Multiple Origins of Neocortex: Contributions of the Dorsal Ventricular Ridge

  • Toru Shimizu
  • Harvey J. Karten
Part of the NATO ASI Series book series (NSSA, volume 200)


The uniqueness of mammalian neocortex may ultimately only be clarified with improved understanding of the evolutionary origins of cortical structure and cortical functions. Comparative studies of the organization of the nonmammalian and mammalian telencephalon may provide valuable clues for understanding the evolution of neocortex. In the nonmammalian telencephalon, there are neuronal populations which correspond to cell groups in the neocortex of mammals in terms of connections, single unit-responses, and functions. Some of these populations lying within the dorsal ventricular ridge, however, are organized in a non-laminar, rather than laminar fashion. These observations suggest that the emergence of basic “cortical” circuit and laminar organization are distinct evolutionary events that can be differentiated and studied independently in order to understand each of their respective contributions to the cognitive functions of the neocortex. Moreover, in contrast to an argument that many cortical visual areas are derived from a single area by gene duplication (Allman, 1977, in press), the origins of neocortex can be separable into at least the precursors of non-laminar and laminar regions, and thus multiple evolutionary origins of neocortex are proposed.


Optic Tectum Striate Cortex Middle Temporal Comparative Neurology Extrastriate Cortex 
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. Abramson, B.P., and Chalupa, L.M. (1985) The laminar distribution of cortical connections with the tecto-and cortico-recipient zones in the cat’s lateral posterior nucleus. Neuroscience, 15: 81–95.PubMedCrossRefGoogle Scholar
  2. Allman, J. (1977) Evolution of the visual system in the early primates. In J. M Sprague and A. N. Epstein (eds.), Progress in Psychobiology and Physiological Psychology, 7, (pp. 1–53). New York: Academic Press.Google Scholar
  3. Allman, J. (in press) Evolution of neocortex. In A. Peters and E.G. Jones (eds.), Cerebral cortex: Vol. 8. New York: Plenum Press.Google Scholar
  4. Allman, J., and Kaas, J.H. (1974) A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain research, 81: 199–213.PubMedCrossRefGoogle Scholar
  5. Antonini, A., Berlucchi, G., and Sprague, J.M. (1985) Cortical systems for visual pattern discrimination in the cat as analyzed with the lesion method. In C. Chagas, R. Gattass, and C. Gross (eds.), Pattern recognition mechanisms (pp. 153–164). New York: Springer-Verlag.Google Scholar
  6. Bagnoli, P. & Burkhalter, A. (1983) Organization of the afferent projections to the Wulst in the pigeon. Journal of Comparative Neurology, 214: 103–113.PubMedCrossRefGoogle Scholar
  7. Bagnoli, P., and Casini, G. (1985) Regional distribution of catecholaminergic terminals in the pigeon visual system. Brain Research, 247: 277–286.CrossRefGoogle Scholar
  8. Bagnoli, P., Francesconi, W., and Magni, F. (1982) Visual wulst-optic tectum relationships in birds: A comparison with the mammalian corticotectal system. Archives Italiennes de Biologie, 120: 212–235.PubMedGoogle Scholar
  9. Benevento, L.A., and Ebner, F.F. (1970) Pretectal, tectal, retinal and cortical projections to tha-lamic nuclei of the Virginia opossum in stereotaxic coordinates. Brain Research, 18: 171–175.PubMedCrossRefGoogle Scholar
  10. Benevento, L.A., and Rezak, M. (1976) The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): An autoradiographic study. Brain Research, 108: 1–24.PubMedCrossRefGoogle Scholar
  11. Benowitz, L.I., and Karten, HJ. (1976) Organization of the tectofugal visual pathway in the pigeon: A retrograde transport study. Journal of Comparative Neurology, 167: 503–520.PubMedCrossRefGoogle Scholar
  12. Berkley, M.A., and Sprague, J.M. (1979) Striate cortex and visual acuity functions in the cat. Journal of Comparative Neurology, 187: 679–702.PubMedCrossRefGoogle Scholar
  13. Berry, M., and Rogers, A.W. (1965) The migration of neuroblasts in the developing cerebral cortex. Journal of Anatomy, 99: 691–709.PubMedGoogle Scholar
  14. Blough, D. (1982). Pigeon perception of letters of the alphabet. Science, 218: 397–398.PubMedCrossRefGoogle Scholar
  15. Bolz, J., and Gilbert, C.D. (1986) Generation of end-inhibition in the visual cortex via inter-laminar connections. Nature, 320: 362–365.PubMedCrossRefGoogle Scholar
  16. Brecha, N., Hunt, S.P., and Karten, H.J. (1976) Relations between the optic tectum and basal ganglia in the pigeon. Society for Neuroscience Abstract, 1: 95.Google Scholar
  17. Caviness, V.S. Jr. (1977) Reeler mutant mouse: A genetic experiment in developing mammalian cortex. In W. M. Cowan & J. A. Ferrendelli, (eds.), Approaches to the cell biology of neu rons (pp. 27–46). Bethesda, Maryland: the Society for Neuroscience.Google Scholar
  18. Chalupa, L.M. (1984) Visual physiology of the mammalian superior colliculus. In H. Vanegas (ed.), Comparative neurology of the optic tectum (pp. 775–818). New York: Plenum Press.Google Scholar
  19. Denton, C.J. (1981) Topography of the hyperstriatal visual projection area in the young domestic chicken, Experimental Neurology, 74: 482–498.PubMedCrossRefGoogle Scholar
  20. Diamond, I.T. (1973) The evolution of the tectal-pulvinar system in mammals: Structural and behavioral studies of the visual system. Symposia of the Zoological Society, London, 33: 205–233.Google Scholar
  21. Diamond, I.T., and Hall, W. C. (1969) Evolution of neocortex. Science, 164: 251–262.PubMedCrossRefGoogle Scholar
  22. Dräger, U.C. (1981) Observations on the organization of the visual cortex in the reeler mouse. Journal of Comparative Neurology, 201: 555–570.PubMedCrossRefGoogle Scholar
  23. Frost, B.J. (1982) Mechanisms for discriminating objects motion from the self-induced motion in the pigeon. In. D.J. Ingle, M.A. Goodale, and R.J.W. Mansfield (eds.), Analysis of visual behavior, 177–196. Cambridge, MA: MIT Press.Google Scholar
  24. Frost, B.J., and DiFranco, D.E. (1976) Motion specific units in the pigeon optic tectum. Vision Research, 16: 1229–1234.PubMedCrossRefGoogle Scholar
  25. Glendenning, K.K., Hall, J.A., Diamond, I.T., and Hall, W.C. (1975) The pulvinar nucleus of Galago senegalensis. Journal of Comparative Neurology, 161: 419–458.PubMedCrossRefGoogle Scholar
  26. Harting, J.K., Diamond, LT., and Hall, W.C. (1973) Anterograde degeneration study of the cortical projections of the lateral geniculate and pulvinar nuclei in the tree shrew (Tupaia glis). Journal of Comparative Neurology, 150: 393–440.PubMedCrossRefGoogle Scholar
  27. Herrnstein, R.J., Lovelnad, D., and Cable, C. (1976) Natural concepts in pigeons. Journal of Experimental Psychology: Animal Behavior Processes, 2: 285–311.CrossRefGoogle Scholar
  28. Hicks, S.P., and D’Amato, C.J. (1968) Cell migrations to the isocortex in the rat. Anatomical Record, 160, 619–634.PubMedCrossRefGoogle Scholar
  29. Hodos, W. (1976) Vision and the visual system: A bird’s eye-view. In J.M. Sprague and A.M. Epstein (eds.), Progress in Psychobiology and Physiological Psychology, 6, (pp.29–62). New York: Academic Press.Google Scholar
  30. Hodos, W., and Bonbright, J.C., Jr. (1974) Intensity difference thresholds in pigeons after lesions of the tectofugal and thalamofugal visual pathway. Journal of Comparative and Physiological Psychology, 87: 1013–1031.PubMedCrossRefGoogle Scholar
  31. Hodos, W., Karten, HJ., and Bonbright, J.C. Jr. (1973) Visual intensity and pattern discrimination after lesions of the thalamofugal visual pathway in pigeons. Journal of Comparative Neurology, 148: 447–468.PubMedCrossRefGoogle Scholar
  32. Hodos, W., Macko, K.A., and Bessette, B.B. (1984) Near field acuity after visual system lesions in pigeons. II: Telencephalon. Behavioural Brain Research, 13: 15–30.PubMedCrossRefGoogle Scholar
  33. Hodos, W., Weiss, S.R.B., and Bessette, B.B. (1986) Size-threshold changes after lesions of the visual telencephalon in pigeons. Behavioural Brain Research, 21: 203–214.PubMedCrossRefGoogle Scholar
  34. Hubel, D.H., and Wiesel, T.N. (1965) Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. Journal of Neurophysiology, 28: 229–289.PubMedGoogle Scholar
  35. Jarvis, C.D. (1974) Visual discrimination and spatial localization deficits after lesions of the tectofugal pathway in pigeons. Brain, Behavior and Evolution, 9: 195–228.PubMedCrossRefGoogle Scholar
  36. Kaas, J.H., Hall, W.C., and Diamond, I.T. (1972) Visual cortex of the grey squirrel (Sciurus carolinensis): Architectonic subdivisions and connections from the visual thalamus. Journal of Comparative Neurology, 145: 273–306.PubMedCrossRefGoogle Scholar
  37. Källén, B. (1962) Embryogenesis of brain nuclei in the chick telencephalon. Ergebnisse der Anatomie und Entwicklungsgeschichte, 36: 62–82.PubMedGoogle Scholar
  38. Kanaseki, T., and Sprague, J.M. (1976) Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comaparative Neurology, 158: 319–338.CrossRefGoogle Scholar
  39. Karten, H.J. (1969) The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Annals New York Academy of Sciences, 167: 146–179.CrossRefGoogle Scholar
  40. Karten, H.J., and Hodos, W. (1970) Telencephalic projections of the nucleus rotundus in the pigeon (Columba livid). Journal of Comparative Neurology, 140: 35–52.PubMedCrossRefGoogle Scholar
  41. Karten, H.J., and Revzin, A.M. (1966) The afferent connections in the nucleus rotundus in the pigeon. Brain Research, 2: 368–377.PubMedCrossRefGoogle Scholar
  42. Karten, H.J., and Shimizu, T. (1989) The origins of neocortex: Connections and lamination as distinct events in evolution. Journal of Cognitive Neuroscience, 1: 291–301.CrossRefGoogle Scholar
  43. Karten, H.J., Hodos, W., Nauta, W.J.H., and Revzin, A.M. (1973) Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology, 150: 253–277.PubMedCrossRefGoogle Scholar
  44. Kertzman, C., and Hodos, W. (1988) Size-difference thresholds after lesions of thalamic visual nuclei in pigeons. Visual Neuroscience, 1: 83–92.PubMedCrossRefGoogle Scholar
  45. Kimberly, R.P., Holden, A.L., and Bamborough, P. (1971) Response characteristics of pigeon forebrain cells to visual stimulation. Vision Research, 11: 475–478.PubMedCrossRefGoogle Scholar
  46. Lin, C.S. (1977) Subdivisions of the inferior pulvinar in the owl monkey. Anatomical Record, 187: 637–638.Google Scholar
  47. Macko, K.A., and Hodos, W. (1984) Near field acuity after visual system lesions in pigeons. I: Thalamus. Behavioural Brain Research, 13: 1–14.PubMedCrossRefGoogle Scholar
  48. Martin, K.A.C. (1988) The lateral geniculate nucleus strikes back. Trends in Neurosciences, 11: 192–194.PubMedCrossRefGoogle Scholar
  49. Miceli, D., Gioanni, H., Repérant, J., and Peyrichoux, J. (1979) The avian visual wulst: I. An anatomical study of afferent and efferent pathways. II An electrophysiological study of the functional properties of single neurons. In A.M. Granda and J.H. Maxwell (eds.), Neural mechanisms of behavior in the pigeon (pp. 223–254). New York: Plenum press.Google Scholar
  50. Miceli, D., Repérant, J., Villalobos, J., and Dionne, L. (1987) Extratelencephalic projections of the avian Wulst. A quantitative autoradiographic study in the pigeon Columba livia. Journal für Hirnforschung, 28: 45–57.PubMedGoogle Scholar
  51. Murphy, P.C., and Silito, A.M. (1987) Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature, 392: 727–729.CrossRefGoogle Scholar
  52. Nauta, W.J.H., and Karten, H.J. (1970) A general profile of the vertebrate brain with sidelights on the ancestry of the cerebral cortex. In F. O. Schmitt (ed.), The Neurosciences: Second Study Program. New York: Rockefeller Press.Google Scholar
  53. Pasternak, T., and Hodos, W. (1977) Intensity difference thresholds after lesions of the Visual Wulst in pigeons. Journal of Comparative and Physiological Psychology, 91: 485–497.PubMedCrossRefGoogle Scholar
  54. Perisic, M., Mihailovic, J., and Cuénod, M. (1971) Electrophysiology of the contralateral and ipsilateral projections to the Wulst in pigeon (Columba livid). International Journal of Neuroscience, 2: 7–14.PubMedCrossRefGoogle Scholar
  55. Pettigrew, J.D. (1979) Binocular visual processing in the owl’s telencephalon. Proceedings of the Royal Society (London), Series B, 204: 435–454.CrossRefGoogle Scholar
  56. Pettigrew, J.D., and Konishi, M. (1976) Neurons selective to for orientation and binocular disparity in the visual Wulst of the barn owl (Tyto alba), Science, 193: 675–678.PubMedCrossRefGoogle Scholar
  57. Rakic, P. (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. Journal of Comparative Neurology, 145: 61–84.PubMedCrossRefGoogle Scholar
  58. Rakic, P. (1988) Specification of cerebral cortical areas. Science, 241: 170–176.PubMedCrossRefGoogle Scholar
  59. Reiner, A., and Karten, H.J. (1983) The laminar source of efferent projections from the avian Wulst. Brain Research, 275: 349–354.PubMedCrossRefGoogle Scholar
  60. Revzin, A.M. (1979) Functional localization in the nucleus rotundus. In A. M. Granda and J. H. Maxwell (Eds.), Neural mechanisms of behavior in the pigeon (pp. 165–175). New York: Plenum Press.Google Scholar
  61. Ritchie, T.C., and Cohen, D.H. (1979) The avian tectofugal visual pathway: Projections of its telencephalon target ectostriatal complex. Society for Neuroscience Abstract, 2:119.Google Scholar
  62. Robson, J.A., and Hall, W.C. (1977) The organization of the pulvinar nucleus in the grey squirrel (Sciurus carolinensis). I. Cytoarchitecture and connections. Journal of Comparative Neurology, 173: 355–388.PubMedCrossRefGoogle Scholar
  63. Rodman, H.R., Gross, C.G., and Albright, T.D. (1989) Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. Journal of Neuroscience, 9: 2033–2050.PubMedGoogle Scholar
  64. Smart, I.H.M. (1973) Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic fibers. Journal of Anatomy, 116: 67–91.PubMedGoogle Scholar
  65. Smart, I.H.M., and Smart, M. (1977) The location of nuclei of different labelling intensities in autoradiographs of the anterior forebrain of postnatal mice injected with [3H] thymidine on the eleventh and twelfth days post-conception. Journal of Anatomy, 123: 515–525.PubMedGoogle Scholar
  66. Smart, I.H.M., and Smart, M. (1982) Growth patterns in the lateral wall of the mouse telencephalon: I. Autoradiographic studies of the histogenesis of the isocortex and adjacent areas. Journal of Anatomy, 134: 273–298.PubMedGoogle Scholar
  67. Sprague, J.M., Hughes, H.C., and Berlucchi, G. (1981) Cortical mechanisms in pattern and form perception. In O. Pompeiano and C.A. Marsan (eds.), Brain mechanisms of perceptual awareness and purposeful behavior (pp. 107–132). New York: Raven press.Google Scholar
  68. Stensaas, L.J., and Gilson, B.C. (1972) Ependymal and subependymal cells of the caudate-pallial junction in the lateral ventricle of the neonatal rabbit. Zeitschrift für Zellforschung, 132: 297–322.CrossRefGoogle Scholar
  69. Stone, J. (1983) Parallel processing in the visual system. New York: Plenum Press.CrossRefGoogle Scholar
  70. Tsai, H.M., Garber, B.B., and Larramendi, L.M.H. (1981) 3H-thymidine autoradiographic analysis of telencephalic histogenesis in the chick embryo: I. Neuronal birthdates of telencephalic compartments in situ. Journal of Comparative Neurology, 198: 275–292.PubMedCrossRefGoogle Scholar
  71. Ulinski, P.S. (1983). Dorsal ventricular ridge, New York: John Wiley & Sons.Google Scholar
  72. Vaughan, W., Jr and Greene, S.L. (1984) Pigeon visual memory capacity. Journal of Experi mental Psychology: Animal Behavior Processes, 10: 256–271.CrossRefGoogle Scholar
  73. Weiskrantz, L. (1986) Blindsight: a case study and implications. New York: Oxford University Press.Google Scholar
  74. Wilson, P. (1980) The organization of the visual hyperstriatum in the domestic chick. I. Topology and topography of the avian projection. Brain Research, 188: 319–332.PubMedCrossRefGoogle Scholar
  75. Yamada, H., and Sano, Y. (1985) Immunohistochemical studies on the serotonin neuron system in the brain of the chicken (Gallus domesticus). II. The distribution of the nerve fibers. Bio-genic Amines, 2: 21–36.Google Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Toru Shimizu
    • 1
  • Harvey J. Karten
    • 1
  1. 1.Department of Neurosciences, M-008University of California, San DiegoLa JollaUSA

Personalised recommendations