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  • 2020–2021 BCSC Basic and Clinical Science Course™

    Go to Academy Store Learn more and Purchase.

    2 Fundamentals and Principles of Ophthalmology

    Part II: Embryology

    Chapter 4: Ocular Development

    General Principles

    Embryogenesis can be thought of as a series of steps that build on one another; each step creates a ripple effect on all subsequent steps. The steps are regulated by genetic programs that are activated in specific cell types and in a specific order. These genetic programs consist of cascades of genes that are expressed in response to external cues. Often, the same genes participate in different cascades and play different roles in different contexts.

    For example, gene products that activate transcription in a particular program may repress transcription in the context of another program, depending on the position of the program within the overall developmental cascade. The cascades are regulated by diffusible ligands (growth factors and hormones) that create overlapping zones of concentration gradients that allow cells to triangulate their position within the developing embryo and determine which program to activate. Misactivation of genetic cascades, whether the result of gene mutations, oocyte abnormalities, or exposure to teratogens, causes embryologic abnormalities that, in the most severe cases, are embryonic lethal or, in less severe cases, give rise to congenital abnormalities.

    During gastrulation (development from a single-layered blastula to a multilayered gastrula), 3 germ layers form in all animal embryos: ectoderm (superficial layer of cells), mesoderm (middle layer), and endoderm (inner layer) (Figs 4-1, 4-2). In addition, vertebrate embryos have an ectomesenchymal cell population that arises from neuroectoderm at the dorsal edge of the neural tube. These cells, known as neural crest cells, are transient migratory stem cells that can form tissues with ectodermal and mesodermal characteristics (Fig 4-3). There are several types of neural crest cells, depending on their location and subsequent contributions. Ocular structures are derived from cranial neural crest cells, which are referred to as neural crest cells in this chapter.

    Figure 4-1 Early stages of embryonic development. The cross section demonstrates the neural tube and underlying notochord with adjacent neural crest cells (green) and mesoderm (red). There is overlying surface ectoderm and underlying endoderm. The optic sulci develop within the neuropore at day 22.

    (Illustration by Paul Schiffmacher. Adapted from Forrester JV, Dick AD, McMenamin PG, Roberts F, Pearlman E. The Eye: Basic Sciences in Practice. 4th ed. Edinburgh: Elsevier; 2016, eFig 2-1.)

    The eye and orbital tissues develop from ectoderm, mesoderm, and neural crest cells, with the neural crest cells making a particularly large contribution. In addition, neural crest cells make key contributions to facial, dental, and cranial structures (Fig 4-4). For this reason, syndromes that arise from neural crest maldevelopment (eg, Goldenhar syndrome) often involve the eye as well as facial, dental, and calvarial abnormalities.

    Following gastrulation, the ectoderm separates into surface ectoderm and neuroectoderm. Each makes a key contribution to development of the eye (Fig 4-5, Table 4-1).

    Figure 4-2 Scanning electron micrographs of normal craniofacial development. A: A parasagittal section through the cranial aspect of a gastrulation-stage mouse embryo. The cells of the 3 germ layers—ectoderm (Ec), mesoderm (M), and endoderm (En)—have distinct morphologies. B: The developing neural plate (N) is apparent in a dorsal view of this presomite mouse embryo. C: Neural folds (arrowhead) can be observed in the developing spinal cord region. The lateral aspects of the brain (B) region have not yet begun to elevate in this mouse embryo in the head-fold stage. D: Three regions of the brain can be distinguished at this 6-somite stage: prosencephalon (P), mesencephalon (M), and rhombencephalon (R, curved arrow). Optic sulci (arrowhead) are visible as evaginations from the prosencephalon. E: The neural tube has not yet fused in this 12-somite embryo. The stomodeum, or primitive oral cavity, is bordered by the frontonasal prominence (F), the first visceral arch (mandibular arch, M), and the developing heart (H). F: Medial and lateral nasal prominences (MNP, LNP) surround olfactory pits in this 36-somite mouse embryo. The Rathke pouch (arrowhead) can be distinguished in the roof of the stomodeum. G: In this lateral view of a 36-somite mouse embryo, the first and second (hyoid, H) visceral arches are apparent. The region of the first arch consists of maxillary (Mx) and mandibular (M) components. Note the presence of the eye with its invaginating lens (arrowhead). Atrial (A) and ventricular (V) heart chambers can be distinguished.

    (Reproduced from Sulik KK, Johnston MC. Embryonic origin of holoprosencephaly: interrelationship of the developing brain and face. Scan Electron Microsc. 1982;(Pt 1):311.)

    Figure 4-3 Migration of neural crest cells. A, Origin of neural crest cells from the junction of surface ectoderm and neuroectoderm (light blue) at the dorsal edge of the neural tube. B, Lateral/ventral migration. C, Differentiation of neural crest cells; note the development of melanocytes, dorsal root ganglia (including sensory ganglia of cranial nerve V), and autonomic ganglia.

    (Illustration by Paul Schiffmacher. Adapted from Forrester JV, Dick AD, McMenamin PG, Roberts F, Pearlman E. The Eye: Basic Sciences in Practice. 4th ed. Edinburgh: Elsevier; 2016, eFig 2-2.)

    • Billon N, Iannarelli P, Monteiro MC, et al. The generation of adipocytes by the neural crest. Development. 2007;134(12):2283–2292.

    • Foster CS, Sainz de la Maza M, Tauber J. The Sclera. New York: Springer Science + Business Media LLC; 2012.

    Figure 4-4 Migration of neural crest cells. A, Lateral and ventral migration of neural crest cells that will contribute to the development of the face and eye. In the head, neural crest cells contribute to tissues initially thought to be of mesodermal origin only. This does not occur in the trunk. Note the optic vesicle at the rostral ventral aspect. B, Cross section of the optic vesicle with invagination of the neuroectoderm (which will contribute to the retina, retinal pigment epithelium, optic nerve) and overlying surface ectoderm (contributes to lens). C, The neural crest cells and mesoderm surrounding the neuroectoderm will contribute to the sclera, cornea, and uvea (melanocytes), among numerous other ocular structures.

    (Illustration by Paul Schiffmacher. Adapted from Forrester JV, Dick AD, McMenamin PG, Roberts F, Pearlman E. The Eye: Basic Sciences in Practice. 4th ed. Edinburgh: Elsevier; 2016:113.)

    Figure 4-5 Embryologic origin of the ocular tissues. 1, Vitreous body; 2, ciliary muscle; 3, ciliary body epithelium; 4, zonular fibers; 5, corneal endothelium; 6, corneal stroma; 7, corneal epithelium; 8, iris sphincter; 9, iris dilator; 10, lens; 11, iris stroma; 12, trabecular meshwork; 13, conjunctiva; 14, inferior oblique muscle; 15, inferior rectus muscle; 16, medial rectus tendon; 17, medial rectus muscle; 18, medial rectus muscle sheath; 19, inferior orbital bones; 20, optic nerve sheath; 21, optic nerve; 22, bulbar sheath; 23, sclera; 24, choroid; 25, neurosensory retina and retinal pigment epithelium; 26, superior rectus muscle.

    (Developed by Evan Silverstein, MD, and Vikram S. Brar, MD. Illustration by Cyndie C. H. Wooley; original art by Paul Schiffmacher.)

    Excerpted from BCSC 2020-2021 series: Section 2 - Fundamentals and Principles of Ophthalmology. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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