Control of Cell Number and Type in the Developing and Evolving Neocortex

  • Barbara L. Finlay
Part of the NATO ASI Series book series (NSSA, volume 200)


Large mammalian brains show “encephalization”: that is, in larger brains, the neocortex claims a disproportionately high percentage of their volume (Jerison, 1973; Jerison, this volume). The magnitude of encephalization is impressive, and its manner is strikingly regular across multiple mammalian radiations (Hofman, 1989). I would like to take advantage of this forum to speculate on the relationship of encephalization to current research on the ontogenetic regulation of neuron number and type in the cortex. The discussion is organized around three questions:
  1. 1.

    Can any persistent feature of development account for the disproportionately large volume of the cortex in large brains?

  2. 2.

    Why do developmental stabilizing mechanisms permit cortical hypertrophy? For example, in the spinal cord there is some trophic relationship between the number of neurons and peripheral muscle and sensory mass, regulated by normally-occurring cell death (Hamburger and Levi-Montalcini, 1949; reviewed in Hamburger and Oppenheim 1982; Oppenheim, 1981). Why is relative cortical volume allowed to grow so large with respect to the volume of its input and terminal zones?

  3. 3.

    Can development give us any clue as to how local areas of cortex get wired for their particular functions? Two views of the brain have competed for decades, whether the brain is best understood as a generalized computing device, or as an accretion of specialized capacities. While some of the functional change in larger brains might be described as faster, more powerful, and more general computing, the most prominent functional changes are the addition of particular, specialized skills. These skills, like echolocation, language, predictive prey tracking and the like, are apparently represented in a modular way in the brain. How can a generalized and regular neocortical hypertrophy be reconciled with the development of modularly-organized special functions?



Brain Size Golden Hamster Tree Shrew Large Brain Gestational Length 
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  1. Angevine, J.B. Jr., and Sidman, R.L. (1962) Autoradiographic study of histogenesis in the cerebral cortex of the mouse. Anat. Rec, 142: 210.Google Scholar
  2. Beaulieu, C., and Collonier, M. (1983) The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat. J. Comp. Neurol., 217: 337–344.PubMedCrossRefGoogle Scholar
  3. Blakemore, C., and Cummings, R.M. (1975) Eye opening in kittens. Vision Res., 15: 1417–1418.PubMedCrossRefGoogle Scholar
  4. Bruckner, G., Mares, V., and Biesold, D. (1976) Neurogenesis in the visual system of the rat: an autoradiographic investigation. J. Comp. Neurol., 166: 245–276.PubMedCrossRefGoogle Scholar
  5. Carlson, M., O’Leary, D.D.M., and Burton, H. (1987) Potential role of thalamocortical connections in recovery of tactile function following somatic sensory cortex lesions in infant primates. Soc. Neurosci. Abs. 13: 75.Google Scholar
  6. Cooper, M.L., and Rakic, P. (1981) Neurogenetic gradients in the superior and inferior colliculi of the rhesus monkey. J. Comp. Neurol., 202: 309–334.PubMedCrossRefGoogle Scholar
  7. 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, pp.19–41. Ed. M. Rockstein. New York: Academic Press.CrossRefGoogle Scholar
  8. Crandall, J.E., and Caviness, V.S. (1984) Thalamocortical connections in newborn mice. J. Comp. Neurol., 228: 542–556.PubMedCrossRefGoogle Scholar
  9. Crossland, W.J., and Uchwat, C.J. (1982) Neurogenesis in the central visual pathways of the golden hamster. Devel. Brain Res., 5: 99–103.CrossRefGoogle Scholar
  10. Dreher, B., and Robinson, S.R. (1988) Development of the retinofugal pathway in birds and mammals: evidence for a common timetable. Brain Beh. Evol., 31: 369–390.CrossRefGoogle Scholar
  11. Ebbeson, S.O.E. (1980) The parcellation theory and its relationship to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell Tissue Res., 213: 179–212.Google Scholar
  12. Eisenberg, J.F. (1981) The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation and Behavior. Chicago: The University of Chicago Press.Google Scholar
  13. Elhanany, E., and White, E.L. (1990) Intrinsic circuitry: synapses involving local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J. Comp. Neurol., 291, 43–54.PubMedCrossRefGoogle Scholar
  14. Finlay, B.L., and Pallas, S.L. (1989) Control of cell number in the developing visual system. Progress in Neurobiol., 32: 207–234.CrossRefGoogle Scholar
  15. Finlay, B.L., Sengelaub, D.R., and Berian, C.A. (1986) Control of cell number in the developing visual system. I. Effects of monocular enucleation. Dev. Brain Res., 28: 1–10.CrossRefGoogle Scholar
  16. Finlay, B.L., and Slattery, M. (1983) Local differences in amount of early cell death in neo-cortex predict adult local specializations. Science, 219: 1349–1351.PubMedCrossRefGoogle Scholar
  17. Frost, D.O. (1984) Axonal growth and target selection during development: retinal projections to the ventrobasal complex and other “nonvisual” structures in neonatal Syrian hamsters. J. Comp. Neurol., 230: 576–592.PubMedCrossRefGoogle Scholar
  18. Hamburger, V., and Levi-Montalcini, R. (1949) Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J. Exp. Zool., 111: 457–502.PubMedCrossRefGoogle Scholar
  19. Hamburger, V., and Oppenheim, R.W. (1982) Naturally occurring neuronal death in vertebrates. Neuroscience Commentaries, 1: 39–55.Google Scholar
  20. Hendrickson, A., and Rakic, P. (1977) Histogenesis and synaptogenesis in the dorsal lateral geniculate nucleus (LGd) of the fetal monkey brain. Anat. Rec, 187: 602.Google Scholar
  21. Heumann, D., and Leuba, G. (1983) Neuronal death in the development and aging of the cerebral cortex of the mouse. Neuropath. & Applied Neurobio., 9: 297–311.CrossRefGoogle Scholar
  22. Hickey, T.L., and Hitchcock, P.F. (1984) Genesis of neurons in the dorsal lateral geniculate nucleus of the cat. J. Comp. Neurol., 228: 186–199.PubMedCrossRefGoogle Scholar
  23. Hofman, M.A. (1989) On the evolution and geometry of the brain in mammals. Progress in Neurobiol., 32: 137–158.CrossRefGoogle Scholar
  24. Howard, B., Miller, B., and Finlay, B.L. (1989) Reorganization of visual callosal projections after early thalamic lesions in the golden hamster. Soc. Neurosci. Abst., 15: 1339.Google Scholar
  25. Hubel, D.H., Wiesel, T.S., and LeVay, S. (1977) Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. R. Soc. Lond., 278: 377–409.CrossRefGoogle Scholar
  26. Innocenti, G.M. (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science, 212: 824–827.PubMedCrossRefGoogle Scholar
  27. Innocenti, G.M., and Caminiti, R. (1980) Postnatal shaping of callosal connections from sensory areas. Exp. Brain Res., 38: 381–394.PubMedCrossRefGoogle Scholar
  28. Ivy, G.O., and Killackey, H. P. (1982) Ontogenetic changes in the projections of neocortical neurons. J. Neurosci., 2: 735–743.PubMedGoogle Scholar
  29. Jenson, H.J. (1973) Evolution of the Brain and Intelligence. New York: Academic Press.Google Scholar
  30. Kane, M.H., Sengelaub, D.R., and Finlay, B.L. (1984) An autoradiographic analysis of the role of cell death in regulation of neocortical cell number. Soc. Neurosci. Abs., 10: 462.Google Scholar
  31. Lamantia, A.-S., and Rakic, P. (1990) Cytological and quantitative characteristics of four cerebral commissures in the rehsus monkey. J. Comp. Neurol., 291: 520–537.PubMedCrossRefGoogle Scholar
  32. Luskin, M.B., and Shatz, C.J. (1985a) Studies of the earliest generated cells of the cat’s visual cortex: cogeneration of subplate and marginal zones. J. Neurosci., 5: 1062–1075.PubMedGoogle Scholar
  33. Luskin, M.B., and Shatz, C.J. (1985b) Neurogenesis in the cat’s primary visual cortex. J. Comp. Neurol., 242: 611–631.PubMedCrossRefGoogle Scholar
  34. Miller, B., Windrem, M.S., Anllo-Vento, L., and Finlay, B.L. (1987) Minor reorganization of thalamocortical projections following large neonatal thalamic lesions in the golden hamster. Soc. Neurosci. Abs., 13: 1419.Google Scholar
  35. Mustari, M.J., Lund, R.D., and Graubard, K. (1979) Histogenesis of the superior colliculus of the albino rat: a tritiate thymidine study. Brain Res., 164: 39–52.PubMedCrossRefGoogle Scholar
  36. Naegele, J.R., Jhaveri, S., and Schneider, G.E. (1988) Sharpening of topographical projections and maturation of geniculocortical axon arbors in the hamster. J. Comp. Neurol., 281: 1–12.Google Scholar
  37. O’Kusky, J., and Colonnier, M. (1982) A laminar analysis of the number of neurons, glia and synapses in the visual cortex (area 17) of adult macaque monkeys. J. Comp. Neurol., 210: 278–290.PubMedCrossRefGoogle Scholar
  38. O’Leary, D.D.M. (1989) Do cortical areas emerge from a protocortex? Trends in Neurosi., 12: 400–406.CrossRefGoogle Scholar
  39. Oppenheim, R.W. (1981) Neuronal death and some related regressive phenomena during neurogenesis: a selective historical review and progress report. In Studies in Developmental Neurobiology, pp. 74–133. Ed. W.M. Cowan. New York: Oxford University Press.Google Scholar
  40. Pagel, M.D., and Harvey, P.H. (1990) Diversity in the brain sizes of newborn mammals. Bio Science, 40: 116–122.Google Scholar
  41. Pallas, S.L., Gilmour, S., and Finlay, B.L. (1988) Control of cell number in the developing neocortex: I. Effects of early tectal ablation. Devel. Brain Res., 43: 1–11.CrossRefGoogle Scholar
  42. Purves, D. (1988) Body and Brain: A Trophic Theory of Neural Connections. Harvard University Press: Cambridge, Ma.Google Scholar
  43. Rakic, P. (1974) Neurons in the rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science, 183: 425–427.PubMedCrossRefGoogle Scholar
  44. Rakic, P. (1988) Specification of cerebral cortical areas. Science, 241: 170–176.PubMedCrossRefGoogle Scholar
  45. Ramirez, L.F., and Kalil, K. (1985) Critical stages for growth in the development of cortical neurons. J. Comp. Neurol., 237: 506–518.PubMedCrossRefGoogle Scholar
  46. Rodier, P.M. (1980) Chronology of neuron development: animal studies and their clinical implications. Develop. Med., and Child Neurol., 22: 525–545.CrossRefGoogle Scholar
  47. Sefton, A.J., MacKay-Sim, A., Baur, L.A., and Cottee, L.J. (1981) Cortical projections to visual centers in the rat: an HRP study. Brain Res., 215: 1–11.PubMedCrossRefGoogle Scholar
  48. Sengelaub, D.R., Dolan, R.P., and Finlay, B.L. (1988) Cell generation, death and retinal growth in the development of the hamster retinal ganglion cell layer: J. Comp. Neurol., 204: 311–317.CrossRefGoogle Scholar
  49. Shatz, C.J., and Luskin, M.B. (1986) The relationship between the geniculocortical aferents and their cortical target cells during the development of the cat’s primary visual cortex. J. Neurosci., 6: 3655–3668.PubMedGoogle Scholar
  50. Shimada, M., and Langman, J. (1970) Cell proliferation, migration and differentaiton on the cerebral cortex of the golden hamster. J. Comp. Neurol., 139: 227–244.PubMedCrossRefGoogle Scholar
  51. Sidman, R.L. (1961) Histogenesis of the mouse retina studies with thymidine 3-H. In: The Structure of the Eye, G.K. Smelser, ed. Academic Press, New York: 487–506.Google Scholar
  52. Sperry, D.G. (1990) Variation and symmetry in the lumbar and thoracic dorsal root ganglion cell populations of newly metamorphosed Xenopus laevis. J. Comp. Neurol., 292: 54–64.PubMedCrossRefGoogle Scholar
  53. Stanfield, B.B., O’Leary, D.D.M., and Fricks, C. (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature, (Lond.) 298: 371–373.CrossRefGoogle Scholar
  54. von Economo, C.F. (1929) The Cytoarchitecture of the Human Cerebral Cortex. Oxford University Press: LondonGoogle Scholar
  55. 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, (Lond) P302: 611–614.CrossRefGoogle Scholar
  56. Wilder, K.C., Kirn, J., Windrem, M.S., and Finlay, B.L. (1986) Control of cell number in the developing visual system: III. Partial tectal ablation. Devel. Brain Res., 28: 23–32.CrossRefGoogle Scholar
  57. Williams, R.W., and Herrup, K. (1988) The control of neurons number. Ann. Rev. Neurosci., 11: 423–454.PubMedCrossRefGoogle Scholar
  58. Windrem, M.S., and Finlay, B.L. (1985) Early thalamic lesions increase neonatal cell death and alter adult cytoarchitecture in the neocortex. Soc. Neurosci. Abstr., 1: 991.Google Scholar
  59. Windrem, M.S., Jan de Beur, S.M., and Finlay, B.L. (1986) Effects of early callosal and thalamic lesions on differentiation of cortical cytoarchitecture. Soc. Neurosci. Abst., 12: 867.Google Scholar
  60. Windrem, M.S., Jan de Beur, S., and Finlay, B.L. (1988) Control of cell number in the developing neocortex: II. Effects of corpus callosum transection. Devel. Brain Res., 43: 13–22.CrossRefGoogle Scholar
  61. Zamenhof, S., and Van Marthens, E. (1979) Brain weight, brain chemical contents and their early manipulation. In: Hahn, M.E., Jensen, C., and Dudek, B.C. eds. Development and Evolution of Brain Size: Behavioral Implications. New York: Academic Press.Google Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Barbara L. Finlay
    • 1
  1. 1.Department of Psychology, Uris HallCornell UniversityIthacaUSA

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