Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T11:11:45.874Z Has data issue: false hasContentIssue false
  • English
  • Français

Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography

Published online by Cambridge University Press:  02 June 2009

Stephen R. Robinson ,
Bogdan Dreher  and
Murray J. McCall
Stephen R. Robinson
Affiliation:
Department of Anatomy, The University of Sydney, Australia
Bogdan Dreher
Affiliation:
Department of Anatomy, The University of Sydney, Australia
Murray J. McCall
Affiliation:
Department of Anatomy, The University of Sydney, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

We have studied the distribution of retinal ganglion cells (RGCs) which have been retrogradely labeled from massive bilateral injections of the enzyme horseradish peroxidase into the retino-recipient nuclei of foetal and postnatal albino rabbits aged from the 24th postconceptional day (24PCD) to adulthood. The number of labeled RGCs increases from about 447,000 on the 24PCD to a peak of about 525,000 on the 27PCD. From the 29PCD to birth (31/32PCD), the number of RGCs rapidly declines to about 375,000. During the next 20 d, the number of RGCs stabilizes at about 335,000. After the 51PCD, the number of RGCs gradually declines to the adult value of about 280,000. Retinal area steadily increases from about 40 mm2 on the 24PCD to about 500 mm2 in the adult, while RGC density decreases. However, the reduction in RGC density is nonuniform: RGC density in the visual streak drops from 18,600 RGCs mm2 on the 24PCD to 4700 RGCs/mm2 in the adult, whereas RGC densities at the superior and inferior edges of the retina decrease proportionally much more (from 9300 to 105 RGCs/mm2 and from 12,000 to 170 RGCs/mm2, respectively). As a result of this differential reduction in RGC density, the streak:superior edge RGC density ratio changes from 2.0:1 on the 24PCD to about 45:1 in the adult, while the streak/inferior edge ratio changes from 1.6:1 to about 28:1. In the periods from the 24PCD to the 29PCD and from the 32PCD to adulthood, the proportional increases in the streak/superior edge and streak/inferior edge RGC density ratios are linearly related to the proportional increases in retinal area. However, between the 29PCD and 32PCD, the RGC density ratios increase at a greater rate than retinal area. We conclude that (1) the centro-peripheral difference in RGC density that is already present on the 24PCD might be attributable to differential RGC generation; (2) the redistribution of RGCs between the 24PCD and adulthood is mainly due to nonuniform expansion of the retina, with minimal expansion of the visual streak and maximal expansion at the superior and inferior retinal edges; and (3) a small component of the increase in the centro-peripheral RGC density ratio, which becomes apparent between the 29PCD and 32PCD, is probably due to differential RGC loss. We discuss the pattern of retinal expansion in the rabbit and the factors which might contribute to it.

Keywords

Retinal ganglion cellsDifferential retinal growthDifferential cell deathDifferential cell generationTrasformationMigrationStretching
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 3 , March 1989 , pp. 201 - 219
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of on–off direction selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
Ali, M.A. (1964). Stretching of retina during growth of salmon (Salmo salar). Growth 28, 83–89.Google ScholarPubMed
Beazley, L.D. & Dunlop, S.A. (1983). The evolution of an area centralis and visual streak in the marsupial Setonix brachyurus. Journal of Comparative Neurology 216, 211–231.CrossRefGoogle ScholarPubMed
Bernard, H.M. (1900). Studies in the retina: rods and cones in the frog and some amphibia. Quarterly Journal of Microscopical Science 43, 23–47.Google Scholar
Braekevelt, C.R., Beazley, L.D., Dunlop, S.A. & Darby, J.E. (1986). Numbers of axons in the optic nerve and of retinal ganglion cells during development in the marsupial Setonix brachyurus. Developmental Brain Research 25, 117–125.CrossRefGoogle Scholar
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281–302.CrossRefGoogle ScholarPubMed
Buhl, E.H. & Peichl, L. (1986). Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. Journal of Comparative Neurology 253, 163–174.CrossRefGoogle Scholar
Campbell, G., Ramoa, A.S. & Shatz, C.J. (1987). Do amacrine cells extend then retract a centrally projecting axon? Society for Neuro-science Abstracts 13, 589.Google Scholar
Choudhury, B.P. (1981). Ganglion cell distribution in the albino rabbit's retina. Experimental Neurology 72, 638–644.CrossRefGoogle ScholarPubMed
Coulombre, A.J. (1955). Correlations of structural and biochemical changes in the developing retina of the chick. American Journal of Anatomy 96, 153–190.CrossRefGoogle ScholarPubMed
Coulombre, A.J. (1956). The role of intraocular pressure in the development of the chick eye, I: Control of eye size. The Journal of Experimental Zoology 133, 211–225.CrossRefGoogle Scholar
Coulombre, A.J., Steinberg, S.N. & Coulombre, J.L. (1963). The role of intraocular pressure in the development of the chick eye, V: Pigmented epithelium. Investigative Ophthalmology 2, 83–89.Google ScholarPubMed
Crespo, D., O'leary, D.D.M. & Cowan, W.M. (1985). Changes in the numbers of optic nerve fibers during late prenatal and postnatal development in the albino rat. Developmental Brain Research 19, 129–134.CrossRefGoogle Scholar
Cunningham, T., Mohler, M. & Giordano, D. (1982). Naturally occurring neuron death in the ganglion cell layer of the neonatal rat: morphology and evidence for regional correspondence with neuron death in superior colliculus. Developmental Brain Research 2, 203–215.CrossRefGoogle Scholar
Dreher, B., Potts, R.A. & Bennett, M.R. (1983). Evidence that the early postnatal reduction in the number of rat retinal ganglion cells is due to a wave of ganglion cell death. Neuroscience Letters 36, 255–260.CrossRefGoogle ScholarPubMed
Dreher, B., Potts, R.A., ni, S.Y.K. & Bennett, M.R. (1984). The development of heterogeneities in distribution and soma sizes of rat retinal ganglion cells. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., Pp. 39–57. New York: Alan R. Liss.Google Scholar
Dreher, B. & Robinson, S.R. (1988). Development of the retinofugal pathway in birds and mammals: evidence for a common “timetable. ” Brain, Behavior, and Evolution 31, 369–390.CrossRefGoogle ScholarPubMed
Dreher, B., Sefton, A.J., ni, S.Y.K. & Nisbett, G. (1985). The morphology, number, distribution, and central projections of Class I retinal ganglion cells in albino and hooded rats. Brain, Behavior, and Evolution 26, 10–48.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1984). Development of the area cen-tralis and visual streak in mammals. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 75–88. New York: Alan R. Liss.Google Scholar
Dunlop, S.A. & Beazley, L.D. (1985). Changing distribution of retinal ganglion cells during area centralis and visual streak formation in the marsupial Setonix brachyurus. Developmental Brain Research 23, 81–90.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1987 a). Cell death in the developing retinal ganglion cell layer of the wallaby Setonix brachyurus. Journal of Comparative Neurology 264, 14–23.CrossRefGoogle ScholarPubMed
Dunlop, S.A. & Beazley, L.D. (1987 b). Axonal morphology in the developing mammalian optic nerve–towards the explanation of transiently high axon numbers. Neuroscience Letters (Suppl.) 27, S71.Google Scholar
Dunlop, S.A., Longley, W.A. & Beazley, L.D. (1987). Development of the area centralis and visual streak in the grey kangaroo Macro-pus fuliginosus. Vision Research 27, 151–164.CrossRefGoogle ScholarPubMed
Fukuda, Y. (1977). A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Research 119, 327–344.CrossRefGoogle ScholarPubMed
Girgis, M. & Shih-Chang, W. (1981). A New Stereotaxic Atlas of the Rabbit Brain. St. Louis, MO: Green.Google Scholar
Glücksmann, A. (1940). Development and differentiation of the tadpole eye. British Journal of Ophthalmology 24, 153–178.CrossRefGoogle ScholarPubMed
Halasz, P. & Martin, P.R. (1984). A microcomputer-based system for semiautomatic analysis for histological sections. Proceedings of the Royal Microscopical Society 19, 312P.Google Scholar
Hanker, J.S., Yates, P.E., Metz, C.B. & Rustioni, A. (1977). A new specific sensitive and noncarcinogenic reagent for the demonstration of horseradish peroxidase. Journal of Histochemistry 9, 789–792.CrossRefGoogle ScholarPubMed
Harman, A.M. & Beazley, L.D. (1987). Patterns of cytogenesis in the developing retina of the wallaby Setonix brachyurus. Anatomy and Embryology 177, 123–130.CrossRefGoogle ScholarPubMed
Henderson, Z.Finlay, B.L. & Wikler, K.C. (1988). Development of ganglion cell topography in ferret retina. Journal of Neuroscience 8, 1194–1205.CrossRefGoogle ScholarPubMed
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology and Visual Science 15, 746–756.Google ScholarPubMed
Hinds, J.W. & Hinds, P.L. (1978). Early development of amacrine cells in the mouse retina: an electron microscopic serial section analysis. Journal of Comparative Neurology 179, 277–300.CrossRefGoogle ScholarPubMed
Hinds, J.W. & Hinds, P.L. (1983). Development of retinal amacrine cells in the mouse embryo: evidence for two modes of formation. Journal of Comparative Neurology 213, 1–23.CrossRefGoogle ScholarPubMed
Hollyfield, J.G. (1971). Differential growth of the neural retina in Xenopus laevis larvae. Developmental Biology 24, 264–286.CrossRefGoogle ScholarPubMed
Horsburgh, G.M. (1987). Cellular degeneration in the developing mammalian visual system. Ph.D. Thesis, The University of Sydney.Google Scholar
Horsburgh, G.M. & Sefton, A.J. (1987). Cellular degeneration and synaptogenesis in the developing retina of the rat. Journal of Comparative Neurology 263, 553–566.CrossRefGoogle ScholarPubMed
Hughes, A. (1971). Topographical relationships between the anatomy and physiology of the rabbit visual system. Documenta Ophthal-mologica 30, 33–159.CrossRefGoogle ScholarPubMed
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: comparative optics and retinal organisation. In Handbook of Sensory Physiology: The Visual System in Vertebrates, Vol. VII/5, ed. Crescitelli, F., pp. 613–756. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Hughes, A. (1981). Population magnitudes and distribution of major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurons. Journal of Comparative Neurology 197, 303–339.CrossRefGoogle Scholar
Hughes, A. (1985). New perspectives in retinal organisation. In Progress in Retinal Research, Vol. 4, ed. Osborne, M. & Chader, G., pp. 243–313. Oxford, England: Pergamon Press.Google Scholar
Hughes, A. & Vaney, D.I. (1980). Coronate cells: displaced amacrines of the rabbit retina? Journal of Comparative Neurology 189, 169–189.CrossRefGoogle ScholarPubMed
Hughes, A. & Wieniawa-Narklewicz, E. (1980). A newly identified population of presumptive microneurons in the cat retinal ganglion cell layer. Nature 284, 468–470.CrossRefGoogle Scholar
Insausti, R.C., Blakemore, C. & Cowan, W.M. (1984). Ganglion cell death during development of the ipsilateral retino-collicular projection in golden hamster. Nature 308, 362–365.CrossRefGoogle ScholarPubMed
Johns, P.R. (1977). Growth of the adult goldfish eye, III: Source of the new retinal cells. Journal of Comparative Neurology 176, 343–358.CrossRefGoogle ScholarPubMed
Johns, P.R. & Easter, S.S. (1977). Growth of the adult goldfish eye, II: Increase in retinal cell number. Journal of Comparative Neurology 176, 331–342.CrossRefGoogle ScholarPubMed
Kerr, J.F.R., Wyllie, A.H. & Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer 26, 239–257.CrossRefGoogle ScholarPubMed
Kliot, M. & Shatz, C.J. (1982). Genesis of different retinal ganglion cell types in the cat. Society for Neuroscience Abstracts 8, 815.Google Scholar
Leventhal, A.G. (1982). Morphology and distribution of retinal ganglion cells projecting to different layers of the dorsal lateral geniculate nucleus in normal and Siamese cats. Journal of Neuroscience 2, 1024–1042.CrossRefGoogle ScholarPubMed
Lia, B., Williams, R.W. & Chalupa, L.M. (1987). Formation of retinal ganglion cell topography during prenatal development. Science 236, 848–851.CrossRefGoogle ScholarPubMed
Lyall, A.H. (1957 a). The growth of the trout retina. Quarterly Journal of Microscopical Science 98, 101–110.Google Scholar
Lyall, A.H. (1957 b). Cone arrangements in teleost retinae. Quarterly Journal of Microscopical Science 98, 189–201.Google Scholar
Mann, I. (1937). Developmental Abnormalities of the Eye. Cambridge: Cambridge University Press.Google Scholar
Mann, I. (1964). The Development of the Human Eye, 3rd Edition. London: British Medical Association.Google Scholar
Martin, P.R., Sefton, A.J. & Dreher, B. (1983). The retinal location and fate of ganglion cells which project to the ipsilateral superior colliculus in neonatal albino and hooded rats. Neuroscience Letters 41, 219–226.CrossRefGoogle Scholar
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1980). How ganglion cells redistribute during postnatal growth of the cat retina. Investigative Ophthalmology and Visual Science (Suppl.) 19, 70.Google Scholar
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Non-uniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598–608.CrossRefGoogle ScholarPubMed
McCall, M.J., Robinson, S.R. & Dreher, B. (1987). Differential retinal growth appears to be the primary factor producing the ganglion cell density gradient in the rat. Neuroscience Letters 79, 78–84.CrossRefGoogle ScholarPubMed
Müller, H. (1952). Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus). Zoologische Jahrbücher (Physiologie) 63, 275–324.Google Scholar
Murakami, D., Sesma, M.A. & Rowe, M.H. (1982). Characteristics of nasal and temporal retina in Siamese and normally pigmented cats: ganglion cell composition, axon trajectory, and laterality of projection. Brain, Behavior, and Evolution 21, 67–113.CrossRefGoogle ScholarPubMed
Oyster, C.W., Takahashi, E.S. & Hurst, D.C. (1981). Density, soma size, and regional distribution of rabbit retinal ganglion cells. Journal of Neuroscience 12, 1331–1346.CrossRefGoogle Scholar
Oyster, C.W., Takahashi, E.S., Fry, K.R. & Lam, D.M.-K. (1987). Ganglion cell density in albino and pigmented rabbit retinas labeled with a ganglion cell-specific monoclonal antibody. Brain Research 425, 25–33.CrossRefGoogle ScholarPubMed
Peichl, L., Buhl, E.H. & Boycott, B.B. (1987). α–ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.CrossRefGoogle ScholarPubMed
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: implications for central magnification factors. Vision Research 25, 1795–1810.CrossRefGoogle ScholarPubMed
Perry, V.H., Henderson, Z. & Linden, R. (1983). Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. Journal of Comparative Neurology 219, 356–368.CrossRefGoogle ScholarPubMed
Provis, J.M. (1979). The distribution and size of ganglion cells in the retina of the pigmented rabbit: a qualitative analysis. Journal of Comparative Neurology 185, 121–138.CrossRefGoogle Scholar
Provis, J.M. (1987). Patterns of cell death in the ganglion cell layer of the human fetal retina. Journal of Comparative Neurology 259, 237–246.CrossRefGoogle ScholarPubMed
Provis, J.M., Van Driel, D., Billson, F.A. & Russell, P. (1985). Development of the human retina: patterns of cell distribution and redistribution in the ganglion cell layer. Journal of Comparative Neurology 233, 429–451.CrossRefGoogle ScholarPubMed
Rakic, P. (1971 a). Guidance of neurons migrating to the fetal monkey neocortex. Brain Research 33, 471–476.CrossRefGoogle Scholar
Rakic, P. (1971 b). Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicro-scopic study in Macacus rhesus. Journal of Comparative Neurology 141, 283–312.CrossRefGoogle ScholarPubMed
Rakic, P. & Riley, K.P. (1983). Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 219, 1441–1444.CrossRefGoogle ScholarPubMed
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1987). Remodeling of cat retinal ganglion cells during fetal and postnatal development. Society for Neuroscience Abstracts 13, 589.Google Scholar
Rapaport, D.H., Robinson, S.R. & Stone, J. (1984). Cell movement and birth in the developing cat retina. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 23–38. New York: Alan R. Liss.Google Scholar
Rapaport, D.H. & Stone, J. (1983 a). Time course of the morphological differentiation of cat retinal ganglion cells: influences on soma size. Journal of Comparative Neurology 221, 42–52.CrossRefGoogle ScholarPubMed
Rapaport, D.H. & Stone, J. (1983 b). The topography of cytogene-sis in the developing retina of the cat. Journal of Neuroscience 3, 1824–1838.CrossRefGoogle ScholarPubMed
Rapaport, D.H. & Stone, J. (1984). The area centralis of the retina in the cat and other mammals: focal point for function and development of the visual system. Neuroscience 11, 289–301.CrossRefGoogle Scholar
Robinson, S.R. (1984). Cell death in the kitten retina. Neuroscience Letters (Suppl.) 15, S57.Google Scholar
Robinson, S.R. (1985). The area centralis is the focal point of retinal development in the cat. Proceedings of Australian Physiological and Pharmacological Society 16, 232P.Google Scholar
Robinson, S.R. (1987). Ontogeny of the area centralis in the cat. Journal of Comparative Neurology 255, 50–67.CrossRefGoogle ScholarPubMed
Robinson, S.R. & Dreher, B. (1988 a). Orientations of dendritic fields in the rabbit retina reflect the pattern of retinal growth. Neuroscience Letters (Suppl.) 30, S115.Google Scholar
Robinson, S.R. & Dreher, B. (1988 b). Centro-peripheral maturation gradients in the ganglion cell population of the rabbit: implications for the ontogeny of the visual streak. (Submitted).Google Scholar
Robinson, S.R., Dreher, B., Horsburgh, G.M. & McCall, M.J. (1986). Development of the ganglion cell density gradient in the rabbit retina. Society for Neuroscience Abstracts 12, 985.Google Scholar
Robinson, S.R., Horsburgh, G.M., Dreher, B. & McCall, M.J. (1987). Changes in the numbers of retinal ganglion cells and optic nerve axons in the developing rabbit. Developmental Brain Research 35, 161–174.CrossRefGoogle Scholar
Seefelder, R. (1923). Ueber die Faltenbildungen der embryonalen Retina. Archiv für Ophthalmologie 111, 82.Google Scholar
Sefton, A.J. & Lam, K. (1984). Quantitative and morphological studies on developing optic axons in normal and enucleated albino rats. Experimental Brain Research 57, 107–117.CrossRefGoogle ScholarPubMed
Sengelaub, D.R. & Finlay, B.L. (1982). Cell death in the mammalian visual system during normal development, I: Retinal ganglion cells. Journal of Comparative Neurology 204, 311–317.CrossRefGoogle ScholarPubMed
Sengelaub, D.R., Dolan, R.P. & Finlay, B.L. (1986). Cell generation, death, and retinal growth in the development of the hamster retinal ganglion cell layer. Journal of Comparative Neurology 246, 527–543.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Sretavan, D.W. (1986). Interactions between retinal ganglion cells during the development of the mammalian visual system. Annual Review of Neuroscience 9, 171–207.CrossRefGoogle ScholarPubMed
Stone, J. (1978). The number and distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 180, 753–772.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook. A Guide to the Preparation and Analysis of Retinal Wholemounts. Sydney: Maitland.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System. The Classification of Retinal Ganglion Cells and its Impact on the Neurobi-ology of Vision. New York: Plenum Press.Google Scholar
Stone, J., Egan, M. & Rapaport, D.H. (1985). The site of commencement of retinal maturation in the rabbit. Vision Research 25, 309–317.CrossRefGoogle ScholarPubMed
Stone, J., Maslim, J. & Rapaport, D.H. (1984). The development of the topographical organization of the cat's retina. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 3–21. New York: Alan R. Liss.Google Scholar
Stone, J. & Rapaport, D.H. (1986). The role of cell death in shaping the ganglion cell population of the adult cat retina. In Visual Neuroscience, ed. Pettigrew, J.D., Sanderson, K.J. & Levick, W.R., pp. 157–165. Cambridge, UK: Cambridge University Press.Google Scholar
Stone, J., Rapaport, D.H., Williams, R.W. & Chalupa, L.M. (1982). Uniformity of cell distribution in the ganglion cell layer of the prenatal cat retina: implications for mechanisms of retinal development. Developmental Brain Research 2, 231–242.CrossRefGoogle Scholar
Tay, D., So, K-F., Jen, L.S. & Lau, K.C. (1986). The postnatal development of the optic nerve in hamsters: an electron microscopic study. Developmental Brain Research 30, 267–273.CrossRefGoogle Scholar
Tiao, Y.C. & Blackmore, C. (1976). Regional specialization in the golden hamster's retina. Journal of Comparative Neurology 160, 439–458.Google Scholar
Tucker, G.S. (1978). Light microscopic analysis of kitten retina: postnatal development in the area centralis. Journal of Comparative Neurology 180, 489–500.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1980). A quantitative comparison between the ganglion cell populations and axonal outflows of the visual streak and periphery of the rabbit retina. Journal of Comparative Neurology 189, 215–233.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Hughes, A. (1976). The rabbit optic nerve: fiber diameter spectrum, fiber count, and comparison with a retinal ganglion cell count. Journal of Comparative Neurology 170, 241–252.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373–391.CrossRefGoogle ScholarPubMed
Vitek, D.J., Schall, J.D. & Leventhal, A.G. (1985). Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. Journal of Comparative Neurology 241, 1–11.CrossRefGoogle ScholarPubMed
Vogel, M. (1978). Postnatal development of the cat's retina. Advances in Anatomy, Embryology, and Cell Biology 54, 6–64.Google ScholarPubMed
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741–750.CrossRefGoogle ScholarPubMed
Walsh, C., Polley, E.H., Hickey, T.L. & Gutllery, R.W. (1983). Generation of cat retinal ganglion cells in relation to central pathways. Nature 302, 611–614.CrossRefGoogle ScholarPubMed
Weiss, P. (1949). Differential growth. In The Chemistry and Physiology of Growth, ed. Parpart, A.K., pp. 135–186. New Jersey: Princeton University Press.Google Scholar
Weiss, P. & Amprino, R. (1940). The effect of mechanical stress on the differentiation of scleral cartilage in vitro and in the embryo. Growth 4, 245–258.Google Scholar
Wong, R.O.L. & Hughes, A. (1987 a). Developing neuronal populations of the cat retinal ganglion cell layer. Journal of Comparative Neurology 262, 473–495.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A. (1987 b). Role of cell death in the topogenesis of neuronal distributions in the developing cat retinal ganglion cell layer. Journal of Comparative Neurology 262, 496–511.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A.R (1987 C). The morphology, number, and distribution of large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159–177.CrossRefGoogle ScholarPubMed
Wyllie, A.H., Kerr, J.F.R. & Currie, A.R. (1980). Cell death: the significance of apoptosis. International Review of Cytology 68, 251–306.CrossRefGoogle ScholarPubMed
Young, R.W. (1984). Cell death during differentiation of the retina in the mouse. Journal of Comparative Neurology 229, 362–373.CrossRefGoogle ScholarPubMed
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.CrossRefGoogle ScholarPubMed