Essentials of Veterinary Ophthalmology. Kirk N. Gelatt

growth of the optic cup epithelial layers results in folding of the inner layer, representing early, anterior ciliary processes. The ciliary body epithelium develops from the neuroectoderm of the anterior optic cup, and the underlying mesenchyme differentiates into the ciliary muscles. Extracellular matrix secreted by the ciliary epithelium becomes the tertiary vitreous and, ultimately, develops into lens zonules.

      The three phases of iridocorneal angle (ICA) maturation include (i) the separation of anterior mesenchyme into corneoscleral and iridociliary regions (i.e., trabecular primordium formation), followed by differentiation of ciliary muscle and folding of the neural ectoderm into ciliary processes; (ii) the enlargement of the corneal trabeculae and development of clefts in the area of the trabecular meshwork; and (iii) the postnatal remodeling of the drainage angle, associated with cellular necrosis and phagocytosis by macrophages, resulting in opening of clefts in the trabecular meshwork and outflow pathways.

      In species born with congenitally fused eyelids (i.e., dog and cat), development of the anterior chamber continues during this postnatal period before eyelid opening. At birth, the peripheral iris and cornea are in contact with maturation of pectinate ligaments by three weeks and rarefaction of the uveal and corneoscleral trabecular meshworks to their adult state during the first eight weeks after birth.

Retina and Optic Nerve Development

Infolding of the neuroectodermal optic vesicle results in a bilayered optic cup with the apices of these two cell layers in direct contact. Primitive optic vesicle cells are columnar, but by 20 days of gestation in the dog, they form a cuboidal layer containing the first melanin granules in the developing embryo. The neurosensory retina develops from the inner nonpigmented layer of the optic cup and the retinal pigment epithelium (RPE) originates from the outer, pigmented layer. Bruch's membrane (the basal lamina of the RPE) is first seen during this time, and becomes well developed over the next week, when the choriocapillaris is developing. By day 45, the RPE cells take on a hexagonal cross‐sectional shape and develop microvilli that interdigitate with projections from photoreceptors of the nonpigmented (inner) layer of the optic cup.

      At the time of lens placode induction, the retinal primordium consists of an outer, nuclear zone and an inner, marginal (anuclear) zone. This process forms the inner and outer neuroblastic layers, separated by their cell processes that make up the transient fiber layer of Chievitz. Cellular differentiation progresses from inner to outer layers and, regionally, from central to peripheral locations. Peripheral retinal differentiation may lag behind that occurring in the central retina by three to eight days in the dog. Retinal ganglion cells develop first within the inner neuroblastic layer, and axons of the ganglion cells collectively form the optic nerve. Cell bodies of the Müller and amacrine cells differentiate in the inner portion of the outer neuroblastic layer. Horizontal cells are found in the middle of this layer; the bipolar cells and photoreceptors mature last, in the outermost zone of the retina.

      Significant retinal differentiation continues postnatally, particularly in species born with fused eyelids. At birth, the canine retina has reached a stage of development equivalent to the human at three to four months of gestation. In the kitten, all ganglion cells and central retinal cells are present at birth with continued proliferation in the peripheral retina continuing during the first two to three postnatal weeks in dogs and cats.

Sclera, Choroid, and Tapetum

      These neural crest‐derived tissues are all induced by the outer layer of the optic cup (future RPE). Normal RPE differentiation is a prerequisite for normal development of the sclera and choroid. The choroid and sclera are relatively differentiated at birth, but the tapetum in dogs and cats continues to develop and mature during the first four months postnatally.

Vitreous

      The primary vitreous forms posteriorly, between the primitive lens and the inner layer of the optic cup. In addition to the vessels of the hyaloid system, the primary vitreous also contains mesenchymal cells, collagenous fibrillar material, and macrophages. Primitive hyalocytes produce collagen fibrils that expand the volume of the secondary vitreous.

      The tertiary vitreous forms as a thick accumulation of collagen fibers between the lens equator and the optic cup. These fibers are called the marginal bundle of Drualt, or Drualt's bundle. Drualt's bundle has a strong attachment to the inner layer of the optic cup, and it is the precursor to the vitreous base and lens zonules. The early lens zonular fibers appear to be continuous with the inner, limiting membrane of the nonpigmented epithelial layer covering the ciliary muscle. Atrophy of the primary vitreous and hyaloid leaves a clear, narrow central zone, which is called Cloquet's canal.

Optic Nerve

Axons from the developing ganglion cells pass through vacuolated cells from the inner wall of the optic stalk. A glial sheath forms around the hyaloid artery. As the hyaloid artery regresses, the space between the hyaloid artery and the glial sheath enlarges. Bergmeister's papilla represents a remnant of these glial cells around the hyaloid artery. Glial cells migrate into the optic nerve and form the primitive optic disc. The glial cells around the optic nerve and the glial part of the lamina cribrosa come from the inner layer of the optic stalk, which is of neural ectoderm origin. Later, a mesenchymal (neural crest origin) portion of the lamina cribrosa develops. Myelinization of the optic nerve begins at the chiasm, progresses toward the eye, and reaches the optic disc after birth.

Eyelids

      The eyelids develop from surface ectoderm, which gives rise to the epidermis, cilia, and conjunctival epithelium. Neural crest mesenchyme gives rise to deeper structures, including the dermis and tarsus. The eyelid muscles (i.e., orbicularis and levator) are derived from craniofacial condensations of mesoderm called somitomeres. The upper eyelid develops from the frontonasal process; the lower eyelid develops from the maxillary process. The lid folds grow together and elongate to cover the developing eye. The upper and lower lids fuse on day 32 of gestation in the dog. Separation occurs two weeks postnatally.

Extraocular Muscles

      The extraocular muscles (EOM) arise from mesoderm in somitomeres (i.e., preoptic mesodermal condensations). Spatial organization of developing eye muscles is initiated before they interact with the neural crest mesenchyme. From studies of chick embryos, it has been shown that the oculomotor‐innervated muscles originate from the first and second somitomeres, the superior oblique muscle from the third somitomere, and the lateral rectus muscle from the fourth somitomere. The entire length of these muscles appears to develop spontaneously rather than from the orbital apex anteriorly.

Section II: Morphology of the Eye and Adnexa

      Introduction

      A thorough understanding of normal ophthalmic anatomy is an integral part of the foundational knowledge for diagnosis and treatment of ophthalmic diseases as the majority of the ocular tissues can be visualized directly. The veterinarian can examine eyes from a wide variety of animal species, and fortunately the eye has largely retained the same basic components, but important and clinically relevant differences do exist. This chapter will primarily present the ophthalmic anatomy of dogs, cats, horses, livestock species, and occasional birds, and relates information important to the clinician. More detailed anatomical information is available in the standard veterinary and comparative anatomy texts.

Orbit

The orbit is the bony fossa that surrounds and protects the eye while separating it from the cranial cavity. Through numerous foramina, the orbit also provides pathways for various blood vessels and nerves involved in the function of the eye and nearby structures. The size, shape, and position of the orbit differ by species and are closely associated with time of visual activity and feeding behavior (Table