Extrinsic Determinants of Retinal Ganglion Cell Development in Cats and Monkeys

  • Audie G. Leventhal
  • Jeffrey D. Schall
Part of the Perspectives in Vision Research book series (PIVR)


Vision in vertebrates is subserved by a number of specialized channels that function in parallel in order to extract simultaneously a variety of features of the environment (reviewed by Stone et al, 1979). As with all things visual, these parallel pathways begin in the retina. The mammalian retina contains a variety of ganglion cell types which have different forms, functional properties, and central projections (Enroth-Cugell and Robson, 1966; Boycott and Wässle, 1974; Cleland and Levick, 1974a,b; Stone and Fukuda, 1974). The developmental processes through which neurons in general and ganglion cells in particular differentiate into distinct types have recently begun to be explored (Eysel et al, 1985; Kirby and Chalupa, 1986; Maslim et al, 1986; Ramoa et al, 1987; Leventhalet al, 1988a,b). Both intrinsic (genetic) factors and extrinsic influences of the cell’s environment appear to mediate the determination of adult cell type.


Beta Cell Ganglion Cell Retinal Ganglion Cell Alpha Cell Dendritic Field 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abramov, I., Gordon, J., Hendrickson, A., Mainline, L., Dobson, V., and Labossiere, E., 1982, The retina of the newborn human infant. Science 217:265–267.PubMedCrossRefGoogle Scholar
  2. Altman, J., 1976, Experimental reorganization of the cerebellar cortex VII. Effects of late X- irradiation schedules that interfere with cell acquisition after stellate cells are formed, J. Comp. Neurol 165:65–76.PubMedCrossRefGoogle Scholar
  3. Altman, J., and Anderson, W. J., 1972, Experimental reorganization of the cerebellar cortex. I. Morphological effects of ehmination of all microneurons with prolonged X-irradiation started at birth, J. Comp. Neurol. 146:355–406.PubMedCrossRefGoogle Scholar
  4. Ault, S. J., Schall, J. D., and Leventhal, A. G., 1985, Experimental alterations of cat retinal ganglion cell dendritic field structure, Soc. Neurosci. Abstr. 11:15.Google Scholar
  5. Bowling, D. B., and Michael, C. R., 1984, Terminal patterns of single, physiologically characterized optic tract fibers in the cat’s lateral geniculate nucleus, J. Neurosci. 4:198–216.PubMedGoogle Scholar
  6. Boycott, B. B., and Wässle, H., 1974, The morphological types of ganglion cells of the domestic cat’s retina, J. Physiol. (London) 240:397–419.Google Scholar
  7. Bradley, P., and Berry, M., 1976, The effects of reduced climbing and parallel fibre input on Purkinje cell dendritic growth. Brain Res. 109:133–151.PubMedCrossRefGoogle Scholar
  8. Carpenter, P., Sefton, A. J., Dreher, B., and Lim, W., 1986, Role of target tissue in regulating the development of retinal ganglion cells in the albino rat: Effects of kainate lesions of the superior colliculus, J. Comp. Neurol. 251:240–259.PubMedCrossRefGoogle Scholar
  9. Cleland, B. G., and Levick, W. R., 1974a, Brisk and sluggish concentrically organized ganglion cells in the cat’s retina, J. Physiol. (London) 240:421–456.Google Scholar
  10. Cleland, B. G., and Levick, W. R., 1974b, Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification, J. Physiol. (London) 240:457–492.Google Scholar
  11. Deitch, J. S., and Rubel, E. W., 1984, Afferent influences on brainstem auditory nuclei of the chicken: Time course and specificity of dendritic atrophy following deafferentation, J. Comp. Neurol. 229:66–79.PubMedCrossRefGoogle Scholar
  12. Enroth-Cugell, C., and Robson, J. G., 1966, The contrast sensitivity of retinal ganglion cell of the cat, J. Physiol. (London) 187:517–552.Google Scholar
  13. Eysel, U. T., Peichl, L., and Wässle, H., 1985, Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period, J. Comp. Neurol. 242:134–145.PubMedCrossRefGoogle Scholar
  14. Friedlander, M. J., Lin, C.-S., Stanford, L. R., and Sherman, S. M., 1979, Structure of physiologically identified X and Y cells in the cat’s lateral geniculate nucleus. Science 204:1114–1117.PubMedCrossRefGoogle Scholar
  15. Harris, R. M., and Woolsey, T. A., 1981, Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damage, J. Comp. Neurol 196:357–376.PubMedCrossRefGoogle Scholar
  16. Hendrickson, A., and Kupfer, C., 1976, The histogenesis of the fovea in the macaque monkey, Invest. Ophthalmol 15:746–756.Google Scholar
  17. Hendrickson, A., and Yuodelis, C., 1984, The morphological development of the human fovea, Ophthalmology 91:603–612.PubMedGoogle Scholar
  18. Hendry, S. H. C., Hockfield, S., Jones, E. G., and McKay, R., 1984, Monoclonal antibody that identifies subsets of neurons in the central visual system of monkey and cat. Nature (London) 307:267–269.CrossRefGoogle Scholar
  19. Illing, R. B., and Wässle, H., 1981, The retinal projection to the thalamus in the cat: A quantitative investigation and a comparison with the retinotectal pathway, J. Comp. Neurol 202:265–285.PubMedCrossRefGoogle Scholar
  20. Jacobs, D. S., Perry, V. H., and Hawken, M. J., 1984, The postnatal reduction of the uncrossed projection from the nasal retina in the cat, J. Neurosci. 4:2425–2433.PubMedGoogle Scholar
  21. Kelly, J. P., and Gilbert, C. D., 1975, The projections of different morphological types of ganglion cells in the cat retina, J. Comp. Neurol 163:65–80.PubMedCrossRefGoogle Scholar
  22. Kirby, M. A., and Chalupa, L., 1986, Retinal crowding alters the morphology of alpha ganglion cells, J. Comp. Neurol. 251:532–541.PubMedCrossRefGoogle Scholar
  23. Kolb, H., 1979, The inner plexiform layer in the retina of the cat: Electron microscopic observations, J. Neurocytol. 8:295–329.PubMedCrossRefGoogle Scholar
  24. Kolb, H., Nelson, R., and Mariani, A., 1981, Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Res. 221:1081–1114.CrossRefGoogle Scholar
  25. 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, J. Neurosci. 2:1024–1042.PubMedGoogle Scholar
  26. Leventhal, A. G., and Creel, D. J., 1985, Retinal projection and functional architecture of cortical areas 17 and 18 in the Tyrosinase-negative albino cat, J. Neurosci. 5:795–807.PubMedGoogle Scholar
  27. Leventhal, A. G., and Schall, J. D., 1983, Structural basis of orientation sensitivity of cat retinal ganglion cells, J. Comp. Neurol. 220:465–475.PubMedCrossRefGoogle Scholar
  28. Leventhal, A. G., Keens, J., and Törk, L, 1980, The afferent ganglion cells and cortical projections of the retinal recipient zone (RRZ) of the cat’s “pulvinar complex,” J. Comp. Neurol. 194:535–554.PubMedCrossRefGoogle Scholar
  29. Leventhal, A. G., Rodieck, R. W., and Dreher, B., 1981, Retinal ganglion cell classes in old-world monkey: Morphology and central projections. Science 213:1139–1142.PubMedCrossRefGoogle Scholar
  30. Leventhal, A. G., Rodieck, R. W., and Dreher, B., 1985, Central projections of cat retinal ganglion cells, J. Comp. Neurol. 237:216–226.PubMedCrossRefGoogle Scholar
  31. Leventhal, A. G., Schall, J. D., and Ault, S. J., 1988a, Extrinsic determinants of retinal ganglion cell structure in the cat, J. Neurosci., 8:2028–2038.PubMedGoogle Scholar
  32. Leventhal, A. G., Schall, J. D., Ault, S. J., Provis, J. M., and Vitek, D. J., 1988b, Class specific cell death during development shapes the distribution and pattern of central projection of cat retina ganglion cells, J. Neurosci., 8:2011–2027.PubMedGoogle Scholar
  33. Linden, R., and Perry, V. H., 1982, Ganglion cell death within the developing retina: A regulatory role for retina dendrites? Neuroscience 7:2813–2837.PubMedCrossRefGoogle Scholar
  34. Mann, L, 1964, The Development of the Human Eye, British Medical Association, London.Google Scholar
  35. Mariani, J., Crepel, F., Mikoshiba, K., Changeux, J. P., and Sotelo, C., 1977, Anatomical, physiological and biochemical studies of the cerebellum from reeler mutant mouse, Philos. Trans. R. Soc. London 281:1–28.CrossRefGoogle Scholar
  36. Maslim, J., Webster, J., and Stone, J., 1986, Stages in the structural differentiation of retinal ganglion cells, J. Comp. Neurol. 254:382–402.PubMedCrossRefGoogle Scholar
  37. Michael, C. R., 1983, Functional classes of neurons in monkey’s lateral geniculate nucleus have distinctive morphology, Soc. Neurosci. Abstr. 9:1047.Google Scholar
  38. Parks, T. N., 1981, Changes in the length and organization of nucleus laminaris dendrites after unilateral otocyst ablation in chick embryos, J. Comp. Neurol. 202:47–57.PubMedCrossRefGoogle Scholar
  39. Perry, V. H., and Cowey, A., 1984, Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey, Neuroscience 12:1125–1137.PubMedCrossRefGoogle Scholar
  40. Perry, V. H., and Linden, R., 1982, Evidence for dendritic competition in the developing retina. Nature (London) 297:683–685.CrossRefGoogle Scholar
  41. Perry, V. H., Oehler, R., and Cowey, A., 1984, Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey, Neuroscience 12:1101–1123.PubMedCrossRefGoogle Scholar
  42. Polyak, S., 1941, The Retina, University of Chicago Press, Chicago.Google Scholar
  43. Rakic, P., and Sidman, R. L., 1973a, Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice, J. Comp. Neurol. 152:103–132.PubMedCrossRefGoogle Scholar
  44. Rakic, P., and Sidman, R. L., 1973b, Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice, J. Comp. Neurol. 152:133–162.PubMedCrossRefGoogle Scholar
  45. Ramoa, A. S., Campbell, G., and Shatz, C. J., 1987, Transient morphological features of identified ganglion cells in living fetal and neonatal retina, Science 237:522–525.PubMedCrossRefGoogle Scholar
  46. Rapaport, D. H., and Stone, J., 1983, Time course of morphological differentiation of cat retinal ganglion cells: Influences on soma size, J. Comp. Neurol. 221:42–52.PubMedCrossRefGoogle Scholar
  47. Rodieck, R. W., Binmoeller, K. F., and Dineen, J., 1985, Parasol and midget ganglion cells of the human retina, J. Comp. Neurol. 233:115–132.PubMedCrossRefGoogle Scholar
  48. Rolls, E. T., and Cowey, A., 1970, Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys, Exp. Brain Res. 10:298–310.PubMedCrossRefGoogle Scholar
  49. Rowe, M. H., and Stone, J., 1980, The interpretation of variation in the classification of nerve cells. Brain Behav. Evol. 17:1233–1251.Google Scholar
  50. Schall, J. D., and Leventhal, A. G., 1987, Relationships between ganglion cell dendritic structure and retinal topography in the cat. J. Comp. Neurol. 257:149–159.PubMedCrossRefGoogle Scholar
  51. Schall, J. D., Perry, V. H., and Leventhal, A. G., 1987, Ganglion cell dendritic structure and retinal topography in the rat, J. Comp. Neurol. 257:160–165.PubMedCrossRefGoogle Scholar
  52. Sotelo, C., 1975, Anatomical, physiological and biochemical studies of the cerebellum from mutant mice. II. Morphological study of cerebellar cortical neurons and circuits in the weaver mouse, Brain Res. 94:19–44.PubMedCrossRefGoogle Scholar
  53. Sotelo, C., and Arsenio-Nunes, M. L., 1976, Development of Purkinje cells in absence of climbing ühers. Brain Res. 111:389–395.CrossRefGoogle Scholar
  54. Sotelo, C., and Changeux, J. P., 1974, Transsynaptic degeneration in cascade in cerebellar cortex of staggerer mutant mice. Brain Res. 67:519–526.PubMedCrossRefGoogle Scholar
  55. Steffan, H., and Van der Loos, H., 1980, Early lesions of mouse vibrissal follicles: Their influence on dendritic orientation in the cortical barrelfield, Exp. Brain Res. 40:419–431.Google Scholar
  56. Stevens, J. K., McGuire, B. A., and Sterhng, P., 1980, Toward a functional architecture of the retina: Serial reconstruction of adjacent ganglion cells. Science 207:317–319.PubMedCrossRefGoogle Scholar
  57. Stone, J., 1965, A quantitative analysis of the distribution of ganglion cells in the cat’s retina, J. Comp. Neurol. 124:337–352.PubMedCrossRefGoogle Scholar
  58. Stone, J., 1966, The nasotemporal division of the cat’s retina, J. Comp. Neurol. 126:585–600.PubMedGoogle Scholar
  59. Stone, J., and Fukuda, Y., 1974, Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells, J. Neurophysiol. 37:722–748.PubMedGoogle Scholar
  60. Stone, J., and Johnston, E., 1981, The topography of primate retina: A study of the human, bushbaby, and new- and old-world monkeys, J. Comp. Neurol. 196:205–223.PubMedCrossRefGoogle Scholar
  61. Stone, J., Campion, J. E., and Leicester, J., 1978, The nasotemporal division of the retina in the Siamese cat, J. Comp. Neurol. 180:783–798.PubMedCrossRefGoogle Scholar
  62. Stone, J., Dreher, B., and Leventhal, A. G., 1979, Hierarchical and parallel mechanisms in the organization of the visual cortex. Brain Res. Rev. 1:345–394.CrossRefGoogle Scholar
  63. Vitek, D. J., Schall, J. D., and Leventhal, A. G., 1985, Morphology, central projections and dendritic field orientation of retinal ganglion cells in the ferret, J. Comp. Neurol. 241:1–11.PubMedCrossRefGoogle Scholar
  64. Walsh, C., and Polley, E. H., 1985, The topography of ganglion cell production in the cat’s retina, J. Neurosci. 5:741–750.PubMedGoogle Scholar
  65. Wässle, H., and Illing, R. B., 1980, The retinal projection to the superior colliculus in the cat: A quantitative study with HRP, J. Comp. Neurol. 190:333–356.PubMedCrossRefGoogle Scholar
  66. Wässle, H., Peichl, L., and Boycott, B. B., 1981a, Dendritic territories of cat retinal ganglion cells, Nature (London) 292:344–345.CrossRefGoogle Scholar
  67. Wässle, H., Peichl, L., and Boycott, B. B., 1981b, Morphology and topography of on- and off- alpha cells in the cat retina, Proc. R. Soc. London Ser. B 212:157–175.CrossRefGoogle Scholar
  68. Woolsey, T. A., and Van der Loos, H., 1970, The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17:205–242.PubMedCrossRefGoogle Scholar
  69. Woolsey, T. A., Dierker, M. L., and Wann, D. F., 1975, Mouse Smi cortex: Qualitative and quantitative classification of Goldi-impregnated barrel neurons, Proc. Natl. Acad. Sci. U.S.A. 72:2165–2169PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Audie G. Leventhal
    • 1
  • Jeffrey D. Schall
    • 2
  1. 1.Department of Anatomy, School of MedicineUniversity of UtahSalt Lake CityUSA
  2. 2.Department of Brain and Cognitive ScienceMassachusetts Institute of TechnologyCambridgeUSA

Personalised recommendations