Evolution of Neocortex

  • John Allman
Part of the Cerebral Cortex book series (CECO, volume 8A)


In this chapter I shall attempt to derive the outlines of a theory of neocortical evolution from a series of observations based mainly on the anatomy and physiology of cerebral cortex in living animals. Such an exercise in evolutionary inference is by its nature a speculative enterprise. Hopefully, it will serve to guide future comparative, developmental and biophysical studies that might shed some additional light on this intriguing but inaccessible topic. To illustrate organizational features of cortex, I have drawn examples mainly from visual cortex.


Visual Cortex Receptive Field Lateral Geniculate Nucleus Apical Dendrite Homeotic Gene 
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. Akam, M., 1987, The molecular basis for metameric pattern in the Drosophila embryo, Development 101:1–22.PubMedGoogle Scholar
  2. Allman, J., 1977, Evolution of the visual system in the early primates, Prog. Psychobiol. Physiol. Psychol. 7:1–53.Google Scholar
  3. Allman, J. M., 1987, Maps in context: Some analogies between visual cortical and genetic maps, in: Matters of Intelligence (L. Vaina, ed.), Reidel, Dordrecht, pp. 369–393.CrossRefGoogle Scholar
  4. Allman, J. M., and Kaas, J. H., 1971a, A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus), Brain Res. 31:84–105.CrossRefGoogle Scholar
  5. Allman, J. M., and Kaas, J. H., 1971b, Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus), Brain Res. 35:89–106.PubMedCrossRefGoogle Scholar
  6. Allman, J., and McGuinness, E., 1988, Visual cortex in primates, in: Comparative Primate Biology, Volume 4 (H. Steklis and J. Erwin, eds.), Alan Liss, New York, pp. 279–326.Google Scholar
  7. Allman, J., Miezin, F., and McGuinness, E., 1985, Stimulus specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons, Annu. Rev. Neurosci. 8:407–430.PubMedCrossRefGoogle Scholar
  8. Allman, J., Miezin, F., and McGuinness, E., 1988, The effects of background motion on the responses of neurons in the first and second cortical visual areas, in: Signal and Sense, Neuroscience Research Program, New York, in press.Google Scholar
  9. Awgulewitsch, A., Utset, M., Hart, C., McGinnis, W., and Ruddle, F., 1986, Spatial restriction in expression of a mouse homeo box locus within the central nervous system, Nature 320:328–335.PubMedCrossRefGoogle Scholar
  10. Baker, J., Petersen, S., Newsome, W., and Allman, J., 1981, Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): A quantitative comparison of medial, dorsomedial, dorsolateral and middle temporal areas, J. Neurophysiol. 45:397–416.PubMedGoogle Scholar
  11. Bennett, A. F., and Ruben, J. A., 1979, Endothermy and activity in vertebrates, Science 206:649–654.PubMedCrossRefGoogle Scholar
  12. Bohringer, R. C., and Rowe, M. J., 1977, The organization of the sensory and motor areas of cerebral cortex in the platypus (Ornithorhynchus anatinus), J. Comp. Nenrol. 174:1–14.CrossRefGoogle Scholar
  13. Bok, S., and Taalman Kip, M., 1939, The size of the body and the size and number of nerve cells in the cerebral cortex, Acta Neerl. Morphol. 3:1–22.Google Scholar
  14. Brauer, K., and Schober, W., 1970, Catalogue of Mammalian Brains, Fischer, Jena.Google Scholar
  15. Carroll, R., 1988, Vertebrate Paleontology and Evolution, Freeman, New York.Google Scholar
  16. Creutzfeldt, O., 1978, The neocortical link: Thoughts on the generality of structure and function in the neocortex, in: Architectonics of the Cerebral Cortex (M. Brazier and H. Petsche, eds.), Raven Press, New York, pp. 367–384.Google Scholar
  17. Crile, G., and Quiring, D., 1940, A record of the body weight and certain organ and gland weights of 3690 animals, Ohio J. Sci. 40:219–259.Google Scholar
  18. Davis, C., Noble-Topham, S., Rossant, J., and Joyner, A., 1988, Expression of the homeo box-containing gene En-2 delineates a specific region of the developing mouse brain, Genes Dev. 2:361–371.PubMedCrossRefGoogle Scholar
  19. Desimone, R., Schein, S., Moran, J., and Ungerleider, L., 1985, Contour, colour, and shape analysis beyond the striate cortex, Vision Res. 25:441–452.PubMedCrossRefGoogle Scholar
  20. Diamond, I. T., Conley, M., Itoh, K., and Fitzpatrick, D., 1985, Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus, J. Comp. Neurol. 242:610.CrossRefGoogle Scholar
  21. Edelman, G. M., 1987, Neural Darwinism, Basic Books, New York.Google Scholar
  22. Eisenberg, J., 1981, The Mammalian Radiations, University of Chicago Press, Chicago.Google Scholar
  23. Elias, H., and Schwartz, D., 1969, Surface area of the cerebral cortex of mammals determined by stereological methods, Science 166:111–113.PubMedCrossRefGoogle Scholar
  24. Flechsig, P., 1904, Einige bemerkungen uber die Untersuchungsmethoden der grosshirnrinde insbesondere des menschen, Ber. Verh. Saechs. Ges. Wiss. Leipzig Math. Phys. K1. 56:5–104, 177-248.Google Scholar
  25. Frahm, H., Stephan, H., and Stephan, M., 1982, Comparison of brain structure volumes in Insectivora and primates. I. Neocortex, J. Hirnforsch. 23:375–389.PubMedGoogle Scholar
  26. Gaul, U., Seifert, E., Struhl, R., and Jackie, H., 1987, Analysis of Kruppel protein distribution during early Drosophila development reveals posttranscriptional regulation, Cell 50:639–647.PubMedCrossRefGoogle Scholar
  27. Gehring, W., 1985, The molecular basis of development, Sci. Am. 153-162.Google Scholar
  28. Gregory, W., 1935, Reduplication in evolution, Rev. Biol. 10:272–290.CrossRefGoogle Scholar
  29. Haberly, L. B., 1985, Neuronal circuitry in olfactory cortex: Anatomy and functional implications, Chem. Senses 10:219–238.CrossRefGoogle Scholar
  30. Haug, H., 1987, Brain sizes, surfaces, and neuronal sizes in the cortex cerebri: A stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant), Am. J. Anat. 180:126–142.PubMedCrossRefGoogle Scholar
  31. Heller, S. B., and Ulinski, P. S., 1987, Morphology of geniculocortical axons in turtles of the genera Pseudemys and Chrysemys, Anat. Embryol 175:505–515.PubMedCrossRefGoogle Scholar
  32. Igarashi, S., and Kamiya, T., 1972, Atlas of the Vertebrate Brain, University Park Press, Baltimore.Google Scholar
  33. Ingham, P., 1988, The molecular genetics of embryonic pattern formation in Drosophila, Nature 335:28–34.CrossRefGoogle Scholar
  34. Ingle, D., 1985, The goldfish as a retinex animal, Science 227:651–654.PubMedCrossRefGoogle Scholar
  35. Kaas, J. H., Hall, W. C., and Diamond, I. T., 1970, Cortical visual areas I and II in the hedgehog: Relation between evoked potential maps and architectonic subdivisions, J. Neurophysiol. 33:595–615.PubMedGoogle Scholar
  36. Kemali, M., and Braitenberg, V., 1969, Atlas of the Frog’s Brain, Springer, Berlin.CrossRefGoogle Scholar
  37. Kluver, H., 1942, Functional significance of the geniculostriate system, Biol. Symp. 7:253–300.Google Scholar
  38. Land, E. H., 1986, An alternative technique for the computation of the designator in the retinex theory of color vision, Proc. Natl. Acad. Sci. USA 83:3078–3080.PubMedCrossRefGoogle Scholar
  39. Laughton, A., and Scott, M., 1984, Sequence of a Drosophila segmentation gene: Protein structure homology with DNA-binding proteins, Nature 310:25–31.CrossRefGoogle Scholar
  40. Lewis, E., 1951, Pseudoallelism and gene evolution, Cold Spring Harbor Symp. Quant. Biol. 16:159–174.PubMedCrossRefGoogle Scholar
  41. Lewis, E., 1978, A gene complex controlling segmentation in Drosophila, Nature 276:565–570.PubMedCrossRefGoogle Scholar
  42. Lewis, J., 1989, Genes and segmentation, Nature 341:382–383.PubMedCrossRefGoogle Scholar
  43. Li, W. H., 1983, Evolution of duplicate genes and pseudogenes, in: Evolution of Genes and Proteins (M. Nei and R. Koehn, eds.), Sinauer, Sunderland, p. 14.Google Scholar
  44. Lund, J., Lund, R., Hendrickson, A., Bunt, A., and Fuchs, A., 1975, The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase, J. Comp. Neurol. 164:287–305.PubMedCrossRefGoogle Scholar
  45. MacArthur, R., and Wilson, E., 1967, The Theory of Island Biogeography, Princeton University Press, Princeton, N.J.Google Scholar
  46. MacDonald, P. M., and Struhl, G., 1986, A molecular gradient in early Drosophila embryos and its role in specifying the body pattern, Nature 324:537–545.PubMedCrossRefGoogle Scholar
  47. Martin, G., Boncinelli, E., Duboule, D., Gruss, P., Jackson, I., Krumlauf, R., Lonai, P., McGuinness, W., Ruddle, F., and Wolgemuth, D., 1987, Nomenclature for homeobox-containing genes, Nature 325:31–32.CrossRefGoogle Scholar
  48. Maunsell, J., and Van Essen, D., 1983, The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey, J. Neurosci. 3:2563–2586.PubMedGoogle Scholar
  49. Mazurskaya, P. Z., 1971, Study of the projection of the retina to the forebrain of the tortoise Emys orbicularis, J. Evol. Biochem. Physiol. 7:532–536. (English translation).Google Scholar
  50. Mazurskaya, P. Z., 1972, Organization of the neuronal receptive fields of the tortoise Emys orbicularis forebrain cortex, J. Evol. Biochem. Physiol. 8:550–555.Google Scholar
  51. McConnell, S. K., 1988, Development and decision-making in the mammalian cerebral cortex, Brain Res. Rev. 13:1–23.CrossRefGoogle Scholar
  52. McGinnis, W., 1985, Homeo box sequences of the antennapedia class are conserved only in higher animal genomes, Cold Spring Harbor Symp. Quant. Biol. 50:263–270.PubMedCrossRefGoogle Scholar
  53. McGinnis, W., Garber, H., Wirz, H., Kuroiwa, A., and Gehring, W., 1984, A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans, Cell 37:403–408.PubMedCrossRefGoogle Scholar
  54. Meinhardt, H., 1982, Models of Biological Pattern Formation, Academic Press, New York.Google Scholar
  55. Merzenich, M. M., Recanzone, G., Jenkins, W. M., Allard, T. T., and Nudo, R. J., 1988, Cortical representational plasticity, in: Neurobiology of Neocortex (P. Rakic and W. Singer, eds.), Wiley, New York, pp. 41–68.Google Scholar
  56. Morgane, P., Jacobs, M., and Galaburda, A., 1986, Evolutionary morphology of the dolphin brain, in: Dolphin Cognition and Behavior: A Comparative Approach (R. Schusterman, J. Thomas, and F. Wood, eds.), Erlbaum, Hillsdale, N.J., pp. 5–30.Google Scholar
  57. Muller, E., 1985, Basal metabolic rates in primates—The possible role of phylogenetic and ecological factors, Comp. Biochem. Physiol. 81A:707–711.CrossRefGoogle Scholar
  58. Odenwald, W., Taylor, C., Palmer-Hill, F., Freidrich, V., Tani, M., and Lazzarini, R., 1987, Expression of a homeo domain protein in noncontact-inhibited cultured cells and postmitotic neurons, Genes Dev. 1:482–496.PubMedCrossRefGoogle Scholar
  59. Ohno, S., 1970, Evolution by Gene Duplication, Springer, Berlin.Google Scholar
  60. Pandya, D., Seltzer, B., and Barbas, H., 1988, Input-output relations in primate cerebral cortex, in: Comparative Primate Biology: Neurosciences (H. Steklis and J. Erwin, eds.), Liss, New York, pp. 39–80.Google Scholar
  61. Pettigrew, J., 1979, Binocular visual processing of the owl’s telencephalon, Proc. R. Soc. London Ser. B 204:435–454.CrossRefGoogle Scholar
  62. Pinto-Lord, M., Evrard, P., and Caviness, V., 1982, Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: A Golgi-EM analysis, Dev. Brain Res. 4:379–393.CrossRefGoogle Scholar
  63. Polyak, S., 1932, The Main Afferent Fiber Systems of the Cerebral Cortex in Primates, University of California Press, Berkeley.Google Scholar
  64. Radinsky, L., 1967, The oldest primate endocast. Am. J. Phys. Anthropol. 27:385–388.PubMedCrossRefGoogle Scholar
  65. Rakic, P., 1988, Specification of cerebral cortical areas, Science 241:170–176.PubMedCrossRefGoogle Scholar
  66. Rakic, P., Bourgeois, J.-P., Eckenhoff, M., Zecevic, N., and Goldman-Rakic, P., 1986, Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex, Science 232:232–235.PubMedCrossRefGoogle Scholar
  67. Rockel, A., Hiornes, R., and Powell, T., 1980, The basic uniformity in structure of the neocortex, Brain 103:221–244.PubMedCrossRefGoogle Scholar
  68. Rockland, K., and Pandya, D., 1979, Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey, Brain Res. 179:3–20.PubMedCrossRefGoogle Scholar
  69. Sanides, F., 1970, Functional architecture of motor and sensory cortices in primates in light of a new concept of neocortical evolution, in: The Primate Brain (C. R. Noback and W. Montagna, eds.), Appleton-Century-Crofts, New York, pp. 137–208.Google Scholar
  70. Scott, M., 1984, Homeotic gene transcripts in the neural tissue of insects, Trends Neurosci. 7:221–223.CrossRefGoogle Scholar
  71. Scott, M., and Carroll, S., 1987, The segmentation and homeotic gene network in early drosophila development, Cell 51:689–698.PubMedCrossRefGoogle Scholar
  72. Sereno, M., and Allman, J., 1990, Cortical and visual areas in mammals, in: Neural Basis of Visual Function (A. Levinthal, ed.), MacMillan, London, in press.Google Scholar
  73. Shepherd, G. M., and Brayton, R. K., 1987, Logic operations are properties of computer-simulated interactions between excitable dendritic spines, Neuroscience 21:151–165.PubMedCrossRefGoogle Scholar
  74. Sousa, A., Gattass, R., and Oswaldo-Cruz, E., 1978, The projection of the opossum’s visual field on the cerebral cortex, J. Comp. Neurol. 177:569–588.PubMedCrossRefGoogle Scholar
  75. Stephan, H., and Andy, O. J., 1970, The allocortex in primates, in: The Primate Brain (C. R. Noback and W. Montagna, eds.), Appleton-Century-Crofts, New York, pp. 109–135.Google Scholar
  76. Tigges, J., Tigges, M., and Perachio, A., 1977, Complementary laminar terminations of afferents to area 17 originating in area 18 and the lateral geniculate nucleus in squirrel monkey, J. Comp. Neurol. 176:87–100.PubMedCrossRefGoogle Scholar
  77. Turing, A., 1952, The chemical basis of morphogenesis, Trans R. Soc. London Ser. B 237:37–72.CrossRefGoogle Scholar
  78. Tusa, R., Palmer, L., and Rosenquist, A., 1981, Multiple cortical visual areas: visual field topography in the cat, in: Multiple Visual Areas (C. Woolsey, ed.), Humana Press, Clifton, N.J., pp. 1–32.CrossRefGoogle Scholar
  79. Ulinski, P., 1983, Dorsal ventricular Ridge, Wiley, New York.Google Scholar
  80. Ulinski, P. S., 1986, Neurobiology of the therapsid-mammal transition, in: The Ecology and Biology of Mammal-like Reptiles (N. Hotton, P. MacLean, J. Roth, and E. Roth, eds.), Smithsonian Institution, Washington, D.C., pp. 149–171.Google Scholar
  81. Ulinski, P. S., 1988, Functional architecture of turtle visual cortex, in: Forebrain in Reptiles (W Schwerdtfeger and W. Smeets, eds.), Karger, Basel, pp. 151–161.Google Scholar
  82. Van Essen, D., 1979, Visual cortical areas, Annu. Rev. Neurosci. 2:227–263.PubMedCrossRefGoogle Scholar
  83. Van Essen, D., 1985, Functional organization of primate visual cortex, in: Cerebral Cortex, Volume 3 (E. Jones, ed.), Plenum Press, New York, pp. 259–329.Google Scholar
  84. Wilson, E., 1975, Sociobiology, Harvard University Press, Cambridge, Mass.Google Scholar
  85. Wilkinson, D., Bhatt, S., Cook, M., Boncinelli, E., and Krumlauf, R., 1989, Segmental expression of Hox-2 homeobox-containing genes in the developing mouse hindbrain, Nature 341:405–409.PubMedCrossRefGoogle Scholar
  86. Zeki, S., 1983, Colour coding in the cerebral cortex: The reaction of cells in monkey visual cortex to wavelength and colours, Neuroscience 9:741–765.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • John Allman
    • 1
  1. 1.Division of BiologyCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations