Development of the Vertebrate Retina

The vertebrate retina has a form that is closely and clearly linked to its func­ tion. Though its fundamental cellular architecture is conserved across verte­ brates, the retinas of individual species show variations that are also of clear and direct functional utility. Its accessibility, readily identifiable neuronal types, and specialized neuronal connectivity and morphology have made it a model system for researchers interested in the general questions of the genet­ ic, molecular, and developmental control of cell type and shape. Thus, the questions asked of the retina span virtually every domain of neuroscientific inquiry-molecular, genetic, developmental, behavioral, and evolutionary. Nowhere have the interactions of these levels of analysis been more apparent and borne more fruit than in the last several years of study of the develop­ ment of the vertebrate retina. Fields of investigation have a natural evolution, rdoving through periods of initial excitement, of framing of questions and controversy, to periods of synthesis and restatement of questions. The study of the development of the vertebrate retina appeared to us to have reached such a point of synthesis. Descriptive questions of how neurons are generated and deployed, and ques­ tions of mechanism about the factors that control the retinal neuron's type and distribution and the conformation of its processes have been posed, and in good part answered. Moreover, the integration of cellular accounts of development with genetic, molecular, and whole-eye and behavioral accounts has begun.

I. Cellular Aspects of Retinal Development.- 1. Neurogenesis and Maturation of Cell Morphology in the Development of the Mammalian Retina.- 1.1. Introduction.- 1.2. Background.- 1.3. Histogenesis and Morphogenesis of the Retina.- 1.3.1. Neurogenesis: An Autoradiographic Analysis.- 1.3.2. Morphogenesis: A Scanning Electron Microscope Analysis.- 1.4. Theoretical Considerations in Retinal Neurogenesis and Morphogenesis.- 1.4.1. Differentiation.- 1.4.2. Lamination.- 1.4.3. Cellular Cohorts.- 1.5. Summary.- 1.6. References.- 2. Retinal Rod Neurogenesis.- 2.1. Introduction.- 2.2. Historical Review.- 2.3. Present Views of Rod Neurogenesis.- 2.4. Embryonic Origin of Rods.- 2.5. References.- 3. The Regulation of Neuronal Production during Retinal Neurogenesis.- 3.1. Introduction.- 3.2. Potential Mechanisms Regulating Cell Number and Type.- 3.2.1. Are Neurons Produced in the Appropriate Ratios as a Result of Strict Lineal Relationships and Highly Deterministic Cell Division Patterns?.- 3.2.2. Are All Neuronal Cell Types Overproduced, with the Appropriate Ratios Established as a Result of a Later Phase of Cell Death?.- 3.2.3. Selective Neurotoxin Lesions in Developing Retina Demonstrate That Neuronal Production Can Be Regulated by the Microenvironment.- 3.3. What Molecular Factors Regulate the Proliferation or Differentiation of Germinal Neuroepithelial Cells in the Developing CNS?.- 3.3.1. Peptide Mitogens.- 3.3.2. Differentiating Factors or Mitotic Inhibitors.- 3.3.3. Other Factors.- 3.4. Germinal Neuroepithelial Cells in the Proliferative Zone of the Retina Continue to Undergo Mitosis in Vitro for up to 3 Weeks.- 3.5. What Factors Can Modify Germinal Neuroepithelial Cell Proliferation in Vitro?.- 3.5.1. Peptide Mitogens and Growth Factors.- 3.5.2. Monoamine Neurotransmitters and Germinal Cell Proliferation.- 3.5.3. External Basement Membrane Is Also Necessary for the Proliferation of Germinal Neuroepithelial Cells.- 3.6. Summary and Conclusions.- 3.7. References.- 4. Development of the Visual System in Hypopigmented Mutants.- 4.1. Introduction.- 4.2. The Role of Retinal Pigment Epithelium in Producing Abnormalities in the Visual System of Hypopigmented Animals.- 4.2.1. Developmental Abnormalities in the Retina of the Albino Rat and Siamese Cat.- 4.3. The Optic Stalk’s Role in Producing Abnormalities in the Visual System of Hypopigmented Animals.- 4.3.1. Embryogenesis of the Optic Stalk.- 4.3.2. Pigment in the Optic Stalk.- 4.3.3. Morphogenesis of the Normally Pigmented Cat Optic Stalk.- 4.3.4. Morphogenesis of the Siamese Optic Stalk.- 4.4. Conclusion.- 4.5. References.- 5. Topographic Organization of the Visual Pathways.- 5.1. Introduction.- 5.1.1. Retinal Growth.- 5.1.2. Retinotectal Topography.- 5.2. Development of the Goldfish Retina.- 5.2.1. Retinal Ganglion Cell Histogenesis.- 5.2.2. Optic Fiber Layer Organization.- 5.2.3. Optic Nerve Head Organization.- 5.2.4. Optic Nerve Organization.- 5.2.5. Organization in the Optic Foramen.- 5.2.6. Organization after Crossing the Midline.- 5.2.7. Organization in the Optic Chiasm.- 5.2.8. Formation and Organization of the Optic Tracts.- 5.2.9. Multiple Maps in the Optic Tracts.- 5.3. Observations in Other Species.- 5.3.1. Lamination of the Optic Fiber Layer.- 5.3.2. Organization of the Optic Nerve and Tract.- 5.4. Boundaries between Dorsal and Ventral Retina.- 5.5. Conclusions.- 5.6. References.- 6. Routing of Axons at the Optic Chiasm: Ipsilateral Projections and Their Development.- 6.1. Introduction.- 6.2. Organization of the Retina with Respect to Projection Laterality.- 6.2.1. The Primate Pattern.- 6.2.2. The Nonprimate Mammalian Pattern.- 6.2.3. The Lower Vertebrate Pattern.- 6.3. Ontogeny of Ipsilaterally Projecting Cells.- 6.3.1. Perturbations of Developing Ipsilateral Projections.- 6.3.2. Hormonal Control of Ipsilateral Projections.- 6.4. Concluding Remarks.- 6.5. References.- 7. Dendritic Interactions between Cell Populations in the Developing Retina.- 7.1. Introduction.- 7.1.1. Regulation of Cellular Distribution.- 7.1.2. Regulation of Cellular Morphology.- 7.2. Dendritic Competition: The Phenomenon.- 7.3. Differential Effects of Afferents and Targets on Cell Survival.- 7.4. The Afferents in the Inner Nuclear Layer.- 7.5. Findings Consistent with the Dendritic Competition Hypothesis.- 7.6. Dendritic Competition: Competition for What?.- 7.6.1. Does Synapse Availability Regulate Competition?..- 7.6.2. Does Dendritic Contact Regulate Competition?.- 7.6.3. Do Chemotrophic Factors Regulate Competition?..- 7.7. Interactions between Cell Types.- 7.8. Summary.- 7.9. References.- 8. Extrinsic Determinants of Retinal Ganglion Cell Development in Cats and Monkeys.- 8.1. Introduction.- 8.2. Experimental Observations.- 8.2.1. Retinal Ganglion Cell Development in the Cat.- 8.2.2. Retinal Ganglion Cell Development in Primates.- 8.3. Summary of Experimental Observations.- 8.4. Implications of Experimental Findings.- 8.4.1. Normal Changes in Morphology Associated with Retinal Eccentricity.- 8.4.2. Implications for Retinal Ganglion Cell Classification.- 8.4.3. Retinal Ganglion Cell Class Differences.- 8.4.4. Independence of Dendritic Field Size and Displacement.- 8.4.5. Retinal Ganglion Cell Development and Competition for Afferents.- 8.4.6. Direct Interactions among Neighboring Cells and Ganglion Cell Development.- 8.4.7. Relation to Other Neuronal Systems.- 8.4.8. Foveal Development.- 8.5. References.- II. Phylogenetic, Evolutionary, and Functional Aspects of Retinal Development.- 9. Development of Cell Density Gradients in the Retinal Ganglion Cell Layer of Amphibians and Marsupials: Two Solutions to One Problem.- 9.1. Overview.- 9.2. Introduction.- 9.3. Identification of Ganglion Cells.- 9.3.1. Amphibians.- 9.3.2. Marsupials.- 9.4. Mature Ganglion Cell Topography.- 9.4.1. Amphibians.- 9.4.2. Marsupials.- 9.5. Development of Ganglion Cell Topography.- 9.5.1. Amphibians.- 9.5.2. Marsupials.- 9.6. Events Underlying Changes in Ganglion Cell Topography.- 9.6.1. Cell Addition to the Ganglion Cell Layer.- 9.6.2. Cell Transformation.- 9.6.3. Cell Death.- 9.6.4. Differential Growth of the Retina.- 9.7. Factors Leading to Differential Retinal Growth in Marsupials.- 9.7.1. Cell Addition to the Inner and Outer Nuclear Layers.- 9.7.2. Changes in the Size, Shape, or Packing of Cells.- 9.8. References.- 10. Developmental Heterochrony and the Evolution of Species Differences in Retinal Specializations.- 10.1. Introduction.- 10.2. Differences between Species in Retinal Organization.- 10.2.1. The Nature of Variation between Vertebrates in Retinal Topography.- 10.2.2. Functional Explanations for Variations in Retinal Topography.- 10.2.3. Ecological Explanations for Variations in Retinal Topography.- 10.2.4. Mechanisms of Development as an Explanation for Variation in Retinal Topography.- 10.3. Toward a Full Explanation of the Development and Evolution of Retinal Specializations.- 10.4. Heterochrony and the Evolution of Retinal Specializations.- 10.4.1. Alterations in Developmental Timing.- 10.4.2. Heterochrony: The Role of Timing in Development and Evolution.- 10.5. Accommodation of Retinal Neurogenesis into Developmental Schedules of Variable Duration.- 10.6. Heterochronic Changes in Ocular Development and Variation in Retinal Cell Number and Topography.- 10.6.1. Comparison of the Hamster and Gerbil: Variation in Duration of Development.- 10.6.2. Comparison of the Rat and the Mouse: Size Scaling.- 10.6.3. Comparison of the Ferret and the Cat: The Effects of Rate of Eye Growth.- 10.6.4. Summary of Cross-Species Comparisons.- 10.7. Summary and Conclusions.- 10.8. References.- 11. Fish Vision.- 11.1. Introduction.- 11.2. Physical Constraints on Eye Design.- 11.3. Why Study Fish Vision?.- 11.4. Teleost Retinal Structure.- 11.5. Growth of the Fish Eye.- 11.5.1. Regulation of Eye Growth.- 11.5.2. Retinal Change during Eye Growth.- 11.5.3. Image Quality during Eye Growth.- 11.5.4. Visual Acuity during Eye Growth.- 11.5.5. Visual Sensitivity during Eye Growth.- 11.6. Understanding Development of the Eye.- 11.7. Summary.- 11.8. References.- 12. Development of Accommodation and Refractive State in the Eyes of Humans and Chickens.- 12.1. Introduction.- 12.2. Differences and Similarities in Human and Chick Eyes.- 12.2.1. Differences.- 12.2.2. Similarities.- 12.3. Methods for Studying the Optics of Eyes.- 12.3.1. Retinoscopy.- 12.3.2. Photographic Refractive Methods.- 12.3.3. Photokeratoscopy.- 12.4. Human Refractive Development.- 12.4.1. Newborn Infants.- 12.4.2. Infants between 1 and 3 Months of Age.- 12.4.3. Infants between 3 and 6 Months of Age.- 12.4.4. Infants and Children between 6 Months and 4 Years of Age.- 12.4.5. The Nature of Infant Astigmatism.- 12.4.6. Summary of Human Refractive Development.- 12.5. Chick Refractive Development.- 12.5.1. Mode of Accommodation.- 12.5.2. Growth of the Eye with Ophthalmic Lenses.- 12.6. How to Use Chicks to Study Human Vision.- 12.6.1. The Relationship of Emmetropization and Myopia.- 12.6.2. Schemes for Emmetropization.- 12.6.3. Relationship of Emmetropization Schemes to Myopia.- 12.6.4. Amblyopia.- 12.7. References.