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Embryology, Anatomy, and Physiology of the Afferent Visual Pathway

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Embryology, Anatomy, and Physiology of the Afferent Visual Pathway CHAPTER 1 Embryology, Anatomy, and Physiology of the Afferent Visual Pathway Joseph F. Rizzo III RETINA Physiology Embryology of the Eye and Retina Blood Supply Basic Anatomy and Physiology POSTGENICULATE VISUAL SENSORY PATHWAYS Overview of Retinal Outflow: Parallel Pathways Embryology OPTIC NERVE Anatomy of the Optic Radiations Embryology Blood Supply General Anatomy CORTICAL VISUAL AREAS Optic Nerve Blood Supply Cortical Area V1 Optic Nerve Sheaths Cortical Area V2 Optic Nerve Axons Cortical Areas V3 and V3A OPTIC CHIASM Dorsal and Ventral Visual Streams Embryology Cortical Area V5 Gross Anatomy of the Chiasm and Perichiasmal Region Cortical Area V4 Organization of Nerve Fibers within the Optic Chiasm Area TE Blood Supply Cortical Area V6 OPTIC TRACT OTHER CEREBRAL AREASCONTRIBUTING TO VISUAL LATERAL GENICULATE NUCLEUSPERCEPTION Anatomic and Functional Organization The brain devotes more cells and connections to vision lular, magnocellular, and koniocellular pathways—each of than any other sense or motor function. This chapter presents which contributes to visual processing at the primary visual an overview of the development, anatomy, and physiology cortex. Beyond the primary visual cortex, two streams of of this extremely complex but fascinating system. Of neces- information flow develop: the dorsal stream, primarily for sity, the subject matter is greatly abridged, although special detection of where objects are and for motion perception, attention is given to principles that relate to clinical neuro- and the ventral stream, primarily for detection of what ophthalmology. objects are (including their color, depth, and form). At Light initiates a cascade of cellular responses in the retina every level of the visual system, however, information that begins as a slow, graded response of the photoreceptors among these ‘‘parallel’’ pathways is shared by intercellular, and transforms into a volley of coordinated action potentials thalamic-cortical, and intercortical connections. The mech- at the level of the retinal ganglion cells (RGCs), the axons anisms by which the visual system uses these data streams of which form the optic nerve. The outflow of visual signals to create vision remain mysterious and are beyond the from photoreceptors is parsed into parallel pathways that are current grasp of technology, although recent multichannel distributed to the diencephalon, midbrain, lateral geniculate recordings within associative visual cortices are providing body, primary visual cortex, and beyond. These pathways insights into how complex visual scenes are assembled are broadly divided into three major streams—the parvocel- by the brain. 3 4 CLINICAL NEURO-OPHTHALMOLOGY RETINA EMBRYOLOGY OF THE EYE AND RETINA Mu¨ller cells differentiate. Cones, which appear before rods, develop around the same time as the horizontal cells, but The sensory retina is a part of the central nervous system both cones and rods do not mature until after connections (CNS). The retina develops from the optic cup, a structure within the inner retina begin to form. Maturation of the pho- formed by the invagination of the lateral walls of the optic toreceptors leads to formation of the outer plexiform layer vesicles, which emerge as outpouchings of the prosencepha- lon during the third week of gestation (1–3) (Fig. 1.1). The (OPL), which establishes connections among photoreceptors invagination is dependent upon a temporally specific associ- and horizontal and bipolar cells (Fig. 1.2). Each Mu¨ller cell ation of the developing optic vesicle with the overlying pre- may be the kernel of a functionally intertwined ‘‘columnar lens ectoderm (4). The outer wall of the optic cup becomes unit’’—each Mu¨ller cell (in the rabbit) ensheathes a collec- the retinal pigment epithelium (RPE), while the inner wall tion of rods, bipolar cells, and amacrine cells, with each mostly develops into the sensory retina (3). cell class having a precisely maintained ratio to Mu¨ller cells Several highly conserved genes contribute to the forma- across the retina (9). tion of the eye and retina (5). The optic cup and optic stalk Generation of cells from the neuroepithelial (or neuro- express Pax-2 and Pax-6, which belong to a family of tran- blastic) layers is followed by their differentiation, and most scription factors involved in the regulation of early develop- differentiated cells then migrate through the developing ret- ment. Pax-2 expression occurs in cells that will form the ina. RGCs migrate inward, leaving in their wake an acellular optic fissure (which develops at the future site of the optic region that is developing into an expanded inner plexiform nerve head) and the optic stalk (which becomes the optic layer (IPL) (Fig. 1.3). Simultaneously, horizontal cells mi- nerve) (6). Pax-6 expression occurs in cells that will become grate inward and combine with cells of the inner neuroblastic the neural retina (and most of the eye except the cornea and layer to form the INL. Photoreceptors remain stationary. De- lens) (7). termination of cell number for each cell class is controlled The general principles of retinal development are as fol- by expression of the homeodomain protein Prox 1, which lows (2,8). Ganglion cells develop first, at the seventh week regulates the timing at which dividing cells become quies- of gestation. Amacrine and horizontal cells develop next. cent (10). Fibroblastic growth factors and hedgehog (Hh) Connections among amacrine cells and RGCs create a nas- proteins also are important for retinal development and RGC cent inner nuclear layer (INL), at which time bipolar and axon guidance (11). N-cadherin plays a crucial role in the Figure 1.1. The formation of the optic vesicle and cup in a 7.5-mm (5-week) human embryo. Note that the stalk has two separate regions, a distal invaginated, crescent-shaped segment and a proximal noninvaginated circular segment. The lens vesicle is formed by an invagination of the pre-lens ectoderm, which in turn prompts the invagination of the optic cup. (Redrawn from Hamilton WJ, Boyd JD, Mossman HW. Human Embryology. Bal- timore, Williams & Wilkins, 1962.) EMBRYOLOGY, ANATOMY, AND PHYSIOLOGY OF THE AFFERENT VISUAL PATHWAY 5 Figure 1.2. Basic structure and temporal order of cell differentiation of the vertebrate retina. A, The neural retina begins as a sheet of neuroepithelial cells (NBL, neuroblastic layer) with processes that contact the internal (ILM) and external (ELM) limiting membranes. B, Ganglion cells (G) are the first cell type to differentiate and migrate toward the ILM to form the ganglion cell layer (GCL). C, Amacrine cells (A) and horizontal cells (H) differentiate next. Cone photoreceptors are born at this stage but do not differentiate until later. The first network of connections, between amacrine cells and ganglion cells, is established as a continuous inner plexiform layer (IPL) across the retina. D, In the inner nuclear layer (INL), bipolar cells (B) and Mu¨ller cells (M) are generated and differentiate. At this stage, both cone (C) and rod (R) photoreceptors composing the outer nuclear layer (ONL) begin to mature, bearing few outer segments or discs. The outer plexiform layer (OPL) emerges, and connections between photoreceptors, horizontal cells, and bipolar cells are formed. Cell genesis (mainly rods) continues at this stage but to a greatly reduced degree. E, At maturity, all cell types are present, connections in both plexiform layers are established, and photoreceptor outer segments are well developed. (From Chalupa LM, Werner JS, eds. The Visual Neurosci- ences. Cambridge, MA, MIT Press, 2004Ϻ78.) development of lamination within the retina (12). RGCs may tivity, influences a competitive selection process that deter- regulate the ultimate number of amacrine cells by secreting mines the final number of RGCs and their pattern of synaptic brain-derived neurotrophic factor (13). arrangement at their termination sites (20). Apoptosis elim- RGC axonal guidance is partially directed by EphA recep- inates noncompetitive RGCs (21). tor tyrosine kinases (14). EphA receptors are expressed on all RGC axons, but only temporal axons have receptors with BASIC ANATOMY AND PHYSIOLOGY high ligand sensitivity. The differential (i.e., temporal versus Retinal Pigment Epithelium nasal) sensitivity is determined by varying degrees of phos- phorylation of the EphA receptor, which (in the chick) is The RPE is a monolayer of cells whose development in controlled by relatively greater expression of ephrin-A6 in lower vertebrates involves expression of Hh proteins (Fig. the nasal retina (15). The relatively low state of phosphoryla- 1.3). Peripherally, in the homologous zone of the pigmented tion of EphA receptors on temporal axons increases their ciliary epithelium in mammals, expression of Hh proteins is sensitivity, which allows them to respond to low concentra- associated with the presence of retinal stem cells that retain tions of ephrin-A ligands at the tectal termination zone. a capacity to differentiate into any type of retinal neuron, Proper topography at the tectum is also at least partially which has therapeutic implications (22). controlled by variable expression of ephrin-A at that location The RPE has several functions. It (a) regenerates chromo- (16). Neuronal activity (via N-methyl-D-aspartate [NMDA] phore; (b) provides trophic support for photoreceptors; (c) receptors) and expression of nitric oxide also contribute to is a transport barrier between the choriocapillaris and the topographic precision (17–19).
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