Journal of Neurocytology

, Volume 31, Issue 3–5, pp 289–298

Scaling laws in the mammalian neocortex: Does form provide clues to function?

  • Kimberly H. Harrison
  • Patrick R. Hof
  • Samuel S.-H. Wang
Article

Abstract

Although descriptions of form have been a mainstay of comparative neuroanatomy, less well explored is the use of quantitative approaches, especially at the cellular level. In the neocortex, many gross and cellular anatomical measures show striking regularities over a wide range of brain sizes. Here we review our recent efforts to accurately characterize these scaling trends and explain them in functional terms. We focus on the expansion of white matter volume with increasing brain size and the formation of surface folds, in addition to principles of processing speed and energetics that may explain these phenomena. We also consider exceptional cases of neocortical morphology as a means of testing putative functional principles and developmental mechanisms. We illustrate this point by describing several morphological specializations at the cellular level that may constitute functional adaptations. Taken together, these approaches illustrate the benefits of a synthesis between comparative neuroanatomy and biophysics.

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References

  1. Aiello, L. C. &; Wheeler, P. (1995) The expensive-tissue hypothesis: The brain and digestive system in primate evolution. Current Anthropology 36, 199–221.Google Scholar
  2. Allen, C. &; Stevens, C. F. (1994) An evaluation of causes for unreliability of synaptic transmission. Proceedings of the National Academy of Sciences USA 91, 10380–10383.Google Scholar
  3. Allman, J. &; Hasenstaub, A. (1999) Brains, maturation times, and parenting. Neurobiology of Aging 20, 447–454.PubMedGoogle Scholar
  4. Allman, J. M. (1999) Evolving Brains. New York: W.H. Freeman.Google Scholar
  5. Beaulieu, C. &; Colonnier, M. (1985) A laminar analysis of the number of round-asymmetrical and flatsymmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. Journal of Comparative Neurololy 231, 180–189.Google Scholar
  6. Beaulieu, C. &; Colonnier, M. (1989) Number and size of neurons and synapses in the motor cortex of cats raised in different environmental complexities. Journal of Comparative Neurology 289, 178–181.PubMedGoogle Scholar
  7. Braitenberg, V. (1998) Selection, the impersonal engineer. Artificial Life 4, 309–310.PubMedGoogle Scholar
  8. Braitenberg, V. &; SchÜz, A. (1998) Cortex: Statistics and Geometry of Neuronal Connectivity. 2nd ed. Berlin: Springer-Verlag.Google Scholar
  9. Bray, D. (1979) Mechanical tension produced by nerve-cells in tissue-culture. Journal of Cell Science 37, 391–410.PubMedGoogle Scholar
  10. Brodmann, K. (1905) Beitrage zur histologischen Lokalisation der Grosshirnrinde: Die Rindenfeldern der niederen Affen. Journal of Psychology and Neurology 4, 177–226.Google Scholar
  11. Changizi, M. A. (2001) Principles underlying mammalian neocortical scaling. Biological Cybernetics 84, 207–215.PubMedGoogle Scholar
  12. Changizi, M. A. (2003) The Brain from 25,000 Feet: High Level Explorations of Brain Complexity, Perception, Induction and Vagueness. Dordrecht: Kluwer Academic.Google Scholar
  13. Chan-Palay, V., Palay, S. L. &; Billingsgagliardi, S. M. (1974) Meynert cells in the primate visual cortex. Journal of Neurocytology 3, 631–658.PubMedGoogle Scholar
  14. Chenn, A. &; Walsh, C. A. (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369.PubMedGoogle Scholar
  15. Cherniak, C. (1994) Component placement optimization in the brain. Journal of Neuroscience 14, 2418–2427.PubMedGoogle Scholar
  16. Chklovskii, D. B. &; Stevens, C. F. (2000) Wiring optimization in the brain. Advances in Neural Information Processing Systems 12, 103–107.Google Scholar
  17. Clark, D. A., Mitra, P. P. &; Wang, S. S.-H. (2001) Scalable architecture in mammalian brains. Nature 411, 189–193.PubMedGoogle Scholar
  18. Cowan, W. M., SÜdhof, T. C. &; Stevens, C. F. (2001) Synapses. Baltimore: Johns Hopkins University Press.Google Scholar
  19. Cragg, B. G. (1967) The density of synapses and neurones in the motor and visual areas of the cerebral cortex. Journal of Anatomy 101, 639–654.PubMedGoogle Scholar
  20. deFelipe, J., Alonso-Nanclares, L. &; Arellano, J. I. (2002) Microstructure of the neocortex: Comparative aspects. Journal of Neurocytology 31(3-5), 299–316.PubMedGoogle Scholar
  21. Elston, G. N., Benavides-Piccione, R. &; deFelipe, J. (2001) The pyramidal cell in cognition: A comparative study in human and monkey. Journal of Neuroscience 21, RC163.Google Scholar
  22. Feng, Y. &; Walsh, C. A. (2001) Protein-protein interactions, cytoskeletal regulation and neuronal migration. Nature Reviews in Neuroscience 2, 408–416.Google Scholar
  23. Feynman, R. P. (1996) Feynman Lectures on Computation. Reading, MA: Perseus Books.Google Scholar
  24. Finlay, B. L., Darlington, R. B. &; Nicastro, N. (2001) Developmental structure in brain evolution. Behavior and Brain Sciences 24, 263–278.Google Scholar
  25. Frahm, H. D., Stephan, H. &; Stephan, M. (1982) Comparison of brain structure volumes in insectivora and primates. I. Neocortex. Journal für Hirnforschung 23, 375–389.Google Scholar
  26. Fries, W., Keizer, K. &; Kuypers, H. G. (1985) Large layer VI cells in macaque striate cortex (Meynert cells) project to both superior colliculus and prestriate visual area V5. Experimental Brain Research 58, 613–616.Google Scholar
  27. Goldman-Rakic, P. S. &; Rakic, P. (1984) Experimental modification of gyral patterns. In Cerebral Dominance: The Biological Foundation (edited by Geschwind, N. &; Galaburda, A. M.) pp. 179–192. Cambridge, MA: Harvard University Press.Google Scholar
  28. Heffner, R. S. &; Masterton, R. B. (1983) The role of the corticospinal tract in the evolution of human digital dexterity. Brain, Behavior and Evolution 23, 165–183.Google Scholar
  29. Hillis, W. (1986) The Connection Machine. Cambridge, MA: MIT Press.Google Scholar
  30. Hof, P. R., Glezer, I., Conde, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A. &; Vogt Weisenhorn, D. M. (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. Journal of Chemical Neuroanatomy 16, 77–116.PubMedGoogle Scholar
  31. Hof, P. R., Glezer, I., Nimchinsky, E. A. &; Erwin, J. M. (2000a) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: Evidence from primates, cetaceans, and artiodactyls. Brain, Behavior and Evolution 55, 300–310.Google Scholar
  32. Hof, P. R. &; Morrison, J. H. (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. Journal of Comparative Neurology 352, 161–186.PubMedGoogle Scholar
  33. Hof, P. R., Nimchinsky, E. A., Young, W. G. &; Morrison, J. H. (2000b) Numbers of Meynert and layer IVb cells in area V1:Astereologic analysis in young and aged macaque monkeys. Journal of Comparative Neurology 420, 113–126.PubMedGoogle Scholar
  34. Hofman, M. A. (1985) Size and shape of the cerebral cortex in mammals. I. The cortical surface. Brain, Behavior and Evolution 27, 28–40.Google Scholar
  35. Hofman, M. A. (1988) Size and shape of the cerebral cortex in mammals. II. The cortical volume. Brain, Behavior and Evolution 32, 17–26.Google Scholar
  36. Hofman, M. A. (1989) On the evolution and geometry of the brain in mammals. Progress in Neurobiology 32, 137–158.PubMedGoogle Scholar
  37. Hofman, M. A. (1991) The fractal geometry of convoluted brains. Journal für Hirnforschung 32, 103–111.Google Scholar
  38. Huxley, J. (1932) Problems of Relative Growth. London: Methuen.Google Scholar
  39. Jack, J. J. B., Noble, D. &; Tsien, R. W. (1975) Electric Current Flow in Excitable Cells. Oxford: Clarendon Press.Google Scholar
  40. Jerison, H. (1987) Brain size. In Encyclopedia of Neuroscience (edited by Adelman, G.) pp. 168–170. Boston: Birkhaeuser.Google Scholar
  41. Jerison, H. J. (1991) Brain Size and the Evolution of Mind. New York: American Museum of Natural History.Google Scholar
  42. Johnson, J. I., Kirsch, J. A. W., Reep, R. L. &; Switzer III, R. C. (1994) Phylogeny through brain traits: More characters for the analysis of mammalian evolution. Brain, Behavior and Evolution 43, 319–347.Google Scholar
  43. Johnston, D. &; Wu, S. M.-S. (1995) Foundations of Cellular Neurophysiology. Cambridge, MA: MIT Press.Google Scholar
  44. Kaas, J. H. (2000) Why is brain size so important: Design problems and solutions as neocortex gets bigger or smaller. Brain and Mind 1, 7–23.Google Scholar
  45. Kamiya, Y. &; Yamasaki, F. (1974) Organ weights in Pontoporia Blainvillei and Platanista Gangetica. Sci. Rep. Whales Res. Inst. 26, 265–270.Google Scholar
  46. Krubitzer, L. (1995) The organization of neocortex in mammals: Are species differences really so different? Trends in Neuroscience 18, 408–417.Google Scholar
  47. Kuida, K., Haydar, T. F., Kuan, C.-Y., Gu, Y., Taya, C., Karasuyama, H., Su, M. S., Rakic, P. &; Flavell, R. A. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325–337.PubMedGoogle Scholar
  48. Lamantia, A.-S. &; Rakic, P. (1990) Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. Journal of Comparative Neurology 291, 520–537.PubMedGoogle Scholar
  49. Lammens, M. (2000) Neuronal migration disorders in man. European Journal of Morphology 38, 327–333.PubMedGoogle Scholar
  50. Le Gros Clark, W. E. (1942) The cells of Meynert in the visual cortex of the monkey. Journal of Anatomy 74, 369–376.Google Scholar
  51. Le Gros Clark, W. E. (1959) The Antecedents of Man. Edinburgh: Edinburgh University Press.Google Scholar
  52. Marret, S., Mukendi, R., Gadisseux, J. F., Gressens, P. &; Evrard, P. (1995) Effect of ibotenate on brain development: An excitotoxic mouse model of microgyria and posthypoxic-like lesions. Journal of Neuropathology and Experimental Neurology 54, 358–370.PubMedGoogle Scholar
  53. Martin, R. D. (1990) Primate Origins and Evolution. Princeton: Princeton University Press.Google Scholar
  54. Mead, C. &; Conway, L. (1980) Introduction to VLSI Systems. Reading, MA: Addison-Wesley.Google Scholar
  55. Mountcastle, V. (1998) Perceptual Neuroscience: The Cerebral Cortex. Cambridge, MA: Harvard University Press.Google Scholar
  56. Nauta, W. J. H. &; Feirtag, M. (1986) Fundamental Neuroanatomy. New York: Freeman.Google Scholar
  57. Niewenhuys, R., Ten Donkelaar, H. &; Nicholson, C. (1998) The Central Nervous System of Vertebrates. Berlin: Springer.Google Scholar
  58. Nimchinsky, E. A., Gilissen, E., Allman, J. M., Perl, D. P., Erwin, J. M. &; Hof, P. R. (1999) A neuronal morphologic type unique to humans and great apes. Proceedings of the National Academy of Sciences USA 96, 5268–5273.Google Scholar
  59. Nimchinsky, E. A., Vogt, B. A., Morrison, J. H. &; Hof, P. R. (1995) Spindle neurons of the human anterior cingulate cortex. Journal of Comparative Neurology 355, 27–37.PubMedGoogle Scholar
  60. O'Kusky, J. &; Colonnier, M. (1982)Alaminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. Journal of Comparative Neurology 210, 278–290.PubMedGoogle Scholar
  61. Peters, A. &; Palay, S. L. (1991) The Fine Structure of the Nervous System: Neurons and Their Supporting Cells. 3rd edn. New York: Oxford University Press.Google Scholar
  62. Rakic, P. (1988) Defects of neuronal migration and the pathogenesis of cortical malformations. Progress in Brain Research 73, 15–37.PubMedGoogle Scholar
  63. Rakic, P. (1995) A small step for the cell, a giant leap for mankind: A hypothesis of neocortical expansion during evolution. Trends in Neuroscience 18, 383–388.Google Scholar
  64. Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N. &; Goldman-Rakic, P. (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232, 232–235.PubMedGoogle Scholar
  65. RamÓn Y Cajal, S. (1990) New Ideas on the Structure of the Nervous System in Man and Vertebrates. Cambridge, MA: MIT Press.Google Scholar
  66. Reep, R. L. &; O'Shea, T. J. (1990) Regional brain morphometry and lissencephaly in the Sirenia. Brain, Behavior and Evolution 35, 185–194.Google Scholar
  67. Rice, D. W. (1967) Cetaceans. In Recent Mammals of the World-A Synopsis of Families (edited by Anderson, S. &; Jones, J. K.) pp. 291–324. New York: Ronald Press.Google Scholar
  68. Ritchie, J. M. (1995) Physiology of axons. In The Axon: Structure, Function and Pathophysiology (edited by Waxman, S. G., Kocsis, J. D. &; Stys, P. K.) pp. 68–96. New York: Oxford University Press.Google Scholar
  69. Rivara, C.-B., Sherwood, C. C., Bouras, C. &; Hof, P. R. (2003) Stereologic characterization and spatial distribution patterns of Betz cells in human primary motor cortex. Anatomical Record 270A, 137–151.Google Scholar
  70. Sabatini, B. L. &; Regehr, W. G. (1999) Timing of synaptic transmission. Annual Review of Physiology 61, 521–542.PubMedGoogle Scholar
  71. Scheibel, M. E. &; Scheibel, A. B. (1978) The dendritic structure of the human Betz cell. In Architectonics of the Cerebral Cortex (edited by Brazier, M. A. B. &; Pets, H.) pp. 43–57. New York: Raven Press.Google Scholar
  72. SchÜz, A. &; Demianenko, G. P. (1995) Constancy and variability in cortical structure. A study on synapses and dendritic spines in hedgehog and monkey. Journal für Hirnforschung 36, 113–122.Google Scholar
  73. SchÜz, A. &; Palm, G. (1989) Density of neurons and synapses in the cerebral cortex of the mouse. Journal of Comparative Neurology 286, 442–455.PubMedGoogle Scholar
  74. SchÜz, A. &; Preissl, H. (1996) Basic connectivity of the cerebral cortex and some considerations on the corpus callosum. Neuroscience and Biobehavioral Reviews 20, 567–570.PubMedGoogle Scholar
  75. Schwartzkroin, P. A. &; Walsh, C. A. (2000) Cortical malformations and epilepsy. Mental Retardation and Developmental Disabilities Research Reviews 6, 268–280.PubMedGoogle Scholar
  76. Shepherd, G. M. (1990) The Synaptic Organization of the Brain. 3rd ed. New York: Oxford University Press.Google Scholar
  77. Sherwood, C. C., Lee, P. W. H., Rivara, C.-B., Holloway, R. L., Gilissen, E. P. E., Simmons, R. M. T., Hakeem, A., Allman, J. M., Erwin, J. M. &; Hof, P. R. (2003) Evolution of specialized pyramidal neurons in the primate motor and visual cortex. Brain, Behavior and Evolution 61, 28–44.Google Scholar
  78. Shultz, J. R. &; Wang, S. S.-H. (2001) How the neocortex got its folds: Ultrastructural parameters underlying macroscopic features. Society for Neuroscience Abstracts.Google Scholar
  79. Smith, D. S., Niethammer, M., Ayala, R., Zhou, Y., Gambello, M. J., Wynshaw-Boris, A. &; Tsai, L. H. (2000) Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian LIS1. Nature Cell Biology 2, 767–775.PubMedGoogle Scholar
  80. Stephan, H., Frahm, H. &; Baron, G. (1981)Newand revised data on volumes of brain structures in insectivores and primates. Folia Primatologica 35, 1–29.Google Scholar
  81. Swadlow, H. A. (2000) Information flow along neocortical axons. In Time and the Brain. Conceptual Advances in Brain Research (edited by Miller, R.) pp. 131–155. Amsterdam: Harwood Academic Publishers.Google Scholar
  82. Swadlow, H. A. &; Waxman, S. G. (1976) Variations in conduction velocity and excitability following single and multiple impulses of visual callosal axons in the rabbit. Experimental Neurology 53, 128–150.PubMedGoogle Scholar
  83. Thompson, D. W. (1942) On Growth and Form. Cambridge: The University Press.Google Scholar
  84. Tower, D. B. (1954) Structural and functional organization ofmammaliancerebral cortex: The correlation of neurone density with brain size. Journal of Comparative Neurology 101, 9–52.Google Scholar
  85. van Essen, D. C. (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318.PubMedGoogle Scholar
  86. Volpe, J. J. (1981) Neurology of the Newborn. Philadelphia: Saunders.Google Scholar
  87. Watts, D. J. &; Strogatz, S. H. (1998) Collective dynamics of 'small-world' networks. Nature 393, 440–442.PubMedGoogle Scholar
  88. Waxman, S. G. &; Swadlow, H. A. (1976) Ultrastructure of visual callosal axons in the rabbit. Experimental Neurology 53, 115–127.PubMedGoogle Scholar
  89. Zhang, K. &; Sejnowski, T. J. (2000)Auniversal scaling law between gray matter and white matter of cerebral cortex. Proceedings of the National Academy of Sciences USA 97, 5621–5626.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Kimberly H. Harrison
    • 1
  • Patrick R. Hof
    • 2
  • Samuel S.-H. Wang
    • 1
  1. 1.Department of Molecular BiologyPrinceton UniversityPrinceton
  2. 2.Fishberg Research Center for Neurobiology, Kastor Neurobiology of Aging Laboratories, and Advanced Imaging ProgramMount Sinai School of MedicineNew YorkUSA

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