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The specification of neuronal identity in the mammalian cerebral cortex

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Summary

The determination of neuronal fate in the developing cerebral cortex has been studied by tracking normal cell lineages in the cortex, and by testing the commitment of young cortical neurons to their normal fates. These studies together suggest that neuronal progenitors are multipotent during development and have the potential to produce neurons destined for many or all of the cortical layers. However, the laminar identity of an individual neuron appears to be specified through environmental interactions at the time of the cell's temrinal mitotic division, prior to its migration into the cortical plate.

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References

  1. Altman, J., and Das, G. D., Autoradiographic and histological studies of postnatal neurogenesis. I. J. comp. Neurol.126 (1966) 337–390.

    Article  CAS  PubMed  Google Scholar 

  2. Angevine, J. B., Jr, and Sidman, R. L., Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature192 (1961) 766–768.

    Article  PubMed  Google Scholar 

  3. Antonini, A., and Shatz, C. J., Relationship between neurochemical phenotype and projection patterns of subplate neurons. Soc. Neurosci. Abstr.15 (1989) 1.

    Google Scholar 

  4. Austin, C., and Cepko, C., Lineage analysis of the mouse cerebral cortex using retrovirus vectors. Soc. Neurosci. Abstr.15 (1989) 599.

    Google Scholar 

  5. Bennett, G. S., and DiLullo, C., Expression of a neurofilament protein by the precursors of a subpopulation of ventricular spinal cord neurons. Devl Biol.107 (1985) 94–106.

    Article  CAS  Google Scholar 

  6. Boulder Committee. Embryonic vertebrate central nervous system: revised terminology. Anat. Rec.166 (1970) 257–262.

    Article  Google Scholar 

  7. Caviness V. S. Jr, Patterns of cell and fiber distribution in the neocortex of the reeler mutant mouse. J. comp. Neurol.170 (1976) 435–448.

    Article  PubMed  Google Scholar 

  8. Caviness, V. S. Jr, Neocortical histogenesis in normal and reeler mice: a developmental study based on [3H]thymidine autoradiography. Dev. Brain Res.4 (1982) 293–302.

    Article  Google Scholar 

  9. Caviness, V. S. Jr, and Sidman, R. L., Time of origin of corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J. comp. Neurol.148 (1973) 141–151.

    Article  PubMed  Google Scholar 

  10. Chun, J. J. M., Nakamura, M. J., and Shatz, C. J., Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons. Nature325 (1987) 617–620.

    Article  CAS  PubMed  Google Scholar 

  11. Chun, J. J. M., and Shatz, C. J., The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J. Neurosci.9 (1989) 1648–1667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chun, J. J. M., and Shatz, C. J., Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J. comp. Neurol.282 (1989) 555–569.

    Article  CAS  PubMed  Google Scholar 

  13. DeLong, G. R., Histogenesis of fetal mouse isocortex and hippocampus in reaggregating cell cultures. Devl Biol.22 (1970) 563–583.

    Article  CAS  Google Scholar 

  14. DeLong, G. R., and Sidman, R. L., Alignment defect of reaggregating cells in cultures of developing brains of reeler mutant mice. Devl Biol.22 (1970) 584–600.

    Article  Google Scholar 

  15. Dräger, U. C., Observations on the organization of the visual cortex in the reeler mouse. J. comp. Neurol.201 (1981) 555–570.

    Article  PubMed  Google Scholar 

  16. Edmonson, J. C., and Hatten, M. E., Glial-guided granule neuron migration in vitro: a high resolution time-lapse video microscopic study. J. Neurosci.7 (1987) 1928–1934.

    Article  Google Scholar 

  17. Frederiksen, K., and McKay, R. D. G., Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci.8 (1988) 1144–1151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Friauf, E., McConnell, S. K., and Shatz, C. J., Functional circuits in the subplate during fetal and early postnatal development of cat visual cortex. J. Neurosci. (1990) in press.

  19. Gilbert, C. D., and Kelly, J. P., The projections of cells in different layers of the cat's visual cortex. J. comp. Neurol.163 (1975) 81–106.

    Article  CAS  PubMed  Google Scholar 

  20. Gilbert, C. D., and Wiesel, T. N., Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature (Lond.)280 (1979) 120–125.

    Article  CAS  PubMed  Google Scholar 

  21. Greenwald, I., Cell-cell interactions that specify certain cell fates inC. elegans development. Trends Genet.5 (1989) 237–241.

    Article  CAS  PubMed  Google Scholar 

  22. His, W., Die Neuroblasten und deren Entstehung im embryonalen Marke. Abh. Math. Phys. Cl. Kgl. Sach. ges. Wiss.15 (1989) 313–372.

    Google Scholar 

  23. Holt, C. E., Bertsch, T. W., Ellis, H. M., and Harris, W. A., Cellular determination in theXenopus retina is independent of lineage and birthdate. Neuron1 (1988) 15–26.

    Article  CAS  PubMed  Google Scholar 

  24. Hubel, D. H., and Wiesel, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.)160 (1962) 106–154.

    Article  CAS  PubMed  Google Scholar 

  25. Innocenti, G. M., Growth and reshaping of axons in the establishment of visual callosal connections. Science212 (1981) 824–827.

    Article  CAS  PubMed  Google Scholar 

  26. Katz, L. C., Local circuitry of identified projection neurons in cat visual cortex brain slices. J. Neurosci.7 (1987) 1223–1249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Katz, L. C., and Wiesel, T., Postnatal development of intrinsic axonal arbors of pyramidal neurons in cat striate cortex. Soc. Neurosci. Abstr.13 (1987) 1025.

    Google Scholar 

  28. Krushel, L. A., and van der Kooy, D., Selective in vitro reassociation of early vs. late postmitotic neurons from the rat forebrain. Soc. Neurosci. Abstr.13 (1987) 1114.

    Google Scholar 

  29. Lemmon, V., and Pearlman, A. L., Does laminar position determine the receptive field properties of cortical neurons? A study of corticotectal cells in area 17 of the normal mouse and the reeler mutant. J. Neurosci.1 (1981) 83–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Levitt, P., Cooper, M. L., and Rakic, P., Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci.1 (1981) 27–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Luskin, M. B., Pearlman, A. L., and Sanes, J. R., Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron1 (1988) 635–647.

    Article  CAS  PubMed  Google Scholar 

  32. Luskin, M. B., and Shatz, C. J., Cogeneration of subplate and marginal zone cells in the cat's primary visual cortex. J. Neurosci.5 (1985) 1062–1075.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Luskin, M. B., and Shatz, C. J., Neurogenesis of the cat's primary visual cortex. J. comp. Neurol.242 (1985) 611–631.

    Article  CAS  PubMed  Google Scholar 

  34. Marin-Padilla, M., Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z. Anat. Entwickl. Gesch.134 (1971) 117–145.

    Article  CAS  Google Scholar 

  35. Martin, K. A. C., and Whitteridge, D., Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. J. Physiol. (Lond.)353 (1984) 463–504.

    Article  CAS  PubMed  Google Scholar 

  36. McConnell, S. K., Migration and differentiation of cerebral cortical neurons after transplantation into the brains of ferrets. Science229 (1985) 1268–1271.

    Article  CAS  PubMed  Google Scholar 

  37. McConnell, S. K., Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J. Neurosci.8 (1988) 945–974.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. McConnell, S. K., Development and decision-making in the mammalian cerebral cortex. Brain Res. Rev.13 (1988) 1–23.

    Article  Google Scholar 

  39. McConnell, S. K., The determination of neuronal fate in the cerebral cortex. Trends Neurosci.12 (1989) 342–349.

    Article  CAS  PubMed  Google Scholar 

  40. McConnell, S. K., Ghosh, A., and Shatz, C. J., Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science245 (1989) 978–982.

    Article  CAS  PubMed  Google Scholar 

  41. McConnell, S. K., and LeVay, S., Anatomical organization of the visual system of the mink (Mustela vison). J. comp. Neurol.250 (1986) 109–132.

    Article  CAS  PubMed  Google Scholar 

  42. O'Leary, D. D. M., and Stanfield, B. B., Occipital cortical neurons with transient pyramidal axons extend and maintain collaterals to subcortical but not intracortical targets. Brain Res.336 (1985) 326–333.

    Article  CAS  PubMed  Google Scholar 

  43. O'Leary, D. D. M., Do cortical areas emerge from a protocortex? Trends Neurosci.12 (1989) 400–406.

    Article  CAS  PubMed  Google Scholar 

  44. O'Leary, D. D. M., and Stanfield, B. B., Selective elimination of axons extended by developing cortical neurons is dependent on regional locale. J. Neurosci.9 (1989) 2230–2246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Pinto-Lord, M. C., Evrard, P., and Caviness, V. S. Jr, Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Dev. Brain. Res.4 (1982) 379–393.

    Article  Google Scholar 

  46. Price, J., and Thurlow, L., Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development104 (1988) 473–482.

    Article  CAS  PubMed  Google Scholar 

  47. Rakic, P., Mode of cell migration to the superficial layers of fetal monkey neocortex. J. comp. Neurol.145 (1972) 61–84.

    Article  CAS  PubMed  Google Scholar 

  48. Rakic, P., Neurons in the rhesus monkey visual cortex: systematic relationship between time of origin and eventual disposition. Science183 (1974) 425–427.

    Article  CAS  PubMed  Google Scholar 

  49. Rakic, P., Contact regulation of neuronal migration, in: The Cell in Contact: Adhesions and Junctions as Morphogenetic Determinants, pp. 67–91. Eds G. M. Edelman and J.-P. Thiery. Neurosciences Research Foundation, Cambridge 1985.

    Google Scholar 

  50. Rakic, P., Specification of cerebral cortical areas. Science241 (1989) 170–176.

    Article  Google Scholar 

  51. Reh, T., Environmental cues influence differentiation of rat retinal germinal neuroepithelium. Soc. Neurosci. Abstr.15 (1989) 12.

    Google Scholar 

  52. Reh, T. A., and Kljavin, I. J., Age of differentiation determines rat retinal germinal cell phenotype: induction of differentiation by dissociation. J. Neurosci.9 (1989) 4179–4189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Reh, T. A., and Tully, T., Regulation of tyrosine-hydroxylase-containing amacrine cell number in the larval frog retina. Devl Biol.114 (1986) 463–469.

    Article  CAS  Google Scholar 

  54. Schlagger, B. L., and O'Leary, D. D. M., Embryonic rat neocortex transplanted homotopically into newborn neocortex develops area appropriate features. Soc. Neurosci. Abstr.15 (1989) 1050.

    Google Scholar 

  55. Shatz, C. J., Chun, J. J. M., and Luskin, M. B., The role of the subplate in the development of the mammalian telencephalon, in: Cerebral Cortex, vol. 7, pp. 35–58. Eds A. Peters and E. G. Jones. Plenum Publishing Corp., New York 1988.

    Chapter  Google Scholar 

  56. Shoukimas, G. M., and Hinds, J. W., The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J. comp. Neurol.179 (1978) 795–830.

    Article  CAS  PubMed  Google Scholar 

  57. Sidman, R. L., Miale, I. L., and Feder, N., Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp. Neurol.1 (1959) 322–333.

    Article  CAS  PubMed  Google Scholar 

  58. Stanfield, B. B., and O'Leary, D. D. M., The transient corticospinal projection from the occipital cortex during the postnatal development of the rat. J. comp. Neurol.238 (1985) 236–248.

    Article  CAS  PubMed  Google Scholar 

  59. Stanfield, B. B., and O'Leary, D. D. M., Fetal occipital cortical neurones transplanted to the rostral cortex can extend and maintain a pyramidal tract axon. Nature298 (1985) 371–373.

    Article  Google Scholar 

  60. Stanfield, B. B., O'Leary, D. D. M., and Fricks, C., Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurons. Nature298 (1982) 371–373.

    Article  CAS  PubMed  Google Scholar 

  61. Symonds, L. L., and Rosenquist, A. C., Laminar origins of visual corticocortical connections in the cat. J. comp. Neurol.229 (1984) 39–47.

    Article  CAS  PubMed  Google Scholar 

  62. Tapscott, S. J., Bennett, G. S., and Holtzer, H., Neuronal precursor cells in the chick neural tube express neurofilament proteins. Nature (Lond.)292 (1981) 836–838.

    Article  CAS  PubMed  Google Scholar 

  63. Temple, S., Division and differentiation of isolated CNS blast cells in microculture. Nature340 (1989) 471–473.

    Article  CAS  PubMed  Google Scholar 

  64. Turner, D. L., and Cepko, C. L., Cell lineage in the rat retina: a common progenitor for neurons and glia persists late in development. Nature328 (1987) 131–136.

    Article  CAS  PubMed  Google Scholar 

  65. Valverde, F., and Facal-Valverde, M. V., Transitory population of cells in the temporal cortex of kittens. Dev. Brain Res.32 (1987) 283–288.

    Article  Google Scholar 

  66. Valverde, F., and Facal-Valverde, M. V., Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: a correlated Golgi and electron microscopic study. J. comp. Neurol.269 (1988) 168–192.

    Article  CAS  PubMed  Google Scholar 

  67. Wahle, P., and Meyer, G., Morphology and postnatal changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J. comp. Neurol.261 (1987) 165–195.

    Article  CAS  PubMed  Google Scholar 

  68. Walsh, C., and Cepko, C. L., Clonally related cortical cells show several migration patterns. Science241 (1988) 1342–1345.

    Article  CAS  PubMed  Google Scholar 

  69. Walsh, C., and Cepko, C. L., Cell lineage and cell migration in the developing cerebral cortex. Experientia46 (1990).

  70. Wetts, R., and Fraser, S. E., Multipotent precursors can give rise to all major cell types of the frog retina. Science239 (1988) 1142–1145.

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Biological Sciences, Stanford University, 94305, Stanford, California, USA

    S. K. McConnell

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McConnell, S.K. The specification of neuronal identity in the mammalian cerebral cortex. Experientia 46, 922–929 (1990). https://doi.org/10.1007/BF01939385

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