall into fourfunctional groups 437Development of the Iris 440The iris stroma forms first by migration ofundifferentiated neural crest cells 440The epithelial layers and the iris muscles develop fromthe rim of the optic cup and are therefore ofneuroectodermal origin 440The pupil is the last feature of the iris to appear 442Most postnatal development of the iris is an addition ofmelanin pigment 443Segmental defects and holes in the iris result fromunsynchronized or failed growth of the optic cup rim 443An ectopic pupil is improperly centered in an otherwisenormal iris 445A persistent pupillary membrane may be the result ofeither insufficient tissue atrophy or tissuehyperplasia 445© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

xviiiContentsChapter 11 The Ciliary Body and theChoroid 447Anatomical Divisions of the Ciliary Body 447The ciliary processes characterize the pars plicata 447The ciliary muscle extends through both pars plicata andpars plana 449The Ciliary Processes and Aqueous Formation 449The ciliary processes are mostly filled with bloodvessels 449The capillaries in the ciliary processes are highlypermeable 451Two layers of epithelium lie between the capillaries andthe posterior chamber 452Aqueous formation involves metabolically driventransport systems 452The ciliary epithelium is anatomically specialized as ablood–aqueous barrier 454Ions are transported around the band of tight junctions toproduce an osmotic gradient in the basal folds of theunpigmented epithelium 455Aqueous production varies during the day and declineswith age 456The major classes of drugs used to reduce aqueousproduction interact either with adrenergic membranereceptors or with the intracellular formation ofbicarbonate ions 458The pars plana is covered by epithelial layers that arecontinuous with the epithelial layers of the parsplicata 459The Ciliary Muscle and Accommodation 461The ciliary muscle has three parts with a complexgeometry 461Contraction of the ciliary muscle produces movementinward toward the lens so that the muscle behaves likea sphincter 463The zonule provides a mechanical linkage betweenciliary muscle and lens 465Accommodation is a result of ciliary musclecontraction 468The primary stimulus to accommodation is retinal imageblur 469Accommodative amplitude decreases progressively withage 472Presbyopia is not a consequence of reduced innervationto the ciliary muscle 473Aging of the ciliary muscle is unlikely to be a significantfactor in presbyopia 474The Choroid 477The choroidal stroma consists of loose connective tissueand dense melanin pigment 477Blood vessels that supply and drain the capillary bedsupplying retinal photoreceptors make up the mainpart of the choroid 478The choriocapillaris is heavily anastomotic but has localfunctional units 479The choriocapillaris varies in capillary density and in theratio of arterioles to venules 480Capillaries in the choriocapillaris are specialized forease of fluid movement across the capillaryendothelium 481Bruch’s membrane lies between capillaries andpigmented epithelium in both the choroid and the parsplana of the ciliary body 481Development of the Ciliary Body and Choroid 482The ciliary epithelium arises from the optic cup, theciliary muscle from neural crest cells 482Formation of the ciliary epithelium may be induced bythe lens 483Formation of the ciliary muscle may be induced by theciliary epithelium 484The ciliary muscle begins to form during the fourthmonth and continues to develop until term 485The muscles associated with the eye originate fromdifferent germinal tissues 486The ciliary processes form in synchrony with the vascularsystem in the ciliary body 486The zonule is produced by the ciliary epithelium 486The choroidal vasculature has two developmentalgradients: center to periphery and inside to outside 488VIGNETTE 11.1 The Source 470Chapter 12 The Lens and the Vitreous 491Structure of the Lens 492Some unusual proteins, the crystallins, are the dominantstructural elements in the lens 492Dense, uniform packing of the crystallins within lenscells is responsible for lens transparency 494Crystallins are highly stable molecules, making themsome of the oldest proteins in the body, but they can bechanged by light absorption and altered chemicalenvironments 494a-Crystallins may play a special role in maintainingnative crystallin structure over time 496The lens is formed of long, thin lens fibers arranged inconcentric shells to form a flattened spheroid 497Lens fibers in each shell meet anteriorly and posteriorlyalong irregular lines 498Lens shells are bound together with miniature locks andkeys, a kind of biological Velcro 499The anterior epithelium is the source of new cells for thelens 501Elongating epithelial cells at the equator become longlens fibers that form new shells in the lens 503The size of the lens and the number of lens fibersincrease throughout life 503Each new lens shell has one more fiber than the previousshell and about five new shells are added each yearafter the age of five 504© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

ContentsxixAn aged lens has about 2500 shells and 3.6 million lensfibers 505The lens capsule encloses the lens shells andepithelium 507The locations at which the zonule inserts onto the lenschange with age 510The Lens as an Optical Element 513The refractive index of the ocular lens varies from onepart of the lens to another 513Lens transparency is related not only to proteinregularity but also to water content, which ismaintained by ion pumping in the epithelium 514The lens contains several different optical zones 515The lens surfaces are parabolic and therefore flattengradually from the poles to the equator 516Both anterior and posterior lens surfaces become morecurved with accommodation, but the anterior surfacechange is larger 519The lens thickens with age and its curvatures increase, butunaccommodated lens power does not increase withage 520The increased lens surface curvatures in accommodationare primarily a consequence of tissue elasticity 522The presbyopic lens is aging, fat, and unresponsive 523Presbyopia is largely, if not solely, associated with agerelatedchanges in the lens 525Cataracts, most of which are age-related, take differentforms and can affect any part of the lens 526The Vitreous 530The vitreous is the largest component of the eye 530The primary structural components of the vitreous arecollagen and hyaluronic acid 530The external layer of the vitreous—the vitreous cortex—attaches the vitreous to surrounding structures 532Inhomogeneity of the vitreous structure producesinternal subdivisions in the vitreous 533The vitreous changes with age 533Shrinkage of the vitreous gel may break attachments tothe retina 536Altered activity of cells normally present in the vitreousor the introduction of cells from outside the vitreousmay produce abnormal collagen production and scarformation 537Vitrectomy removes abnormal portions of thevitreous 538Development of the Lens and Vitreous 539The lens forms from a single cell line 539Most failures of lens development are manifest ascongenital cataracts 540The primary vitreous forms around the embryonichyaloid artery 541The secondary vitreous, initially acellular, forms outsidethe vasa hyaloidea propria 541Most developmental anomalies in the vitreous representincomplete regression of the hyaloid artery system 541VIGNETTE 12.1 Putting the Lens in Its ProperPlace 512BOX 12.1 Cataract Surgery 528Chapter 13 Retina I: Photoreceptors andFunctional Organization 545The Retina’s Role in Vision 545The retina detects light and tells the brain about aspectsof light that are related to objects in the world 545Objects are defined visually by light and by variations inlight reflected from their surfaces 546The retina makes sketches of the retinal image fromwhich the brain can paint pictures 547Functional Organization of the Retina 549Photoreceptors catch photons and produce chemicalsignals to report photon capture 549Photoreceptor signals are conveyed to the brain bybipolar and ganglion cells 551Lateral pathways connect neighboring parts of theretina 552Recurrent pathways may assist in adjusting thesensitivity of the retina 554The retina has anatomical and functional layers 555Catching Photons: Photoreceptors and TheirEnvironment 560Each photoreceptor contains one of four photopigments,each of which differs in its spectral absorption 560Color vision requires more than one photopigment 562The photopigments are stacked in layers within the outersegments of the photoreceptor 564Light absorption produces a structural change in thephotopigments 565Structural change in the photopigment activates anintracellular second-messenger system using cGMP asthe messenger 566A decrease in cGMP concentration closes cation channels,decreases the photocurrent, and hyperpolarizes thephotoreceptor 568Absorption of one photon can produce a detectable rodsignal 570Photocurrent in the outer segment decreases inproportion to the number of absorbed photons 572Photopigments activated by photon absorption areinactivated, broken down, and then regenerated 573Photoreceptor sensitivity is modulated by intracellularCa 2+ 575Changes in photoreceptor sensitivity account for lessthan half of the retina’s sensitivity increase in the darkand sensitivity decrease in the light 578© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

ContentsxxiThe spatial distribution of a pigment in and around thefovea is responsible for entoptic images associated withthe fovea 661Photoreceptor densities vary with respect to the center ofthe fovea, where cones have their maximum densityand rods are absent 663The human retina varies from center to periphery interms of the spatial detail in the retinal sketch 664Maximum cone densities vary among different retinas bya factor of three 666The human retina has about 4.5 million cones and 91million rods 666Blue cones have a different distribution than red and greencones have: the center of the fovea is dichromatic 667There are more red cones than green cones, and moregreen cones than blue cones 668The distribution of different types of cones is neitherregular nor random 668Cone pedicles probably tile the retina in and near thefovea, but rod spherules probably never form a singlelayeredtiling 672The pedicles of cones in and near the fovea are displacedradially outward from the cone inner segments, butspatial order is preserved 674The density of horizontal cells is highest near the foveaand declines in parallel with cone density 675Neither H1 nor H2 horizontal cells form tilings 676All types of cone and rod bipolar cells are distributed liketheir photoreceptor types 676The different types of bipolar cells provide differentamounts of coverage with their dendrites 678All bipolar cell terminals form tilings at different levels inthe inner plexiform layer 679AII amacrine cells tile the retina, varying in density asganglion cells do 681Medium- and large-field amacrine cells are low-densitypopulations whose processes generate high coveragefactors 682Ganglion cell density declines steadily from theparafovea to the periphery of the retina 685Midget and parasol ganglion cell dendrites tile atdifferent levels in the inner plexiform layer 687Spatial resolution is limited by cone spacing in the foveaand parafovea and by midget ganglion cells elsewherein the retina 690A Final Look at Three Small Pieces of Retina: Dots for theRetinal Sketches 691A sampling unit is the smallest retinal region containingat least one representative from each type of ganglioncell 691Sampling units are smallest at the foveal center and aredominated by cone signals 692Rods and blue cones become significant in the parafovealsampling units 694Rods and rod pathways dominate in peripheral samplingunits 695The problem of understanding how the retina works canbe reduced to the problem of understanding itssampling units 698The central representation of a sampling unit depends onthe number of ganglion cells it contains 698BOX 15.1 Locating Species of Molecules: Immunohistochemistry670Chapter 16 The Retina In Vivo andthe Optic Nerve 701Electrical Signals and Assessment of Retinal Function 702A difference in electrical potential exists between thevitreal and choroidal surfaces of the retina and betweenthe front and back of the eye 702The electroretinogram measures a complex change involtage in response to retinal illumination 702The a-wave and off effect are generated by the photoreceptors,the c-wave by the pigment epithelium 703The b-wave is either a direct reflection of ON bipolar cellactivity or is indirectly related to their activity by asecondary potential arising from Müller’s cells 704The ERG is useful as a gross indicator of photoreceptorfunction 706Multifocal ERGs provide assessments of retinal functionwithin small areas of the retina 707The Retinal Vessels and Assessment of Retinal Health 708The retina in vivo is invisible 708Since the choroidal circulation is usually not directlyvisible, irregularities and nonuniformities on thefundus are commonly indicators of pathology 711The central retinal artery is an end-arterial system 712The capillaries supplied by the central retinal arteryramify in the inner two-thirds of the retina 713Retinal detachment separates photoreceptors from theirblood supply 714The foveal center lacks capillaries 715Retinal capillaries are specialized to create a blood–retinabarrier 715Retinal blood flow is autoregulated 717The arterial and venous branches on the retinal surfacecan be distinguished ophthalmoscopically 717Drainage of the inner retina is segmental 718The Optic Nerve 719All ganglion cell axons and all branches of the centralretinal artery and vein converge at the optic nervehead 719The nerve head and the optic nerve consist primarily ofaxon bundles separated by sheaths of glial cells andconnective tissue 719The blood supply and drainage differ between the preandpostlaminar portions of the nerve head 721© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.

xxiiContentsGanglion cell axons form a stereotyped pattern as theycross the retina to the optic nerve head 722Axons from many widely separated ganglion cells arecollected in bundles in the nerve fiber layer 723Axon bundles have an orderly arrangement in the nervehead 724Scotomas observed in advanced stages of glaucomacorrespond to those produced by lesions along thesuperior and inferior temporal margin of the nervehead 727The lamina cribrosa is weaker than the rest of thesclera 727Field defects in glaucoma may be due to blockage ofaxonal transport secondary to deformation of thelamina cribrosa 728Ganglion cell loss in experimental glaucoma does notappear to be selective by cell type or axon diameter 730Development of the Retina and Optic Nerve 732The retina develops from the two layers of the opticcup 732Retinal development proceeds from the site of the futurefovea to the periphery 733Retinal neurons have identifiable birthdays 733Ganglion cells, horizontal cells, and cones are the firstcells in the retina to be born 733As distance from the fovea increases, the firstborn cellsappear at progressively later dates 735Synapse formation has a center-to-periphery gradientsuperimposed on a gradient from inner retina to outerretina 736The location of the future fovea is specified very early;the pit is created by cell migration 737Foveal cones are incomplete at birth 737Photoreceptor densities are shaped by cell migration andretinal expansion 739Ganglion cell density is shaped by migration, retinalexpansion, and cell death 740The spatial organization of the retina may depend onspecific cell–cell interactions and modifications of cellmorphology during development 741Retinal blood vessels develop relatively late 743Developing vessels are inhibited by too muchoxygen 744The optic nerve forms as tissue in the optic stalk isreplaced with developing ganglion cell axons and glialcells 745Fusion of the optic stalks produces the optic chiasm,where pioneering axons must choose the ipsilateral orcontralateral path 746The last stages of development in the optic nerve areaxon loss and myelination 746The inner retina seems relatively immune to congenitalanomalies 748The most common developmental anomalies are failuresto complete embryonic structures or eliminate transientstructures 748BOX 16.1 Fluorescein Angiography and the Adequacyof Circulation 710Epilogue Time and Change 753Postnatal Growth and Development 753The newborn eye increases in overall size for the next 15years 753Refractive error is quite variable among newborn infants,but the variation decreases with growth 754Visual functions mature at different rates during the first6 years of life 756Changes in the lens and vitreous that begin in infancycontinue throughout life 758Maturation and Senescence 759The average refractive error is stable from ages 20 to 50,but the eye becomes more hyperopic and then moremyopic later in life 759Although the gross structure of the eye is stable after theage of 20, tissues and membranes are constantlychanging 760Retinal illuminance and visual sensitivity decrease withage 761Visual acuity declines after age 50, largely because ofoptical factors 763Historical References and AdditionalReading HR–1Glossary G–1Index I–1© Sinauer Associates, Inc. This material cannot be copied, reproduced, manufacturedor disseminated in any form without express written permission from the publisher.