The Eye

By | December 23, 2014

The eye (organum visus) develops as a neuroectodermal outgrowth of the embryonic prosencephalon that contacts surface ectoderm and is enveloped by induced mesodermal and neural crest mesenchyme. The definitive eye and its adnexa are contained within an orbit that is only partly bony. Associated with the bulb of the eye are extraocular muscles that move it; periorbital fascia and fat that surround and cushion it; eyelids and conjunctivae that protect it; and a lacrimal apparatus that keeps its surface moist, provides the first barrier to infection, and helps to nourish the cornea.

As a consequence of its dual origin, the eye has both central and peripheral neural elements. The optic nerve is a central nervous system structure with myelin formed by oligodendroglial cells, whereas the nerves of the extraocular muscles and iris are peripheral nervous system structures with lemmocyte (Schwann cell) sheaths for myelin. The vascular and fibrous tunics surrounding the optic nerve are homologous to the meninges surrounding the brain and spinal cord. The intervaginal space of the optic nerve is continuous with the subarachnoid space of the brain and contains cerebrospinal fluid.

There is considerable variation between breeds in regard to the position of the eyes, the size of the orbit, and the size and shape of the palpebral opening.

Development

Aguirre et al. (1972) studied the early development of the dog’s eye and its adnexa from day 15 to functional maturity using serially sectioned embryos in the Cornell University Collection. Subsequent studies involved histologic examination of fetuses removed from the uterus 25, 28, 30, 33, and 35 days post coitum.

The first indication of the formation of the eye is seen as an optic sulcus on the neural fold rostral to the notochord on each side. The neuroectoderm surrounding this sulcus proliferates rostrolaterally to form the optic vesicle, a hollow diverticulum of the prosencephalon. As the optic vesicle forms, its caudal surface is contacted by mesodermal mesenchyme and its peripheral surface is surrounded by superficial ectoderm. Shortly thereafter, migrating neural crest cells contribute to the forming vesicle and future orbital tissues. The anterior portion of the vesicle invaginates to form an optic cup with the concomitant formation of the lens placode in the adjacent surface ectoderm. The optic cup assumes a rounded appearance by day

30. There is an optic fissure along the ventral meridian where the lateral and medial folds of the optic cup meet and eventually fuse. The occurrence of the fissure allows for the penetration of the vascular mesoderm. Failure of the fissure to close results in defects of one or more of the tunics of the eye (colobomata). Such defects are common in the Collie breed as part of the heritable Collie eye syndrome.

The connection of the optic cup to the brainstem lengthens and attenuates as growth proceeds, forming the optic stalk, which will later become the optic nerve. Anteriorly, the optic vesicle induces the overlying surface ectoderm to proliferate, forming the lens placode, which is present by gestational day 15. As the optic vesicle invaginates, the placode also invaginates into the optic cup. By day 25, it pinches off from the surface ectoderm to form the lens vesicle, the anlage of the crystalline lens. The first anlage of the lens capsule is evident by day 25. The remaining surface ectoderm becomes the epithelium of the cornea. The deeper stromal and posterior epithelial layers of the cornea are derived from neural crest mesenchymal cells.

The hyaloid artery is present at day 25, arising from the mesenchyme surrounding the optic cup. It enters the posterior end of the optic fissure to supply the inner surface of the cup and the mesenchyme filling the optic cup becomes the primary vitreous. The hyaloid artery grows anteriorly and reaches the posterior lens surface by day 28, where it branches extensively to form the posterior portion of the tunica vasculosa lentis, a plexus of vessels derived from the anterior ciliary vessels that completely surrounds the lens by day 30. Secondary vitreous, secreted by the glial component consisting of Müller cells within the inner layer of the optic cup, surrounds the primary vitreous beginning at approximately gestational day 26. With the growth of the eyeball, the secondary vitreous continues to elaborate and the primary vitreous becomes reduced to a narrow funnel (Cloquet canal) between the optic nerve and posterior lens surface. The hyaloid vessels between the optic disc and lens begin to atrophy at approximately day 45 with remnants commonly present until 10 or 11 days after birth. The retinal arteries of the adult are derived from the portion of the hyaloid vasculature that supplied the inner layer of the optic cup.

The anterior face of the lens and primordial iris are supplied by the anterior portion of the tunica vasculosa lentis. The portion of the vascular tunic supplying the lens also atrophies late in gestation so that the lens is normally avascular at birth and in adult life.

The cavity of the optic vesicle, originally continuous with the third ventricle of the brain, is obliterated on approximately day 33, when the inner and outer walls of the optic cup fuse. The outer layer becomes the retinal pigment epithelium. The inner layer proliferates to form all layers of the neurosensory retina. Axons from the ganglion cells of the innermost layer grow toward the optic stalk, which they invade on approximately gestational day 30, and follow toward the brainstem.

Maturation of the retina proceeds from central to peripheral and is not complete until 8 weeks after birth.

By day 25, the primary vitreous body contains amorphous fibrillar material and no cellular components except for vascular elements. By day 30, the vitreous body consists of randomly oriented fibrillar structures and some loose cells with cytologic characteristics of fibroblasts. Subsequently, the primitive vitreous body becomes increasingly more confined to the central part of the vitreal space. By day 33, the vitreous body is avascular at the periphery, becoming the definitive or secondary vitreous body. At day 35 the primary vitreous body is an empty space with few hyalocytes and almost no hyaloid vasculature.

The epithelia of the ciliary body and the posterior surface of the iris are also derived from the neuroectoderm of the inner layer of the optic cup, but are nonvisual (pars ceca retinae). The richly vascular mesenchyme surrounding the anterior tunica vasculosa lentis forms the stroma of the iris. The central area of the iris (pupillary membrane) is thin and normally completely atrophies by 14 days after birth, forming the pupil. Incomplete atrophy, resulting in persistent pupillary membranes, has been observed as a heritable defect in Basenji dogs. The dilator and sphincter muscles of the iris differentiate from the neuroectodermal pars iridica retinae.

Rarefaction of the mesenchyme between that which forms the stroma of the iris and that which forms the substantia propria and posterior epithelium of the cornea is evident by day 45. Progressive rarefaction forms a cavity that fills with aqueous humor to become the anterior chamber of the adult eye.

The mesenchyme (much of which is neural crest in origin) adjacent to the optic cup is induced by the outer layer of the cup to form the richly vascular tunica vasculosa bulbi. This vascular tunic comprises the iris, ciliary body, and choroid. At the periphery of the lens, the vascular mesenchyme proliferates into the folds, ciliary processes, of the ciliary body. Fibers form from the nonpigmented epithelium of the ciliary body and extend to the lens equator. These elongate as the globe increases in size to form the definitive zonula ciliaris, the suspensory ligament of the lens. Neural crest cells form the ciliary muscle fibers of the ciliary body. Contraction of these muscles is thought to relax tension on the zonula fibers, allowing the lens to become rounder, increasing its refractive power for near vision (accommodation). As the anterior optic cup develops in unison with the mesenchyme to create the iris, ciliary body, and suspensory ligament of the lens, the posterior chamber is formed.

External to the vascular tunic, the mesenchyme (primarily of neural crest origin) condenses to form the fibrous sclera, which is homologous to the dura mater of the brain. Neural crest cells are the source of the posterior corneal epithelial cells of the cornea as well as stromal fibroblasts (keratocytes). The extraocular muscles are derived from somitomere mesoderm caudal to the developing eye vesicle. Although the myofibers of these muscles are mesodermal, the connective tissues associated with them are of neural crest origin. Gilbert (1947) demonstrated that the extrinsic ocular muscles of the cat arise from three distinct but closely approximated anlagen that are homologous with the premandibular, mandibular, and hyoid head cavities of lower vertebrates. The same is probably true for the dog.

The eyelids appear as folds superior and inferior to the eye on approximately day 25 of gestation. These enlarge, grow over the cornea, and narrow the palpebral fissure by approximately half on day 35. The eyelids completely cover the cornea and fuse by day 40. The superficial musculature of the lids, the m. orbicularis oculi, forms from the platysma sheet and is recognizable by approximately day 40. Huber (1922) has described the postnatal development of the platysma derivatives.

Dogs are born with the lid margins still adherent to one another. Final maturation of the eye occurs after birth; most notable are changes in the retina, iridocorneal angle, corneal epithelium, and tapetum. The fused lids normally separate approximately 2 weeks postpartum, and the palpebral fissure is able to be opened. Premature separation of the lids results in severe ophthalmitis, apparently as a result of the immaturity of the lacrimal apparatus.

The retina of the dog, as in many precocial species, is not fully developed at birth. Differentiation of the multicellular inner layer of the optic cup into inner (marginal) and outer (nucleated) layers to form the precursor of the sensory retina does not occur until embryonic days 25-28. Intracellular pigment granules may be observed at the periphery of the outer layer near the ora serrata, which will later form the pigment epithelium. By day 30, the anterior part of the pigment epithelium consists of cells arranged in pseudostratified columnar fashion and the nerve fiber layer may be observed at the posterior pole of the retina. The inner and outer neuroblastic layers of the retina may be distinguished posterior to the equator by day 30. In the posterior region, the nerve fiber layer becomes prominent and the axons join to form the optic nerve. By day 35, the retinal pigment epithelium becomes pigmented posterior to the equator of the optic cup. The photoreceptors are not developed until approximately 16 to 35 days after birth. This lag in photoreceptor maturation is reflected by the electrical activity of the retina in response to photic stimulation. Vascularization of the retina occurs postnatally.

The Eyeball

The Eye As An Optical Device

Eyelids

Lacrimal Apparatus

Muscles

Innervation

Vasculature

Comparative Ophthalmology

Major works in comparative ophthalmology include Walls (1942), Rochon-Duvigneaud (1943), Polyak (1957), Prince (1956), Duke-Elder (1958), Prince et al. (1960), Smythe (1961), Crescitelli (1977), and Cronly-Dillon and Gregory (1991) and Schwab (2011). A full-color atlas of comparative ophthalmoscopy is also available, and an expanding number of color atlases of veterinary ophthalmology have been published. Ocular histology and fine structure are superbly treated in the text by Hogan et al. (1971).