The Regulation of Neuronal Production during Retinal Neurogenesis

  • Thomas A. Reh
Part of the Perspectives in Vision Research book series (PIVR)


The vertebrate central nervous system is composed of a large number of different types of neurons that can be distinguished on the basis of morphology, biochemistry, and electrophysiology. During the development of the nervous system, these various kinds of neurons are produced in precise ratios with respect to one another, resulting in the appropriate numbers of the different cell types necessary for the functioning of the adult nervous system. How these different cell types are generated in the correct numbers and ratios is a central problem of developmental neurobiology. While there is some information concerning the factors involved in the origin of cellular diversity in the peripheral nervous system (Patterson, 1978; Le Douarin, 1986; Rohrer et al, 1986) and work in neural crest has shown that a variety of environmental factors can influence the particular phenotype the neural crest cell ultimately achieves, little is known about the mechanisms that give rise to the even greater cellular diversity in the central nervous system. The question of how the precise ratios of neurons found in the adult CNS arise during development is the subject of this chapter. While cell death is likely to play a very important role in regulating final neuronal numbers in many areas of the CNS (Cowan, 1973), this aspect of neural development is reviewed in other chapters in this volume (Chapters 7, 9, and 10) and therefore will only be considered briefly in this chapter.


Nerve Growth Factor Ganglion Cell Retinal Ganglion Cell Neural Crest Cell Kainic Acid 
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  1. Anderson, M. J., and Waxman, S. G., 1985a, Neurogenesis in adult vertebrate spinal cord in situ and in vitro: A new model system, Ann. N.Y. Acad. Sci. xx:213–233.Google Scholar
  2. Anderson, M. J., and Waxman, S. G., 1985b, Neurogenesis in tissue cultures of adult teleost spinal cord. Dev. Brain Res. 20:203–212.Google Scholar
  3. Barakat, L, and Sensenbrenner, M., 1981, Brain extracts that promote the proliferation of neuroblasts from chick embryo in culture. Dev. Brain Res. 1:355–368.Google Scholar
  4. Barakat, I., Sensenbrenner, M., and Labourdette, G., 1983, Purines stimulate chick neuroblast proliferation in culture, Neurosci. Lett. 41:325–330.PubMedGoogle Scholar
  5. Barakat, L, Sensenbrenner, M., and Labourdette, G., 1984, In bovine extracts, RNAs are active factors that stimulate the proliferation of chick neuroblasts in culture, J. Neuro sci. Res. 11:117–129.Google Scholar
  6. 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.PubMedGoogle Scholar
  7. 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.Google Scholar
  8. Benveniste, E. N., and Merril, J. E., 1986, Stimulation of oligodendroglial proliferation and maturation by interleukin 2, Nature (London) 321:610–613.Google Scholar
  9. Besnard, F., Perraud, F., Sensenbrenner, M., and Labourdette, G., 1987, Platelet derived growth factor is a mitogen for glial but not for neuronal rat brain cells in vitro, Neurosci. Lett. 73:287–292.PubMedGoogle Scholar
  10. Blanks, J. C., and Bok, D., 1977, An autoradiographic analysis of postnatal cell proliferation in the normal and degenerative mouse retina, J. Comp. Neurol. 174:317–328.PubMedGoogle Scholar
  11. Bottenstein, J. E., 1985, Growth and differentiation of neural cells in defined media, in Cell Culture in the Neurosciences (J. E. Bottenstein and G. Sato, eds.), pp. 3–44, Plenum Press, New York.Google Scholar
  12. Breakefield, X. O., 1976, Neurotransmitter metabolism in murine neuroblastoma. Life Sci. 18:267–278.PubMedGoogle Scholar
  13. Cone, C. D., and Cone, C. M., 1976, Induction of mitosis in mature neurons in central nervous system by sustained depolarization, Science 192:155–158.PubMedGoogle Scholar
  14. Cone, C. D., and Cone, C. M, 1978, Evidence of normal mitosis with complete cytokinesis in central nervous system neurons during sustained depolarization witli guavaine, Exp. Neurol. 60:41–55.PubMedGoogle Scholar
  15. Cowan, W. M., 1973, Neuronal death as a regulative mechanism in the control of cell number in the nervous system, in Development and Aging in the Nervous System (M. Rockstein, ed.), pp. 19–41, Academic Press, New York.Google Scholar
  16. Cowan, W. M., and Finger, T. E., 1982, Regeneration and regulation in the developing central nervous system with special reference to the reconstitution of the optic tectum of the chick following removal of the mesencephalic alar plate, in Neuronal Development (N. C. Spitzer, ed.), pp. 377–412, Plenum Press, New York.Google Scholar
  17. Detwiler, S. R., 1945, The results of unilateral and bilateral extirpation of the forebrain of Amblystoma, J. Exp. Zool 100:103–115.Google Scholar
  18. Detwiler, S. R., 1946, Midbrain regeneration in Amblystoma, Anat. Ree. 94:229–241.Google Scholar
  19. Ek, B., Westermark, B., Wateson, A., and Heldin, C. H., 1982, Stimulation of tyrosine-specific phosphorylation by platelet derived growth factor, Nature (London) 295:419–420.Google Scholar
  20. Erickson, C. A., and Turley, E. A., 1987, The effects of epidermal growth factor on neural crest cells in tissue culture, Exp. Cell Res. 169:267–279.PubMedGoogle Scholar
  21. Erlich, O., and Morgan, I. G., 1980, Kainic acid lesions chick retina amacrine cells, Neuro sci. Lett. 17:43–48.Google Scholar
  22. Giulian, D., and Lahman, L. B., 1985, Interleukin I simulation of astroglial proliferation after brain injury. Science 228:497–499.PubMedGoogle Scholar
  23. Giulian, D., and Young, D. G., 1986, Brain peptides and glial growth. Identification of cells that secrete glial promoting factors, J. Cell Biol. 102:812–820.PubMedGoogle Scholar
  24. Giulian, D., Allen, R. L., Baker, T. J., and Tomozawa, Y., 1986, Brain peptides and glial growth, J. Cell Biol. 102:803–811.PubMedGoogle Scholar
  25. Haffke, S. C., and Seeds, N., 1975, Neuroblastoma:The E. coli of neurobiology, Life Sci. 16:1649–1658.PubMedGoogle Scholar
  26. Hampton, C. K., Garcia, C., and Redburn, D. A., 1981, Localization of kainic acid sensitive cells in the mammalian retina, J. Neurosci. Res. 6:99–111.PubMedGoogle Scholar
  27. Harrison, R. G., 1947, Wound healing and reconstitution of the central nervous system of the amphibian embryo after removal of parts of the neural plate, J. Exp. Zool. 106:27.PubMedGoogle Scholar
  28. Heldin, C. H., Westermark, B., and Wasteson, A., 1981, Specific receptors for platelet-derived growth factor on cells derived from connective tissue and glia, Proc. Natl. Acad. Sci. U.S.A. 78:3664–3668.PubMedGoogle Scholar
  29. Herrup, K., 1986, Cell lineage relationships in the development of the mammalian CNS: Role of cell lineage in control of cerebellar Purkinje cell number. Dev. Biol. 115:148–154.PubMedGoogle Scholar
  30. Herrup, K., Diglio, T. J., and Letsou, A., 1984, Cell lineage relationships in the development of the mammalian CNS: The facial nerve nucleus. Dev. Biol. 103:329–336.PubMedGoogle Scholar
  31. Hinds, J. W., and Hinds, P. L., 1974, Early ganglion cell differentiation in the mouse retina: An electron microscopic analysis utilizing serial sections. Dev. Biol. 37:381–416.PubMedGoogle Scholar
  32. 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.PubMedGoogle Scholar
  33. Hinds, J. W., and Hinds, P. L. 1979, Differentiation of photoreceptors and horizontal cell in the embryonic mouse retina: An electron microscopic serial section analysis, J. Comp. Neurol. 187:495–512.PubMedGoogle Scholar
  34. Hollyfield, J. G., 1968, Differential addition of cells to the retina in Rana pipiens tadpoles. Dev. Biol. 18:163–179.PubMedGoogle Scholar
  35. Holtfreter, J., and Hamburger, V., 1955, Amphibians, inAnalysis of Development (B. Willier, P. Weiss, and V. Hamburger, eds.), pp. 230–296, W. B. Saunders, Philadelphia.Google Scholar
  36. Ingham, C. A., and Morgan, 1. G., 1983, Dose-dependent effects of intravitreal kainic acid on specific cell types in chicken retina, Neuroscience 9:151–181.Google Scholar
  37. Juurlink, B., and Federhoff, S., 1982, The development of mouse spinal cord in tissue culture. II. Development of neuronal precursor cells, In Vitro 18:179–182.PubMedGoogle Scholar
  38. Kaltenbach, J. C., and Hobbs, A. W., 1972, Local action of thyroxine on amphibian metamorphosis. V. Cell Division in the eye of the anuran larvae affected by thyroxine-cholesterol implants, J. Exp. Zool 179:157–165.PubMedGoogle Scholar
  39. Kimmel, C. D., and Warga, R. M., 1986, Tissue specific cell lineages originate in the gastrula of the zebrafish, Science 231:365–368.PubMedGoogle Scholar
  40. Kimmel, C. B., and Warga, R. M., 1987, Cell lineages generating axiomuscle in the zebrafish embryo. Nature (London) 327:234–237.Google Scholar
  41. Königsberg, LR., and Pfister, K. K., 1986, Replicative and differentiative behavior in daughter pairs of myogenic stem cells. Exp. Cell Res. 167:63–74.PubMedGoogle Scholar
  42. Kriegstein, A., and Dichter, M. A., 1984, Neuron generation in dissociated cell cultures from fetal rat cerebral cortex. Brain Res. 295:184–189.PubMedGoogle Scholar
  43. Large, T. H., Bodary, S. C., Clegg, D. O., Westcamp, G., Otten, U., and Reichardt, L. F., 1986, Nerve growth factor gene expression in the developing rat brain. Science 234:352–355.PubMedGoogle Scholar
  44. Lauder, J. M., 1985, Roles for neurotransmitters in development: Possible interaction with drugs during the fetal and neonatal periods. Prevention of physical and mental congenital defects, part C: Basic and Medical Science, Education, and Future Strategies, pp. 375–380, Alan R. Liss, New York.Google Scholar
  45. Lauder, J. M., and Krebs, H., 1976, Effects of /?-chlorophenolaline on time of neuronal origin during embryogenesis in the rat. Brain Res. 107:638–644.PubMedGoogle Scholar
  46. Lauder, J. M., Wallace, J. A., Krebs, H., and Petrusz, P., 1980, Serotonin as a timing mechanism in neuroembyrogenesis, in Progress in Psychoneuroendocrinology (E. Bambrillo, G. Recogni, and D. Dewead, eds.), pp. 539–556, Elsevier/North-Holland Biomedical Press, New York.Google Scholar
  47. Lauder, J. M., Paul, Y. Z., and Krebs, H., 1981, Maternal influences on tryptophan hydroxylase activity in embryonic rat brain. Dev. Neurol. 4:291–295.Google Scholar
  48. Le Douarin, N. M., 1986, Cell line segregation during peripheral nervous system ontogeny. Science 231:1515–1522.PubMedGoogle Scholar
  49. Leutz, A., and Schachner, M., 1981, Epidermal growth factor stimulates DNA synthesis of astrocytes in primary cerebellar cultures. Cell Tissue Res. 220:393–404.PubMedGoogle Scholar
  50. Levi-Montalcini, R., 1982, Developmental neurobiology and the natural history of nerve growth factor, Annu. Rev. Neurosci. 5:341–362.PubMedGoogle Scholar
  51. Lewis, P. D., Patel, A. J., Bendek, G., and Balazs, R., 1977, Effect of reserpine on cell proliferation in the developing rat brain: A quantitative histological study. Brain Res. 129:299–308.PubMedGoogle Scholar
  52. Lia, B. A., Williams, R. W., and Chalupa, L. M., 1987, Formation of retinal ganglion cell topography during pre-natal development. Science 236:848–851.PubMedGoogle Scholar
  53. Lillien, L. E., and Claude, P., 1985, Nerve growth factor is a mitogen for cultured chromaffin cells. Nature (London) 317:632–634.Google Scholar
  54. Lyser, K. M., 1968, Early differentiation of motor neuroblasts in the chick embryo as studied by electron microscopy. Dev. Biol. 17:117–142.PubMedGoogle Scholar
  55. Lyser, K. M., 1977, Differentiation of cells in organ culture, in Cell Tissue and Organ Cultures in Neurobiology (S. Fedoroff and L. Hertz, eds.), pp. 121–140, Academic Press, New York.Google Scholar
  56. Massague, J., 1987, The TGF-ß family of growth and differentiation factors, Cell 49:437–438.PubMedGoogle Scholar
  57. Mattsson, M. E. K., Engberg, G., Ruussala, A.-L, Hall, K., and Pahlman, S., 1986, Mitogenic response of human SH-SY5Y neuroblastoma cells to insulin-like growth factor I and II is dependent on the stage of differentiation, J.Cell Biol. 102:1949–1954.PubMedGoogle Scholar
  58. Mead, R., Schmidt, G. H., and Ponder, B. A. J. 1987, Calculating numbers of tissue progenitor cells using chimeric animals, Dev. Biol. 121:273–276.PubMedGoogle Scholar
  59. Model, P. G., 1978, Regulation of the Mauthner cell following unilateral rotation of the prospective hindbrain in axolotl neurulae (Ambystoma mexicanum). Brain Res. 153:135–143.PubMedGoogle Scholar
  60. Morrest, D. K., 1970, The pattern of neurogenesis in the retina of the rat, Z. Anat. Entwicklungsgesch. 131:45–67.Google Scholar
  61. Nagy, T., and Reh, T., 1987, Nervous system specific antibodies in frog, Soc. Neuro sci. Abstr. 13:385–412.Google Scholar
  62. Negishi, K., Teranishi, T., and Kato, S., 1982, New dopaminergic and indoleamine-accumulating cells in the growth zone of goldfish retinas after neurotoxic destruction. Science 216:747–749.PubMedGoogle Scholar
  63. Negishi, K., Teranishi, T., and Kato, S., 1985, Growth rate of a peripheral annulus defined by neurotoxic destruction in the goldfish retina, Dev, Brain Res, 4 1–295Google Scholar
  64. Negishi, K., Teranishi, T., Kato, S., and Nakamura, Y., 1987, Paradoxical induction of dopaminergic cells following intravitreal injection of high doses of 6-hydroxydopamine in juvenile carp retina, Dev. Brain Res. 33:67–79.Google Scholar
  65. Oppenheim, R. W., 1981, Neuronal cell death and some related regressive phenomena during neurogenesis: A selective historical review and progress report, in Studies in Developmental Neurobiology (W. M. Cowan, ed.), pp. 74–98, Oxford University Press, New York.Google Scholar
  66. Patel, A. J., 1985, Neurotrophic drugs and brain development: Effects on cell replication in vivo and in vitro. Prevention of physical and mental congenital defects, part C: Basic and Medical Science, Education, and Future Strategies, pp. 301–305, Alan R. Liss, New York.Google Scholar
  67. Patel, A. J., Vertes, Z. S., Lewis, P. D., and Lie, M., 1980, Effect of chlorpromazine on self- proliferation in the developing rat brain. A combined biochemical and morphological study. Brain Res. 202:414–428.Google Scholar
  68. Patterson, P. H., 1978, Environmental determination of autonomic neurotransmitter functions, Annu. Rev. Neurosci. 1:1–17.PubMedGoogle Scholar
  69. Perris, R., von Boxberg, Y., and Löfberg, J., 1988, Local environmental matrices determine region-specific phenotypes in neural crest cells. Science 241:86–88.PubMedGoogle Scholar
  70. Prasad, K. N., 1975, Differentiation of neuroblastoma in culture, Biol. Rev. 2:129–165.Google Scholar
  71. Prasad, K. N., and Hsie, A. W., 1971, Morphological differentiation of mouse neuroblastoma cells induced in vitro by db-cAMP, Nature (London) 233:141–142.Google Scholar
  72. Price, J., Turner, D., and Cepko, C. 1987, Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer, Proc. Natl. Acad. Sei. U.S.A. 84:156–160.Google Scholar
  73. Quinn, L. S., Holtzer, H., and Nimeroff, M., 1985, Generation of chick skeletal muscle cells in groups of 16 from stem cells, Nature (London) 313:692–694.Google Scholar
  74. Reh, T. A., 1987a, Cell-specific regulation of neuronal production in the larval frog retina, J. Neurosci. 7:3317–3324.PubMedGoogle Scholar
  75. Reh, T. A., 1987b, A role for the extracellular matrix in CNS neurogenesis, Soc. Neurosci. Abstr. 13:55.Google Scholar
  76. Reh, T. A., and Constantine-Paton, M., 1983, Qualitative and quantitative measures of plasticity during the normal development of theRana pipiens retinotectal projection, Dev. Brain Res. 10:187–200.Google Scholar
  77. Reh, T. A., Nagy, T., and Gretton, H., 1987, Retinal pigmented epithelial cells induced to transdifferentiate to neurons by laminin. Nature (London) 330:68–71.Google Scholar
  78. Reh, T. A., and Radke, K., 1988, A role for the extracellular matrix in retinal neurogenesis in vitro. Dev. Biol. 129:283–293.PubMedGoogle Scholar
  79. Reh, T. A., and Tully, T., 1986, Regulation of tyrosine hydroxylase containing amacrine cell number in larval frog retina. Dev. Biol. 114:463–469.PubMedGoogle Scholar
  80. Rohrer, H., Acheson, A. L., Thibault, J., and Thoenen, H., 1986, Developmental potential of quail dorsal root ganglion cells analyzed in vitro andin vivo. J. Neuro sci. 6:2616–2624.Google Scholar
  81. Rothstein, H., Worgul, B., and Weinsieder, A., 1981, Regulation of lens morphogenesis and cataract pathogenesis by pituitary-dependent, insulin-like mitogens, in Cellular Communication During Ocular Development (J. B. Sheffield and S. R. Hilfer eds.), pp. 111–144, Springer- Verlag, Berlin.Google Scholar
  82. Saneto, R. P., and de Villis, J., 1985, Hormonal regulation of the proliferation and differentiation of astrocytes and oligodendrocytes in primary culture, in Cell Culture in the Neurosciences (J. E. Bottenstein and G. Sato, eds.), pp. 125–159, Plenum Press, New York.Google Scholar
  83. Schubert, D., Harris, A. J., Heinemann, S., Kidokoro, Y., Partrick, J., Steinbach, J. H., 1973, Induced differentiation of a neuroblastoma, in Tissue Culture of the Nervous System (G. Sato, ed.), p. 55, Plenum Press, New York.Google Scholar
  84. Sensenbrenner, M., Booher, J., and Mandel, P., 1971, Cultivation and growth of dissociated neurones from chick embryo cerebral cortex in the presence of different substrates, Z. Zellforsch. Mirosk. Anat. 117:559–569.Google Scholar
  85. Sensenbrenner, M., Booher, J., and Mandel, P., 1973, Histochemical study of dissociated nerve cells from embryonic chick cerebral hemispheres in flask cultures, Experientia 29:699–701.PubMedGoogle Scholar
  86. Sensenbrenner, M., Labourdette, G., Delaunoy, J. P., Pettmann, B., Devilliers, G., Moonen, G., and Bock, E., 1980a, Morphological and biochemical differentiation of glial cells in primary culture, inTissue Culture in Neurobiology (E. Giacobini, A. Vernadakis, and A. Shahar, eds.), pp. 385–395, Raven Press, New York.Google Scholar
  87. Sensenbrenner, M., Wittendorp, E., Barakat, L, and Rechenmann, R. V., 1980b, Autoradiographic study of proliferating brain cells in culture. Dev. Biol 75:268–277.PubMedGoogle Scholar
  88. Sensenbrenner, M., Barakat, L, and Labourdette, G., 1982, Proliferation and maturation of neuronal cells from the central nervous system in culture, inNeurotransmitter Interaction and Compartmentation (H. F. Bradford, ed.), pp. 497–514, Plenum Press, New York.Google Scholar
  89. Simpson, D. L., Morrison, R., de Vellis, J., and Herschman, H. R., 1982, Epidermal growth factor binding and mitogenic activity on purified populations of cells from the central nervous system, J. Neurochem. Res. 8:453–462.Google Scholar
  90. Sooy, L. E., and Metzger-Freed, L., 1970, A serum macromolecule-supplemented medium for frog cell lines, Exp. Cell Res. 60:482–485.PubMedGoogle Scholar
  91. Spira, A. W., Hudy, S., and Hannah, R. S., 1984, Ectopic photoreceptor cells and cell death in the developing rat retina, Anat. Embryol. 169:293–301.PubMedGoogle Scholar
  92. Sporn, M. B., Roberts, A. B., Wakefield, L. M., and Assoian, R. K., 1986, Transforming growth factor-ß: Biological function and chemical structure, Science 233:532–534.PubMedGoogle Scholar
  93. Stelzner, D. J., and Strauss, J. A., 1986, A quantitative analysis of frog optic nerve regeneration: Is retrograde ganglion cell death or collateral axonal loss related to selective reinnervation? J. Comp. Neurol. 245:83–106.PubMedGoogle Scholar
  94. Stent, G. S., Weisblat, D. A., Blair, S. S., and Zackson, S. L., 1982, Cell lineage in the development of the leech nervous system, in Neuronal Development (N. C. Spitzer, ed.), pp. 1–25, Plenum Press, New York.Google Scholar
  95. Sternberg, P. W., 1988, Control of cell fate within equivalence groups in C. elegans, Trends Neurosci. 11:259–264.Google Scholar
  96. Stillwell, E. F., Cone, C. M., and Cone, C. D., 1973, Stimulation of DNA synthesis in CNS neurons by sustained depolarization. Nature (London) 246:110–111.Google Scholar
  97. Straznicky, C., and Gaze, R. M., 1972, The growth of the retina in Xenopus laeris: An autoradiographic study, J.Embryol. Exp. Morph. 26:67–79.Google Scholar
  98. Svoboda, K. K. H., and O’Shea, K. S. 1987, An analysis of cell shape and the neuroepithelial basal lamina during optic vesicle formation in the mouse embryo. Development 100:185–200.PubMedGoogle Scholar
  99. Tuckett, S., and Morris-Kay, G. M., 1986, The distribution of fibronectin, laminin and entactin in the neurulating rat embryo studied by indirect immuno-fluorescence, J.Embryol. Exp. Mor- phol. 94:95–112.Google Scholar
  100. Turner, D. L., and Cepko, C., 1987, A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131–136.PubMedGoogle Scholar
  101. Turner, J. E., and Delaney, R. K., 1979, Retinal ganglion cell response to axotomy and nerve growth factor antiserum in the regenerating visual system of the newt: An ultrastructural morphometric analysis. Brain Res. 177:35–47.PubMedGoogle Scholar
  102. Turner, J. E., Delaney, R. K., and Johnson, J. E., 1981, Retinal ganglion cell response to axotomy and nerve growth factor antiserum treatment in the regenerating visual system of the goldfish: An in vivo and in vitro analysis. Brain Res. 204:283–294.PubMedGoogle Scholar
  103. Turner, J. E., Schwabb, M. E., and Thoenen, H., 1982, Nerve growth factor stimulates neurite outgrowth from goldfish retinal explants: The influence of a prior lesion, Dev. Brain Res. 4:59–66.Google Scholar
  104. Vollmer, G., and Layer, P. G., 1986, An in vitro model of proliferation and differentiation of the chick retina: Coaggregates of retinal and pigment epithelial cells, J.Neuro sci. 6(7): 1885- 1896.Google Scholar
  105. Weston, J. A., 1986, Phenotypic diversification in neural crest derived cells: The time and stability of commitment during early development. Curr. Topics Dev. Biol. 20:195–210.Google Scholar
  106. Wetts, R., and Herrup, K., 1982a, Interaction of granule, Purkinje, and olivary neurons in lurcher chimeric mice. I. Qualitative studies, J. Embryol. Exp. Morphol. 68:87–98.Google Scholar
  107. Wetts, R., and Herrup, K., 1982b, Cerebellar Purkinje cells are descended from a small number of progenitors committed during early development: Quantitative analysis of lurcher chimeric mice, Brain Res. 250:358–362.PubMedGoogle Scholar
  108. Wetts, R., and Herrup, K., 1982c, Interaction of granule, Purkinje, and olivary neurons in lurcher chimeric mice. II. Granule cell death, J. Neurosci. 2:1494–1498.Google Scholar
  109. Young, R. W., 1984, Cell death during differentiation of the retina in the mouse, J. Comp. Neurol 229:362–373PubMedGoogle Scholar

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© Plenum Press, New York 1989

Authors and Affiliations

  • Thomas A. Reh
    • 1
  1. 1.Department of Medical PhysiologyUniversity of CalgaryCalgaryCanada

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