Advertisement

Development of Cell Density Gradients in the Retinal Ganglion Cell Layer of Amphibians and Marsupials

Two Solutions to One Problem
  • Lyn D. Beazley
  • Sarah A. Dunlop
  • Alison M. Harman
  • Lee-Ann Coleman
Part of the Perspectives in Vision Research book series (PIVR)

Abstract

A feature of the mature vertebrate retina is the nonuniform distribution of ganglion cells. High ganglion cell densities in the temporally situated area centralis and in the nasotemporally aligned visual streak subserve high activity vision in the frontal field and along the horizon. We have described the different developmental strategies adopted in amphibia and in mammals to form an area centralis and visual streak from an essentially uniform cell distribution. To facilitate the mammalian studies, we chose to study marsupials since they are born at a much more immature stage than eutherians.

In frogs, cell division continues at the retinal circumference throughout life, adding cells to each retinal layer. During the formation of cell density gradients, more cells are added at the nasal and temporal poles than elsewhere, suggesting that high cell densities are generated by differential cell addition. Dying cells have not been observed during this process, suggesting that cell death does not play a part in shaping live cell density gradients. Continued areal growth reduces cell densities throughout life.

By contrast, in mammals, all ganglion cells are generated in an early phase of cell division well before the area centralis and visual streak are present. As these specializations appear, ganglion cell numbers fall by approximately one third. Dying cells are seen and are present in greater numbers in regions destined to become of low cell density than elsewhere, indicating that cell death may play a role in the formation of live cell topography. Asymmetric retinal expansion may also be important. A second phase of mitosis adds cells to the inner and outer nuclear layers at the time cell density gradients become pronounced in the ganglion cell layer. This later phase of cell generation ceases first in areas adjacent to the presumptive area centralis. Continued cell addition to peripheral retina would differentially expand the retina and may thereby reduce cell densities more in those parts of the ganglion cell layer outside the area centralis and visual streak. However, even after the completion of mitosis and cell death, ganglion cell density gradients are not as steep as in the adult. During the later stages, ganglion cell topography must therefore be accentuated by other factors of retinal growth such as changes in the size and shape of cells.

Keywords

Ganglion Cell Retinal Ganglion Cell Optic Nerve Head Ganglion Cell Layer Outer Nuclear Layer 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Beach, D. H., and Jacobson, M., 1979, Patterns of cell proliferation in the retina of the clawed frog during development, J. Comp. Neurol 183:603–614.PubMedCrossRefGoogle Scholar
  2. Beazley, L. D., 1984, Formation of specific neuronal connections in the visual system of lower vertebrates, inCurrent Topics in Research on Synapses, Vol. 1 (D. G. Jones, ed.), pp. 53–119, Alan R. Liss, New York.Google Scholar
  3. Beazley, L. D., and Dunlop, S. A., 1983, The evolution of an area centralis and visual streak in the marsupial Setonix brachyurus, J. Comp. Neurol 216:211–231.PubMedCrossRefGoogle Scholar
  4. Beazley, L. D., Darby, J. E., and Perry, V. H., 1986, Cell death in the retinal ganglion cell layer during optic nerve regeneration for the frog Rana pipiens, Vision Res. 26:543–556.PubMedCrossRefGoogle Scholar
  5. Beazley, L. D., Perry, V. H., Baker, B., and Darby, J. E., 1987, An investigation into the role of ganglion cells in the regulation of division and death of other retinal cells, Dev. Brain Res. 33:169–184.CrossRefGoogle Scholar
  6. Bousfield, J. D., and Pessoa, V. F., 1980, Changes in ganglion cell density during postmetamorphic development in a neotropical tree frog, Hyla raniceps, Vision Res. 20:501–510.PubMedCrossRefGoogle Scholar
  7. Braekevelt, C. R., Beazley, L. D., Dunlop, S. A., and Darby, J. E., 1986, Numbers of axons in the optic nerve and of retinal ganglion cells during development in the marsupial Setonix brachyurus, Dev. Brain Res. 25:117–125.CrossRefGoogle Scholar
  8. Brooke, R. N. L., Downer, J. De C, and Powell, T. P. S., 1965, Centrifugal fibers to the retina in the monkey and cat, Nature (London) 207:1365–1367.CrossRefGoogle Scholar
  9. Bunt, A. H., and Minckler, D. S., 1977, Displaced ganglion cells in the retina of the monkey. Invest. Ophthalmol. Vis. Sci. 16:95–98.PubMedGoogle Scholar
  10. Bunt, S. M., and Lund, R. D., 1981, Development of a transient retino-retinal pathway in hooded and albino rats, Brain Res. 211:399–404.PubMedCrossRefGoogle Scholar
  11. Bunt, S. M., Lund, R. D., and Land, P. W., 1983, Prenatal development of the optic projection in albino and hooded rats, Dev. Brain Res. 6:149–168.CrossRefGoogle Scholar
  12. Campbell, G., Ramoa, A. S., and Shatz, C. J., 1987, Transient features of ganglion cell morphology during development of the cat retina. Invest. Ophthalmol. Vis. Sci. (Suppl.) 28:286.Google Scholar
  13. Coleman, L.-A., Dunlop, S. A., and Beazley, L. D., 1984, Patterns of cell division during visual streak formation in the frog Limnodynastes dorsalis, J. Embryol. Exp. Morphol. 83:119–135.PubMedGoogle Scholar
  14. Coleman, L.-A., Harman, A. M., and Beazley, L. D., 1987, Displaced retinal ganglion cells in the wallaby Setonix brachyurus, Vision Res. 27:1269–1277.PubMedCrossRefGoogle Scholar
  15. Drager, U. C., 1985, Birth dates of retinal ganglion cells giving rise to the crossed and uncrossed optic projections in the mouse, Proc. R. Soc. Lond. (Biol.) 224:57–77.CrossRefGoogle Scholar
  16. Dreher, B., Potts, R. A., Ni, S. Y. K., and 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, Vol. 9 (J. Stone, B. Dreher, and D. H. Rapaport, eds.), pp. 39–57, Alan R. Liss, New York.Google Scholar
  17. Dunlop, S. A., and Beazley, L. D., 1981, Changing retinal ganglion cell distribution in the frog Heleioporus eyrei, J. Comp. Neurol. 202:221–236.PubMedCrossRefGoogle Scholar
  18. Dunlop, S. A., and Beazley, L. D., 1984a, Development of the area centralis and visual streak in mammals, in Development of Visual Pathways in Mammxils, Vol. 9 (J. Stone, B. Dreher, and D. H. Rapaport, eds.), pp. 75–88, Alan R. Liss, New York.Google Scholar
  19. Dunlop, S. A., and Beazley, L. D., 1984b, A morphometric study of the retinal ganglion layer and optic nerve in postmetamorphic Xenopus laevis. Vision Res. 5:417–427.CrossRefGoogle Scholar
  20. Dunlop, S. A., and Beazley, L. D., 1985a, Cell distributions in the retinal ganglion cell layer of adult Leptodactylid frogs after premetamorphic eye rotation, J. Embryol. Exp. Morphol. 89:159–173.PubMedGoogle Scholar
  21. Dunlop, S. A., and Beazley, L. D., 1985b, Changing distribution of retinal ganglion cells during area centralis and visual streak formation in the marsupial Setonix brachyurus. Dev. Brain Res. 23:81–90.CrossRefGoogle Scholar
  22. Dunlop, S. A., and Beazley, L. D., 1986, A retino-retinal projection contributes minimally towards high axon numbers in the marsupial Setonix brachyurus, Soc. Neurosci. Abstr. 12:3413.Google Scholar
  23. Dunlop, S. A., and Beazley, L. D., 1987, Cell death in the developing retinal ganglion cell layer of the wallaby Setonix brachyurus, J. Comp. Neurol. 264:14–23.PubMedCrossRefGoogle Scholar
  24. Dunlop, S. A., Longley, W. A., and Beazley, L. D., 1987, Development of the area centralis and visual streak in the grey kangaroo Macropus fuliginosus. Vision Res. 27:151–164.PubMedCrossRefGoogle Scholar
  25. Dunlop, S. A., Coleman, L.-A., Harman, A. M., and Beazley, L. D., 1988, Development of the marsupial primary visual system, in The Developing Marsupial-A Model for Biomedical Research (C. H. Tyndale-Biscoe and P. A. Janssens, eds.), pp. 117–131, Springer-Verlag, Heidelberg.Google Scholar
  26. Fite, K. V., 1976, The Amphibian Visual System. A Multidisciplinary Approach,Academic Press, New York.Google Scholar
  27. Freeman, B., and Tancred, E., 1978, The number and distribution of ganglion cells in the retina of the brush-tailed possum, Trichosurus vulpecula, J. Comp. Neurol. 177:557–568.PubMedCrossRefGoogle Scholar
  28. Freeman, B., and Watson, C. R. R., 1978, The optic nerve of the brush-tailed possum, Trichosurus vulpecula: Fibre diameter spectrum and conduction latency groups, J.Comp. Neurol 179:739–752.PubMedCrossRefGoogle Scholar
  29. Fujita, S., 1962, Kinetics of cellular proliferation, Exp. Cell Res. 28:52–60.PubMedCrossRefGoogle Scholar
  30. Glucksmann, A., 1940, Development and differentiation of the tadpole eye, Br. J. Ophthalmol. 25:154–178.Google Scholar
  31. Harman, A. M., and Beazley, L. D., 1987, Patterns of cytogenesis in the developing retina of the wallaby Setonix brachyurus, Anat. Embryol. 177:123–130.PubMedCrossRefGoogle Scholar
  32. Harman, A. M., and Beazley, L. D., 1988, Postnatal cytogenesis in the dorsal lateral geniculate nucleus (LGNd) and superior colliculus (SC) of the marsupial, Setonix brachyurus (quokka), Neurosci. Lett. (Suppl.) 30:873.Google Scholar
  33. Harman, A. M., and Beazley, L. D., 1988, Generation of retinal cells in the wallaby,Setonix brachyurus, Neurosci., in press.Google Scholar
  34. Hendrickson, A., and Kupfer, C., 1976, The histogenesis of the fovea in the macaque monkey. Invest. Ophthal. 15:746.Google Scholar
  35. Hinds, J. W., and Hinds, P. L., 1978, Early development of amacrine cells in the mouse retina: An electron microscopic, serial section analysis, J. Comp. Neurol. 179:277–300.PubMedCrossRefGoogle Scholar
  36. Hinds, J. W., and Hinds, P. L., 1983, Development of retinal amacrine cells in the mouse embryo: Evidence for two modes of formation, J. Comp. Neurol. 213:1–23.PubMedCrossRefGoogle Scholar
  37. Hokoc, J. N., and Oswaldo-Cruz, E., 1978, Quantitative analysis of the opossum’s optic nerve: An electron microscopic study, J. Comp. Neurol. 178:773–782.PubMedCrossRefGoogle Scholar
  38. Hokoc, J. N., and Oswaldo-Cruz, E., 1979, A regional specialization in the opossum’s retina: Quantitative analysis of the ganglion cell layer, J. Comp. Neurol. 183:385.PubMedCrossRefGoogle Scholar
  39. Hughes, A., 1961, Cell degeneration in the larval ventral horn of Xenopus laevis, J. Embryol. Exp. Morphol. 9:269.PubMedGoogle Scholar
  40. Hughes, A., 1975, A quantitative analysis of cat retinal ganglion cell topography, J. Comp. Neurol. 163:107–128.PubMedCrossRefGoogle Scholar
  41. Hughes, A., 1977, The topography of vision in mammals, in Handbook of Sensory Physiology, Vol. VII/5 (F. Crescitelli, ed.), pp. 615–756, Springer-Verlag, Berlin.Google Scholar
  42. Hughes, A., 1985, New perspectives in retinal organization, in Progress in Retinal Research, Vol. 4 (N. N. Osborne and G.J. Chader, eds.), pp. 243–313, Pergamon Press, Oxford.Google Scholar
  43. Humphrey, M. F., and Beazley, L. D., 1985, Retinal ganglion cell death during optic nerve regeneration in the frog Hyla moorei, J. Comp. Neurol. 236:383–402.CrossRefGoogle Scholar
  44. Hunt, R. R., Cohen, J. S., and Mason, B. J., 1987, Cell patterning in pigment-chimeric eyes in Xenopus: Germinal cell transplants and their contributions to growth of the pigmented retinal epithelium, Proc. Natl. Acad. Sci. U.S.A. 84:3302–3306.PubMedCrossRefGoogle Scholar
  45. Itaya, S. K., 1980, Retinal efferents from the pretectal area in the rat. Brain Res. 201:436–441.PubMedCrossRefGoogle Scholar
  46. Jacobson, M., 1960, The representation of the visual field on the optic tectum of the frog: Evidence for the presence of an area centralis retinae, J.Physiol. 154:31–32.Google Scholar
  47. Jacobson, M., 1962, The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count, Q. J. Exp. Physiol. 47:170–178.Google Scholar
  48. Jacobson, M., 1976, Histogenesis of the retina of the clawed frog with implications for the pattern of development of retinotectal connections. Brain Res. 103:541–545.PubMedCrossRefGoogle Scholar
  49. Johns, P. R., 1977, Growth of the adult goldfish eye, III. Source of new retinal cells, J. Comp. Neurol. 176:343–358.PubMedCrossRefGoogle Scholar
  50. Johns, P. R., and Easter, S., 1977, Growth of the adult goldfish eye. II. Increase in retinal cell number, J. Comp. Neurol. 176:331–342.PubMedCrossRefGoogle Scholar
  51. Johns, P. R., Rusoff, A. C., and Dubin, M. W., 1979, Postnatal neurogenesis in the kitten retina, J. Comp. Neurol. 187:545–556.PubMedCrossRefGoogle Scholar
  52. Kirby, M. A., Clift-Forsberg, L., Wilson, P. D., and Rapisardi, S. C., 1982, Quantitative analysis of the optic nerve of the North American opossum (Didelphis virginiana): An electron microscope study, J. Comp. Neurol. 211:318–327.PubMedCrossRefGoogle Scholar
  53. Kuwabara, T., and Wiedman, T. A., 1974, Development of the prenatal rat retina, Invest. Ophthalmol Vis. Sci. 13:725–739.Google Scholar
  54. Lia, B., Williams, R. W., and Chalupa, L. M., 1987, Formation of retinal ganglion cell topography during prenatal development. Science 236:848–851.PubMedCrossRefGoogle Scholar
  55. Linden, R., 1987, Displaced ganglion cells in the retina of the rat, J. Comp. Neurol. 258:138–143.PubMedCrossRefGoogle Scholar
  56. Mann, I., 1964, The Development of the Eye, 3rd ed., British Medical Association, London.Google Scholar
  57. Mastronarde, D. N., Thibeault, M. A., and Dubin, W. M., 1984, Non-uniform postnatal growth of the cat retina, J. Comp. Neurol. 228:598–608.PubMedCrossRefGoogle Scholar
  58. Meyer, R. L., 1978, Evidence from thymidine labelling for continuing growth of retina and tectum in juvenile goldfish, Exp. Neurol. 59:99–111.PubMedCrossRefGoogle Scholar
  59. Perry, V. H., 1981, Evidence for an amacrine cell system in the ganglion layer of the rat retina, Neuroscience. 6:931–944.PubMedCrossRefGoogle Scholar
  60. Perry, V. H., 1982, The ganglion cell layer of the mammalian retina, in Progress in Retinal Research (N. N. Osborne and G. J. Chader, eds.), pp. 53–80, Pergamon Press, Oxford.Google Scholar
  61. Perry, V. H., and Cowey, A., 1985, The ganglion cell and cone distributions in the monkey’s retina: Implications for central magnification factors. Vision Res. 12:1795–1810.CrossRefGoogle Scholar
  62. Perry, V. H., Henderson, Z., and Linden, R., 1983, Postnatal changes in the retinal ganglion cell and optic axon populations in the pigmented rat, J. Comp. Neurol. 219:356–368.PubMedCrossRefGoogle Scholar
  63. Peterson, E. H., and Ulinski, P. S., 1979, Quantitative studies of retinal ganglion cells in a turtle, Pseudemys scripta elegans. I. Number and distribution of ganglion cells, J. Comp. Neurol. 186:17–42.PubMedCrossRefGoogle Scholar
  64. Provis, J. M., 1979, The distribution and size of ganglion cells in the retina of the pigmented rabbit: A quantitative analysis, J. Comp. Neurol. 185:121–139.PubMedCrossRefGoogle Scholar
  65. Provis, J. M., 1987, Patterns of cell death in the ganglion cell layer of the human fetal retina, J. Comp. Neurol. 259:237–246.PubMedCrossRefGoogle Scholar
  66. Rapaport, D. H., and Stone, J., 1982, The site of commencement of maturation in mammalian retina: Observations in the cat. Dev. Brain Res. Google Scholar
  67. Rapaport, D. H., Wilson, P. D., and Rowe, M. H., 1981, The distribution of ganglion cells in the retina of the North American opossum (Didelphis virginiana), J. Comp. Neurol. 199:465- 480.Google Scholar
  68. Saxen, L., 1954, The development of the visual cells, Ann. Acad. Sei. Fenn. A 23:1–93.Google Scholar
  69. Scalia, F., and Teitelbaum, I., 1978, Absence of efferents to the retina in the frog and toad. Brain Res. 153:340–344.PubMedCrossRefGoogle Scholar
  70. Schnyder, H., and Kunzle, H., 1984, Is there a retinopetal system in the rat? Exp. Brain Res. 56:502–508.PubMedCrossRefGoogle Scholar
  71. Sengelaub, D. R., and Finlay, B. L., 1982, Cell death in the mammalian visual system during normal development. I. Retinal ganglion cells, J. Comp. Neurol. 204:311–317.PubMedCrossRefGoogle Scholar
  72. Sengelaub, D. R., Dolan, R. P., and Finlay, B. L., 1986, Cell generation, death and retinal growth in the hamster retinal ganglion cell layer, J. Comp. Neurol. 246:527–543.PubMedCrossRefGoogle Scholar
  73. Sidman, R. L., 1961, Histogenesis of mouse retina studied with thymidine-3H, in The Structure of the Eye (G. K. Smelser, ed.), pp. 487–506, Academic Press, New York.Google Scholar
  74. Steinberg, R. H., Reid, M., and Lacy, P. L., 1973, The distribution of rods and cones in the retina of the cat (Felis domesticus), J. Comp. Neurol. 148:229–248.PubMedCrossRefGoogle Scholar
  75. 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
  76. Stone, J., 1978, The number and distribution of ganglion cells in the cat’s retina, J. Comp. Neurol. 180:753–772.PubMedCrossRefGoogle Scholar
  77. Stone, J., Egan, M., and Rapaport, D. H., 1985, The site of commencement of retinal maturation in the rabbit, Vision Res. 25:309–317.PubMedCrossRefGoogle Scholar
  78. Stone, J., Maslim, J., and Rapaport, D. H., 1984, The development of the topographical organisation of the cat’s retina, inDevelopment of Visual Pathways in Mammals (J. Stone, B. Dreher, and D. H. Rapaport, eds.), pp. 3–21, Alan R. Liss, New York.Google Scholar
  79. Stone, J., Rapaport, D. H., Williams, R. W., and Chalupa, L., 1982, Uniformity of cell distribution in the ganglion cell layer of the prenatal cat retina: Implications for mechanisms of retinal development, Dev. Brain Res. 2:231–242.CrossRefGoogle Scholar
  80. Straznicky, K., and Gaze, R. M., 1971, The growth of the retina in Xenopm laevis: An autoradiographic study, J. Embryol. Exp. Morphol. 26:67.PubMedGoogle Scholar
  81. Tay, D., Hiscock, J., and Straznicky, C., 1982, Temporo-nasal asymmetry in the accretion of retinal ganglion cells in late larval and postmetamorphic Xenopus, Anat. Embryol 164:75–83.PubMedCrossRefGoogle Scholar
  82. 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
  83. Walsh, C., Polley, E. H., Hickey, T. L., and Guillery, R. W., 1983, Generation of cat retinal ganglion cells in relation to central pathways. Nature (London) 302:611.CrossRefGoogle Scholar
  84. Williams, R. W., Bastiani, M. J., Lia, B., and Chalupa, L. M., 1986, Growth cones, dying axons and developmental fluctuations in the fibre population of the cat’s optic nerve, J. Comp. Neurol. 246:32–69.PubMedCrossRefGoogle Scholar
  85. Wong, R. O. L., and Dunlop, S. A. D., 1988, Dendritic development of retinal ganglion cells in the marsupial Setonix brachyurvs, quokka, Neurosci. Lett. (Suppl.) 30:S141.Google Scholar
  86. Wong, R. O. L., and Hughes, A., 1987a, Developing neuronal populations of the cat retinal ganglion cell layer, J. Comp. Neurol. 262:433–495.Google Scholar
  87. Wong, R. O. L., and Hughes, A., 1987b, The role of cell death in the topogenesis of neuronal populations in the cat retinal ganglion cell layer, J. Comp. Neurol. 262:496–511.PubMedCrossRefGoogle Scholar
  88. Wong, R. O. L., Wye-Dvorak, J., and Henry, G. H., 1986, Morphology and distribution of neurons in the retinal ganglion cell layer of the adult Tammar wallaby-Macropus eugenii, J. Comp. Neurol. 253:1–12.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Lyn D. Beazley
    • 1
  • Sarah A. Dunlop
    • 1
  • Alison M. Harman
    • 1
  • Lee-Ann Coleman
    • 1
  1. 1.Department of PsychologyUniversity of Western AustraliaNedlandsAustralia

Personalised recommendations