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Development and Morphology of the Eye and Adnexa

Revised from 6th edition of Veterinary Ophthalmology, Chapter 1: Ocular Embryology and Congenital Malformations, by Cynthia S. Cook; and Chapter 2: Ophthalmic Anatomy, by Jessica M. Meekins, Amy J. Rankin, and Don A. Samuelson

Section I: Development of the Eye and Adnexa

Ocular development has been investigated in some detail in rodents, the dog, and the cow, and demonstrates that the sequence of developmental events is very similar across species. When comparing these studies, one should consider differences in duration of gestation, differences in anatomical end point (e.g., presence of a tapetum, macula, or Schlemm's canal), and when eyelid fusion breaks (during the sixth month of gestation in the human versus two weeks postnatal in the dog and cow) (Tables 1.1 and 1.2).

Gastrulation and Neurulation

Cellular mitosis following fertilization results in transformation of the single-cell zygote into a cluster of 12-16 cells. With continued cellular proliferation, this morula becomes a blastocyst, containing a fluid-filled cavity. The cells of the blastocyst will form both the embryo proper and the extraembryonic tissues (i.e., amnion and chorion). At this early stage, the embryo is a bilaminar disc, consisting of hypoblast and epiblast. This embryonic tissue divides the blastocyst space into the amniotic cavity (adjacent to epiblast) and the yolk sac (adjacent to hypoblast).

Gastrulation (formation of the mesodermal germ layer) begins during day 10 of gestation in the dog (day 7 in the mouse; days 15-20 in the human). The primitive streak forms as a longitudinal groove within the epiblast (i.e., future ectoderm). Epiblast cells migrate toward the primitive streak, where they invaginate to form the mesoderm. This forms the three classic germ layers: ectoderm, mesoderm, and endoderm. Gastrulation proceeds in a cranial-to-caudal progression; simultaneously, the cranial surface ectoderm proliferates, forming bilateral elevations called the neural folds (i.e., future brain). The columnar surface ectoderm in this area now becomes known as the neural ectoderm.

As the neural folds elevate and approach each other, a specialized population of mesenchymal cells, the neural crest, emigrates from the neural ectoderm at its junction with the surface ectoderm. Migration and differentiation of the neural crest cells are influenced by the hyaluronic acid-rich extracellular matrix. This acellular matrix is secreted by the surface epithelium as well as by the crest cells, and it forms a space through which the crest cells migrate. The neural crest cells migrate peripherally beneath the surface ectoderm to spread throughout the embryo, populating the region around the optic vesicle and ultimately giving rise to nearly all the connective tissue structures of the eye (Table 1.3).

Table 1.1 Sequence of ocular development in human, mouse, and dog.

Human (approximate post-fertilization age) Mouse (day post-fertilization) Dog (day post-fertilization or P = postnatal day) Developmental events Month Week Day 1 3 22 8 13 Optic sulci present in forebrain 4 24 9 15 Optic sulci convert into optic vesicles 10 17 Optic vesicle contacts surface epithelium
Lens placode begins to thicken 26 Optic vesicle surrounded by neural crest mesenchyme 2 5 28 10.5 Optic vesicle begins to invaginate, forming optic cup
Lens pit forms as lens placode invaginates
Retinal primordium thickens, marginal zone present 32 11 19 Optic vesicle invaginated to form optic cup
Optic fissure delineated
Retinal primordium consists of external limiting membrane, proliferative zone, primitive zone, marginal zone, and internal limiting membrane
Oculomotor nerve present 33 11.5 25 Pigment in outer layer of optic cup
Hyaloid artery enters through the optic cup
Lens vesicle separated from surface ectoderm
Retina: inner marginal and outer nuclear zones 11.5 29 Basement membrane of surface ectoderm intact
Primary lens fibers form
Trochlear and abducens nerves appear
Lid fold present 6 37 12 Edges of optic fissure in contact 12 30 TVL present
Lens vesicle cavity obliterated
Ciliary ganglion present 41 12 32 Posterior retina consists of nerve fiber layer, inner neuroblastic layer, transient fiber layer of Chievitz, proliferative zone, outer neuroblastic layer, and external limiting membrane 17 32 Eyelids fuse (dog) 7 Anterior chamber beginning to form 12.5 40 Secondary lens fibers present 48 14 32 Corneal endothelium differentiated 8 51 Optic nerve fibers reach the brain
Optic stalk cavity is obliterated
Lens sutures appear
Acellular corneal stroma present 54 30-35 Scleral condensation present 9 57 17 40 First indication of ciliary processes and iris - EOMs visible
Eyelids fuse (occurs earlier in the dog) 10 45 Pigment visible in iris stroma
Ciliary processes touch lens equator
Rudimentary rods and cones appear 45-1P Hyaloid artery begins to atrophy to the disc 3 12 - Branches of the central retinal artery form 4 51 Pupillary sphincter differentiates
Retinal vessels present - 56 Ciliary muscle appears - Tapetum present (dog) 5 40 Layers of the choroid are complete with pigmentation 6 - Eyelids begin to open, light perception 1P Pupillary dilator muscle present 7 1-14P Pupillary membrane atrophies 1-16P Rod and cone inner and outer segments present in posterior retina 10-13P Pars plana distinct 9 16-40P Retinal layers developed 14P Regression of pupillary membrane, TVL, and hyaloid artery nearly complete
Lacrimal duct canalized

Table 1.2 Sequence of ocular development in the cow.

Ocular part or event Gestational size (mm) Lens Optic vesicle 6 Lens placode 6 Optic cup and lens placode 10 Separation of lens vesicle from surface ectoderm 10 Primary lens fibers 15 Lens vesicle cavity disappears 24 Completion of lens capsule 50 Secondary lens fibers 58 Perilenticular vascular mesoderm Extension of primary vitreous (hyaloid artery) to...