Journal of Neurocytology

, Volume 31, Issue 3–5, pp 299–316 | Cite as

Microstructure of the neocortex: Comparative aspects

  • Javier DeFelipe
  • Lidia Alonso-Nanclares
  • Jon I. Arellano


The appearance of the neocortex, its expansion, and its differentiation in mammals, represents one of the principal episodes in the evolution of the vertebrate brain. One of the fundamental questions in neuroscience is what is special about the neocortex of humans and how does it differ from that of other species? It is clear that distinct cortical areas show important differences within both the same and different species, and this has led to some researchers emphasizing the similarities whereas others focus on the differences. In general, despite of the large number of different elements that contribute to neocortical circuits, it is thought that neocortical neurons are organized into multiple, small repeating microcircuits, based around pyramidal cells and their input-output connections. These inputs originate from extrinsic afferent systems, excitatory glutamatergic spiny cells (which include other pyramidal cells and spiny stellate cells), and inhibitory GABAergic interneurons. The problem is that the neuronal elements that make up the basic microcircuit are differentiated into subtypes, some of which are lacking or highly modified in different cortical areas or species. Furthermore, the number of neurons contained in a discrete vertical cylinder of cortical tissue varies across species. Additionally, it has been shown that the neuropil in different cortical areas of the human, rat and mouse has a characteristic layer specific synaptology. These variations most likely reflect functional differences in the specific cortical circuits. The laminar specific similarities between cortical areas and between species, with respect to the percentage, length and density of excitatory and inhibitory synapses, and to the number of synapses per neuron, might be considered as the basic cortical building bricks. In turn, the differences probably indicate the evolutionary adaptation of excitatory and inhibitory circuits to particular functions.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amitai, Y. (2001) Thalamocortical synaptic connections: Efficacy, modulation, inhibition and plasticity. Reviews of Neuroscience 12, 159–173.Google Scholar
  2. Anderson, S., Mione, M., Yun, K. &; Rubenstein, J. L. (1999) Differential origins of neocortical projection and local circuit neurons: Role of Dlx genes in neocortical interneuronogenesis. Cerebral Cortex 9, 646–654.PubMedGoogle Scholar
  3. Beaulieu, C. (1993) Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Research 609, 284–292.PubMedGoogle Scholar
  4. 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 Neurology 231, 180–189.PubMedGoogle Scholar
  5. 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, 178–187.PubMedGoogle Scholar
  6. Beaulieu, C., Campistron, G. &; Crevier, C. (1994) Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat. Journal of Comparative Neurology 339, 559–572.PubMedGoogle Scholar
  7. Beaulieu, C., Kisvarday, Z., Somogyi, P., Cynader, M. &; Cowey, A. (1992) Quantitative distribution of GABA-immunopositive and-immunonegative neurons and synapses in the monkey striate cortex (area 17). Cerebral Cortex 2, 295–309.PubMedGoogle Scholar
  8. Benavides-Piccione, R. &; deFelipe, J. (2003) Different populations of tyrosine hydroxylaseimmunoreactive neurons defined by differential expression of nitric oxide synthase in the human temporal cortex. Cerebral Cortex 13, 297–307.PubMedGoogle Scholar
  9. Blue, M. E. &; Parnavelas, J. G. (1983) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. Journal of Neurocytology 12, 697–712.PubMedGoogle Scholar
  10. Bourgeois, J.-P. &; Rakic, P. (1993) Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. Journal of Neuroscience 13, 2801–2820.PubMedGoogle Scholar
  11. Bourgeois, J.-P., Goldman-Rakic, P. S. &; Rakic, P. (1994) Synaptogenesis in the prefrontal cortex of rhesus monkey. Cerebral Cortex 4, 78–96.PubMedGoogle Scholar
  12. Buxhoeveden, D. P. &; Casanova, M. F. (2002) The minicolumn hypothesis in neuroscience. Brain 125, 935–951.PubMedGoogle Scholar
  13. Cajal, S. R. (1899) Estudios sobre la corteza cerebral humana II: Estructura de la corteza motriz del hombre y mamíferos superiores. Revista Trimestral Microgáfica 4, 117–200. Translated in deFelipe, J. &; Jones, E. G. (1988). Cajal on the Cerebral Cortex. New York: Oxford University Press.Google Scholar
  14. Cajal, S. R. (1917) Recuerdos de mi vida, Vol. 2: Historia de mi labor científica. Madrid: Moya.Google Scholar
  15. Campbell, M. J. &; Morrison, J. H. (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. Journal of Comparative Neurology 282, 191–205.PubMedGoogle Scholar
  16. 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
  17. Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Research 9, 268–287.PubMedGoogle Scholar
  18. Colonnier, M. (1981) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In The Organization of the Cerebral Cortex (edited by Schmitt, F. O., Worden, F. G., Adelman, G. &; Dennis, S. G.) pp. 125–152. Cambridge: MIT Press.Google Scholar
  19. Conti, F. &; Weinberg, R. J. (1999) Shaping excitation at glutamatergic synapses. Trends in Neuroscience 22, 451–458.Google Scholar
  20. 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
  21. deFelipe, J. (1993) Neocortical neuronal diversity: Chemical heterogeneity revealed by co-localization studies of classic neurotransmitters, neuropeptides, calcium binding proteins and cell surface molecules. Cerebral Cortex 3, 273–289.PubMedGoogle Scholar
  22. deFelipe, J. (1997) Microcircuits in the brain. In Lecture Notes in Computer Science, Vol. 1240 (edited by Mira, J., Moreno-DÍaz, R. &; Cabestany, J.) pp. 1–14. Berlin: Springer.Google Scholar
  23. deFelipe, J. (2002) Cortical interneurons: From Cajal to 2001. In Changing Views of Cajal's Neuron (edited by Azmitia, E., deFelipe, J., Jones, E. G., Rakic, P. &; Ribak, C.) Progress in Brain Research 136, 215–238.Google Scholar
  24. deFelipe, J. &; Jones, E. G. (1988) Cajal on the Cerebral Cortex. New York: Oxford University Press.Google Scholar
  25. deFelipe, J. &; FariÑas, I. (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Progress in Neurobiology 39, 563–607.PubMedGoogle Scholar
  26. DEFELIPE, J., HENDRY, S. H. C., HASHIKAWA, T., MOLINARI, M. &; JONES, E. G. (1990) A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37, 655–673.PubMedGoogle Scholar
  27. deFelipe, J., Marco, P., FairÉn, A., &; Jones, E. G. (1997) Inhibitory synaptogenesis in mouse somatosensory cortex. Cerebral Cortex 7, 619–634.PubMedGoogle Scholar
  28. deFelipe, J., Marco, P., Busturia, I. &; Merchanperez, A. (1999a) Estimation of the number of synapses in the cerebral cortex: Methodological considerations. Cerebral Cortex 9, 722–732.PubMedGoogle Scholar
  29. deFelipe, J., GonzÁlez-Albo, M. C., del RÍo, M. R. &; Elston, G. N. (1999b) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. Journal of Comparative Neurology 412, 515–526.PubMedGoogle Scholar
  30. deFelipe, J., Arellano, J. I., MerchÁn-PÉrez, A., GonzÁlez-Albo, M. C., Walton, K. &; LlinÁs, R. (2002) Spaceflight induces changes in the synaptic circuitry of the postnatal developing neocortex. Cerebral Cortex 12, 883–891.PubMedGoogle Scholar
  31. del RÍo, M. R. &; deFelipe, J. (1996) Colocalization of calbindin D-28k, calretinin and GABA immunoreactivities in neurons of the human temporal cortex. Journal of Comparative Neurology 369, 472–482.PubMedGoogle Scholar
  32. del RÍo, M. R. &; deFelipe, J. (1997a) Double bouquet cell axons in thehumantemporal neocortex: Relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. Journal of Chemical Neuroanatomy 13, 243–251.PubMedGoogle Scholar
  33. del RÍio, M. R. &; deFelipe, J. (1997b) Colocalization of parvalbumin and calbindin d-28k in neurons including chandelier cells of thehumantemporal neocortex. Journal of Chemical Neuroanatomy 12, 165–173.PubMedGoogle Scholar
  34. Dexler, H. (1913) Das Hirn von Halicore dugong Erxl. Gegenbaurs Morphologisches Jahrbuch 45, 97–190.Google Scholar
  35. Elston, G. N., Tweedale, R. &; Rosa, M. G. P. (1999a) Cortical integration in the visual system of the macaque monkey: Large scale morphological differences of pyramidal neurones in the occipital, parietal and temporal lobes. Proceedings of the Royal Society of London Series B 266, 1367–1374.Google Scholar
  36. Elston, G. N., Manger, P. R. &; Pettigrew, J. D. (1999b) Morphology of pyramidal neurones in cytochrome oxidase modules of the S-I bill representation of the platypus. Brain Behavior and Evolution 53, 87–101.Google Scholar
  37. Elston, G. N., Benavides-Piccione, R. &; deFelipe, J. (2001) The pyramidal cell in cognition: A comparative study in man and monkey. Journal of Neuroscience 21, RC163, 1–5.Google Scholar
  38. FairÉn, A., deFelipe, J. &; Regidor, J. (1984) Nonpyramidal neurons. General account. In Cellular Components of the Cerebral Cortex, Vol. 1, Cerebral Cortex (edited by Peters, A. &; Jones, E. G.) pp. 201–253.NewYork: Plenum Press.Google Scholar
  39. Gabbott, P. L. A. &; Bacon, S. J. (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions. Journal of Comparative Neurology 364, 609–636.PubMedGoogle Scholar
  40. Gabbott, P. L. A., Dickie, B. G. M., Vaid, R. R., Headlam, A. J. N. &; Bacon, S. J. (1997) Localcircuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution. Journal of Comparative Neurology 377, 465–499.PubMedGoogle Scholar
  41. Galarreta, M. &; Hestrin, S. (2001) Electrical synapses between GABA-releasing interneurons. Nature Reviews Neuroscience 2, 425–433.PubMedGoogle Scholar
  42. Gilbert, G. D. &; Kelly, J. P. (1975) The projection of cells in different layers of the cat's visual cortex. Journal of Comparative Neurology 163, 81–106.PubMedGoogle Scholar
  43. Glezer, I. I., Jacobs, M. S. &; Morgane, P. J. (1988) Implications of the “initial brain” concept for brain evolution in Cetacea. The Behavioral and Brain Sciences 11, 75–116.Google Scholar
  44. Glezer, I. I. &; Morgane, P. J. (1990) Ultrastructure of synapses and Golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale. Brain Research Bulletin 24, 401–427.PubMedGoogle Scholar
  45. Glezer, I. I., Hof, P. R., Leranth, C. &; Morgane, P. J. (1993) Calcium-binding protein-containing neuronal populations in mammalian visual cortex: A comparative study in whales, insectivores, bats, rodents, and primates. Cerebral Cortex 3, 249–272.PubMedGoogle Scholar
  46. Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscopic study. Journal of Anatomy 93, 420–433.PubMedGoogle Scholar
  47. Haug, H. (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: A stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). The American Journal of Anatomy 180, 126–142.PubMedGoogle Scholar
  48. Hendry, S. H. C., Schwark, H. D., Jones, E. G. &; Yan, J. (1987) Numbers and proportions of GABAimmunoreactive neurons in different areas of monkey cerebral cortex. Journal of Neuroscience 7, 1503–1519.PubMedGoogle Scholar
  49. Hof, P. R., Glezer, I. 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
  50. Hof, P. R., Glezer, I. I., Nimchinsky, E. A. &; Erwin, J. M. (2000) 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
  51. Houser, C. R., Vaughn, J. E., Hendry, S. H. C., Jones, E. G. &; Peters, A. (1984) GABA neurons in cerebral cortex. Functional Properties of Cortical Cells. In Cerebral Cortex (edited by Jones, E. G. &; Peters, A.) pp. 63–89. New York: Plenum Press.Google Scholar
  52. Hubel, D. H. &; Wiesel, T. N. (1977) Functional architecture of macaque monkey cortex. Proccedings of the Royal Society of London Series B 198, 1–59.Google Scholar
  53. Huttenlocher, P. R. &; Dabholkar, A. S. (1997) Regional differences in synaptogenesis in human cerebral cortex. Journal of Comparative Neurology 387, 167–178.PubMedGoogle Scholar
  54. Johnson, J. I., Kirsch, J. A., Reep, R. L. &; Switzer, R. C. 3RD (1994) Phylogeny through brain traits: More characters for the analysis of mammalian evolution. Brain, Behavior and Evolution 43, 319–347.Google Scholar
  55. Jones, E. G. (1983) The columnar basis of cortical circuitry. In The Clinical Neurosciences (edited by Willis, W. D.) pp. 357–383. New York: Churchill Livingstone.Google Scholar
  56. Jones, E. G. (2000a) Microcolumns in the cerebral cortex. Proceedings of the National Academy of Sciences of USA 97, 5019–5021.Google Scholar
  57. Jones, E. G. (2000b) Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annual Review of Neuroscience 23, 1–37.PubMedGoogle Scholar
  58. Jones, E. G. &; Powell, T. P. S. (1970) Electron microscopy of the somatic sensory cortex of the cat. I. Cell types and synaptic organization. Philosophical Transactions of the Royal Society of London Biological Sciences 257, 1–11.Google Scholar
  59. Jones, E. G. &; Hendry, S. H. C. (1986) Co-localization of GABA and neuropeptides in neocortical neurons. Trends in Neuroscience 10, 71–76.Google Scholar
  60. Jones, E. G. &; Wise, S. P. (1977). Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. Journal of Comparative Neurology 175, 391–438.PubMedGoogle Scholar
  61. Kawaguchi, Y. &; Kubota, Y. (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex 7, 476–486.PubMedGoogle Scholar
  62. Kubota, Y. &; Kawaguchi, Y. (2000) Dependence of GABAergic synaptic areas on the interneuron type and target size. Journal of Neuroscience 20, 375–386.PubMedGoogle Scholar
  63. Letinic, K., Zoncu, R. &; Rakic, P. (2002) Origin of GABAergic neurons in the human neocortex. Nature 417, 645–649.PubMedGoogle Scholar
  64. Lewis, D. A. &; Lund, J. S. (1990) Heterogeneity of chandelier neurons in monkey neocortex: Corticotropinreleasing factor-and parvalbumin-immunoreactive populations. Journal of Comparative Neurology 293, 599–615.PubMedGoogle Scholar
  65. Lorente de NÓ, R. (1938) Architectonics and structure of the cerebral cortex. In Physiology of the Nervous System (edited by Fulton, J. F.) pp. 291–330. New York: Oxford University Press.Google Scholar
  66. Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. H. &; Fuchs, A. F. (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. Journal of Comparative Neurology 164, 287–304.Google Scholar
  67. LÜscher, C., Nicoll, R. A., Malenka, R. C. &; Muller, D. (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nature Neuroscience 3, 545–550.PubMedGoogle Scholar
  68. Mackenzie, P. J., Kenner, G. S., Prange, O., Shayan, H., Umemiya, M. &; Murphy, T. H. (1999) Ultrastructural correlates of quantal synaptic function at single CNS synapses. Journal of Neuroscience 19, RC13, 1–7.PubMedGoogle Scholar
  69. Marco, P. &; deFelipe, J. (1997) Altered synaptic circuitry in the human temporal epileptogenic neocortex. Experimental Brain Research 114, 1–10.Google Scholar
  70. Marin, O., Yaron, A., Bagri, A., Tessierlavigne, M. &; Rubenstein, J. L. (2001) Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293, 872–875.PubMedGoogle Scholar
  71. Micheva, K. D. &; Beaulieu, C. (1995) Postnatal development of GABA neurons in the rat somatosensory barrel cortex: A quantitative study. European Journal of Neuroscience 7, 419–430.PubMedGoogle Scholar
  72. Micheva, K. D. &; Beaulieu, C. (1996) Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to the GABA circuitry. Journal of Comparative Neurology 373, 340–354.PubMedGoogle Scholar
  73. Mountcastle, V. B. (1978) An organizing principle for cerebral function: The unit module and the distributed system. In The Mindful Brain (edited by Mountcastle, V. B. &; Edelman, G. M.) pp. 7–50. Cambridge: MIT Press.Google Scholar
  74. Mountcastle, V. B. (1997) The columnar organization of the neocortex. Brain 120, 701–722.PubMedGoogle Scholar
  75. Nieuwenhuys, R. (1994) The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anatomy and Embryology 190, 307–337.PubMedGoogle Scholar
  76. 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 ofUSA 96, 5268–5273.Google Scholar
  77. 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
  78. Peters, A. (1987) Synaptic specificity in the cerebral cortex. In Synaptic Function (edited by Edelman, G. M., Gall, W. E. &; Cowan, W. M.) pp. 373–397. New York: John Wiley.Google Scholar
  79. Peters, A. &; Jones, E. G. (1984) Cerebral Cortex Vol. 1: Cellular Components of the Cerebral Cortex. New York: Plenum Press.Google Scholar
  80. Peters, A. &; Palay, S. L. (1996) The morphology of synapses. Journal of Neurocytology 25, 687–700.PubMedGoogle Scholar
  81. Peters, A., Palay, S. L. &; Webster, H. DE F. (1991) The Fine Structure of the Nervous System. Neurons and their Supporting Cells. New York: Oxford University Press.Google Scholar
  82. Peters, A. &; Sethares, C. (1997) The organization of double bouquet cells in monkey striate cortex. Journal of Neurocytology 26, 779–797.PubMedGoogle Scholar
  83. Petrides, M. &; Pandya, D. N. (1994) Comparative architectonic analysis of the human and the macaque frontal cortex. Handbook of Neurophysiology 9, 17–58.Google Scholar
  84. Poe, B. H., Linville, C. &; Brunso-Bechtold, J. (2001) Age-related decline of presumptive inhibitory synapses in the sensorimotor cortex as revealed by the physical dissector. Journal of Comparative Neurology 439, 65–72.PubMedGoogle Scholar
  85. Powell, T. P. S. (1981) Ceratin aspects of the intrinsic organization of the cerebral cortex. In Brain Mechanisms and Perceptual Awareness (edited by Pompeiano, O. &; Ajmone Marsan, C.) pp. 1–19. New York: Raven Press.Google Scholar
  86. Preuss, T. M. &; Coleman, G. Q. (2002) Human-specific organization of primary visual cortex: Alternating compartments of dense Cat 301 and calbindin immunoreactivity in layer 4A. Cerebral Cortex 12, 671–691.PubMedGoogle Scholar
  87. Rakic, P. (1988) Specification of cerebral cortical areas. Science 241, 170–176.PubMedGoogle Scholar
  88. Rakic, P. (2002) Evolving concepts of cortical radial and areal specification. In Changing Views of Cajal's Neuron (edited by Azmitia, E., deFelipe, J., Jones, E. G., Rakic, P. &; Ribak, C.) Progress in Brain Research 136, 265–280.Google Scholar
  89. 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
  90. Rakic, P., Bourgeois, J.-P. &; Goldman-Rakic, P. S. (1994) Synaptic development of the cerebral cortex: Implications for learning, memory, and mental illness. Progress in Brain Research 104, 227–243.Google Scholar
  91. Ren, J. Q., Aika, Y., Heizmann, C. W. &; Kosaka, T. (1992) Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons. Experimental Brain Research 92, 1–14.Google Scholar
  92. Reep, R. L., Johnson, J. I., Switzer, R. C. &; Welker, W. I. (1989) Manatee cerebral cortex: Cytoarchitecture of the frontal region in Trichechus Manatus Latirostris. Brain, Behavior and Evolution 34, 365–386.Google Scholar
  93. Rockel, A. J., Hiorns, R. W. &; Powell, T. P. S. (1980) The basic uniformity in structure of the neocortex. Brain 103, 221–244.PubMedGoogle Scholar
  94. Schikorski, T. &; Stevens, C. F. (1999) Quantitative fine-structural analysis of olfactory cortical synapses. Proceedings of the National Academy of Sciences of USA 96, 4107–4112.Google Scholar
  95. 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
  96. Silberberg, G., Gupta, A. &; Markram, H. (2002) Stereotypy in neocortical microcircuits. Trends in Neuroscience 25, 227–230.PubMedGoogle Scholar
  97. Skoglund, T. S., Pascher, R. &; Berthold, C. H. (1996) Heterogeneity in the columnar number of neurons in different neocortical areas in the rat. Neuroscience Letters 208, 97–100.PubMedGoogle Scholar
  98. Sloper, J. J. (1973) An electron microscope study of the neurons of the primate motor and somatic sensory cortices. Journal of Neurocytology 2, 351–359.PubMedGoogle Scholar
  99. Sloper, J. J., Hiorns, R. W. &; Powell, T. P. S. (1979) A qualitative and quantitative electron microscopic study of the neurons in the primate motor and somatic sensory cortices. Philosophical Transactions of the Royal Society of London Series B 285, 141–171.PubMedGoogle Scholar
  100. Somogyi, P., TamÁs, G., Lujan, R. &; Buhl, E. H. (1998) Salient features of synaptic organization in the cerebral cortex. Brain Research Reviews 26, 113–135.PubMedGoogle Scholar
  101. Stolzenburg, J. U., Reichenbach, A. &; Neumann, M. (1989) Size and density of glial and neuronal cells within the cerebral neocortex of various insectivorian species. Glia 2, 78–84.PubMedGoogle Scholar
  102. Takumi, Y., RamÍrez-LeÓn, V., Laake, P., Rinvik, E. &; Ottersen, O. P. (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nature Neuroscience 2, 618–624.PubMedGoogle Scholar
  103. Tan, S. S., Kalloniatis, M., Sturm, K., Tam, P. P., Reese, B. E. &; Faulkner-Jones, B. (1998) Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron 21, 295–304.PubMedGoogle Scholar
  104. Thomson, A. M. &; Deuchars, J. (1997) Synaptic interactions in neocortical local circuits: Dual intracellular recordings in vitro. Cerebral Cortex 7, 510–522.PubMedGoogle Scholar
  105. TÖmbÖl, T. (1974) An electron microscopic study of the neurons of the visual cortex. Journal of Neurocytology 3, 525–531.PubMedGoogle Scholar
  106. Tyler, C. J., Dunlop, S. A., Lund, R. D., Harman, A. M., Dann, J. F., Beazley, L. D. &; Lund, J. S. (1998) Anatomical comparison of the macaque and marsupial visual cortex: Common features that may reflect retention of essential cortical elements. Journal of Comparative Neurology 400, 449–468.PubMedGoogle Scholar
  107. Wang, Y., Gupta, A., Toledo-Rodriguez, M., Wu, C. Z. &; Markram, H. (2002) Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cerebral Cortex 12, 395–410.PubMedGoogle Scholar
  108. West, M. J. &; Gundersen, H. J. (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. Journal of Comparative Neurology 296, 1–22.PubMedGoogle Scholar
  109. White, E. L. (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure, Function and Theory. Boston: Birkhäuser.Google Scholar
  110. White, E. L., Weinfeld, L. &; Lev, D. L. (1997)Asurvey of morphogenesis during the early postnatal period in PMBSF barrels of mouse SmI cortex with emphasis on barrel D4. Somatosensory &; Motor Research 14, 34–55.Google Scholar
  111. Williams, R. W. &; Rakic, P. (1988) Three-dimensional counting: An accurate and direct method to estimate numbers of cells in sectioned material. Journal of Comparative Neurology 278, 344–352.PubMedGoogle Scholar
  112. Winfield, D. A., Gatter, K. C. &; Powell, T. P. S. (1980) Aelectron microscopic study of the types and proportions of neurons in the cortex of the motor and visual areas of the cat and rat. Brain 103, 245–258.PubMedGoogle Scholar
  113. Zecevic, N. &; Rakic, P. (1991) Synaptogenesis in monkey somatosensory cortex. Cerebral Cortex 1, 510–523.PubMedGoogle Scholar
  114. Zecevic, N., Bourgeois, J.-P. &; Rakic, P. (1989) Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Developmental Brain Research 50, 11–32.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Javier DeFelipe
    • 1
  • Lidia Alonso-Nanclares
    • 1
  • Jon I. Arellano
    • 1
  1. 1.Instituto Cajal (CSIC)MadridSpain

Personalised recommendations