The evolution of the brain, the human nature of cortical circuits, and intellectual creativity

Frontiers in Neuroanatomy

Volumn , Issue MAY, 2011, Pages

  DeFelipe, Javier ^a,b,c  

^a INSTITUTO CAJAL   (Spain)

^b TECHNICAL UNIVERSITY OF MADRID   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Brain size; Cortical circuits; Evolution; Human nature; Number synapses; Pyramidal neurons

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL BEHAVIOR; BEHAVIOR CHANGE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN SIZE; BRAIN WEIGHT; CELL AGGREGATION; CELLULAR DISTRIBUTION; CYTOARCHITECTURE; DENDRITE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FUNCTIONAL MORPHOLOGY; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; INTELLIGENCE; LEARNING; MEMORY; MENTAL DEVELOPMENT; NEOCORTEX; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; QUALITY OF LIFE; REVIEW; SPECIES COMPOSITION; STRUCTURE ANALYSIS; SYNAPTIC POTENTIAL;

EID: 84861865997     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2011.00029     Document Type: Review

References (102)

1. Anderson, S. A., Kaznowski, C. E., Horn, C., Rubenstein, J. L., and McConnell, S. K. (2002). Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb. Cortex 12, 702-709.
2. Ballesteros-Yáñez, I., Benavides-Piccione, R., Bourgeois, J. P., Changeux, J. P., and DeFelipe, J. (2010). Alterations of cortical pyramidal neurons in mice lacking high-affinity nicotinic receptors. Proc. Natl. Acad. Sci. U.S.A. 107, 11567-11572.
3. Ballesteros-Yáñez, I., Benavides-Piccione, R., Elston, G. N., Yuste, R., and DeFelipe, J. (2006). Density and morphology of dendritic spines in mouse neocortex. Neuroscience 138, 403-409.
4. Ballesteros-Yánez, I., Muñoz, A., Contreras, J., Gonzalez, J., Rodriguez-Veiga, E., and DeFelipe, J. (2005). The double bouquet cell in the human cerebral cortex and a comparison with other mammals. J. Comp. Neurol. 486, 344-360.
5. Balter, M. (2009). On the origin of art and symbolism. Science 323, 709-711.
6. Barton, R. A. (2002). How did brains evolve? Nature 415, 134-135.
7. Barton, R. A., and Harvey, P. H. (2000). Mosaic evolution of brain structure in mammals. Nature 405, 1055-1058.
8. Beaulieu, C. (1993). Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res. 609, 284-292.
9. Beaulieu, C., and Colonnier, M. (1989). Number and size of neurons and synapses in the motor cortex of cats raised in different environmental complexities. J. Comp. Neurol. 289, 178-181.
10. Beaulieu, C., Kisvarday, Z., Somogyi, P., Cynader, M., and Cowey, A. (1992). Quantitative distribution of GABA-immunopositive and-immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb. Cortex 2, 295-309.
11. Benavides-Piccione, R., Ballesteros-Yañez, I., DeFelipe, J., and Yuste, R. (2002). Cortical area and species differences in dendritic spine morphology. J. Neurocytol. 31, 337-346.
12. Benavides-Piccione, R., and DeFelipe, J. (2007). Distribution of neurons expressing tyrosine hydroxylase in the human cerebral cortex. J. Anat. 211, 212-222.
13. Bermúdez de Castro, J. M. (2002). El chico de la Gran Dolina. Barcelona: Crítica.
14. Byrne, R. W., Barnard, P. J., Davidson, I., Janik, V. M., McGrew, W. C., Miklósi, A., and Wiessner, P. (2004). Understanding culture across species. Trends Cogn. Sci. (Regul. Ed.) 8, 341-346.
15. Bystron, I., Blakemore, C., and Rakic, P. (2008). Development of the human cerebral cortex: Boulder Committee revisited. Nat. Rev. Neurosci. 9, 110-122.
16. Cajal, S. R. (1899). Estudios sobre la corteza cerebral humana I: corteza visual. Rev. Trim. Microgr. 4, 1-63.
17. Translated in: DeFelipe, J., and Jones, E. G. (1988). Cajal on the Cerebral Cortex. New York: Oxford University Press.
18. Cajal, S. R. (1917). Recuerdos de Mi Vida, Vol. 2, Historia de Mi Labor Científica. Madrid: Moya.
19. Campbell, M. C., and Tishkoff, S. A. (2008). African genetic diversity: implications for human demographic history, modern human origins, and complex disease mapping. Annu. Rev. Genomics Hum. Genet. 9, 403-433.
20. Clark, D. A., Mitra, P. P., and Wang, S. S. (2001). Scalable architecture in mammalian brains. Nature 411, 189-193.
21. Conard, N. J. (2010). Cultural modernity: consensus or conundrum? Proc. Natl. Acad. Sci. U.S.A. 107, 7621-7622.
22. Conel, J., and Le, R. (1941). The Postnatal Development of the Human Cerebral Cortex. Vol. 2. The Cortex of the One-Month Infant. Cambridge, MA: Harvard University Press.
23. Conel, J., and Le, R. (1967). The Postnatal Development of the Human Cerebral Cortex. Vol. 8. The Cortex of the Six-Year Child. Cambridge, MA: Harvard University Press.
24. Couzin, I. D. (2009). Collective cognition in animal groups. Trends Cogn. Sci. (Regul. Ed.) 13, 36-43.
25. Cragg, B. G. (1967). The density of synapses and neurones in the motor and visual areas of the cerebral cortex. J. Anat. 101, 639-654.
26. de Winter, W., and Oxnard, C. E. (2001). Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409, 710-714.
27. DeFelipe, J. (2002). Cortical interneurons: from Cajal to 2001. Prog. Brain Res. 136, 215-238.
28. DeFelipe, J. (2006). Brain plasticity and mental processes: Cajal again. Nat. Rev. Neurosci. 7, 811-817.
29. DeFelipe, J. (2010a). "Reflexiones sobre lo bello, el arte y la evolución del cerebro," in Neuroestética, ed. A. Martín Araguz (Madrid: Saned), 51-76.
30. DeFelipe, J. (2010b). From the connectome to the synaptome: an epic love story. Science 330, 1198-1201.
31. DeFelipe, J., Alonso-Nanclares, L., and Arellano, J. I. (2002). Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31, 299-316.
32. DeFelipe, J., and Fariñas, I. (1992). The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39, 563-607.
33. DeFelipe, J., Hendry, S. H., Hashikawa, T., Molinari, M., and Jones, E. G. (1990). A microcolumnar structure of monkey cerebral cortex revealed by immunocytochemical studies of double bouquet cell axons. Neuroscience 37, 655-673.
34. del Río, M. R., and DeFelipe, J. (1996). Colocalization of calbindin D-28k, calretinin, and GABA immunoreactivities in neurons of the human temporal cortex. J. Comp. Neurol. 369, 472-482.
35. del Río, M. R., and DeFelipe, J. (1997). Double bouquet cell axons in the human temporal neocortex: relationship to bundles of myelinated axons and colocalization of calretinin and calbindin D-28k immunoreactivities. J. Chem. Neuroanat. 13, 243-251.
36. Dexler, H. (1913). Das Hirn von Halicore dugong Erxl. Gegenbaurs. Morphol. Jahrb. 45, 97-190.
37. Elston, G. N. (2007). "Specializations of the neocortical pyramidal cell during primate evolution," in Evolution of the Nervous Systems: A Comprehensive Reference, Vol. 4 Primates, eds J. H. Kaas and T. M. Preuss (Amsterdam: Elsevier), 191-242.
38. Elston, G. N., Benavides-Piccione, R., and DeFelipe, J. (2001). The pyramidal cell in cognition: a comparative study in man and monkey. J. Neurosci. 21, 1-5.
39. Elston, G. N., Elston, A., Casagrande, V. A., and Kaas, J. (2005). Pyramidal neurons of granular prefrontal cortex the galago: complexity in the evolution of the psychic cell in primates. Anat. Rec. 285, 610-618
40. Finlay, B. L., and Darlington, R. B. (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578-1584.
41. Gabbott, P. L., and 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. J. Comp. Neurol. 364, 609-636.
42. Gabbott, P. L., Dickie, B. G., Vaid, R. R., Headlam, A. J., and Bacon, S. J. (1997). Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: morphology and quantitative distribution. J. Comp. Neurol. 377, 465-499.
43. Gaspar, P., Berger, B., Febvret, A., Vigny, A., Krieger-Poulet, M., and Borri-Voltattorni, C. (1987). Tyrosine hydroxylase-immunoreactive neurons in the human cerebral cortex: a novel catecholaminergic group? Neurosci. Lett. 80, 257-262.
44. Glezer, I. I., Hof, P. R., Leranth, C., and Morgane, P. J. (1993). Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cereb. Cortex 3, 249-272.
45. Glezer, I. I., Jacobs, M. S., and Morgane, P. J. (1988). Implications of the "initial brain" concept for brain evolution in Cetacea. Behav. Brain Sci. 11, 75-116.
46. 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). Am. J. Anat. 180, 126-142.
47. Hendry, S. H., Schwark, H. D., Jones, E. G., and Yan, J. (1987). Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J. Neurosci. 7, 1503-1519.
48. Henshilwood, C. S., d'Errico, F., and Watts, I. (2009). Engraved ochres from the Middle Stone Age levels at Blombos cave, South Africa. J. Hum. Evol. 57, 27-47.
49. Henshilwood, C. S., d'Errico, F., Yates, R., Jacobs, Z., Tribolo, C., Duller, G. A., Mercier, N., Sealy, J. C., Valladas, H., Watts, I., and Wintle, A. G. (2002). Emergence of modern human behavior: Middle Stone Age engravings from South Africa. Science 295, 1278-1280.
50. Hof, P. R., Glezer, I. I., Conde, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., and 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. J. Chem. Neuroanat. 16, 77-116.
51. Hof, P. R., Glezer, I. I., Revishchin, A. V., Bouras, C., Charnay, Y., and Morgane, P. J. (1995). Distribution of dopaminergic fibers and neurons in visual and auditory cortices of the harbor porpoise and pilot whale. Brain Res. Bull. 36, 275-284.
52. Hof, P. R., Glezer, L. I., Nimchinsky, E. A., and Erwin, J. M. (2000). Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav. Evol. 55, 300-310.
53. Holloway, R. (1996). "Evolution of the human brain" in Handbook of Human Symbolic Evolution, eds A. Lock and C. R. Peters (Oxford: Oxford University Press), 74-125.
54. Hornung, J. P., Tork, I., and De Tribolet, N. (1989). Morphology of tyrosine hydroxylase-immunoreactive neurons in the human cerebral cortex. Exp. Brain Res. 76, 12-20.
55. Jacobs, B., Schall, M., Prather, M., Kapler, L., Driscoll, L., Baca, S., Jacobs, J., Ford, K., Wainwright, M., and Treml, M. (2001). Regional dendritic and spine variation in human cerebral cortex: a quantitative study. Cereb. Cortex 11, 558-571.
56. Jakovcevski, I., Mayer, N., and Zecevic, N. (2011). Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. Cereb. Cortex. doi: 10.1093/cercor/bhq245. [Epub ahead of print].
57. Jerison, H. J. (1973). Evolution of the Brain and Intelligence. New York: Academic Press.
58. Johnson, J. I., Kirsch, J. A., Reep, R. L., and Switzer, R. C. III. (1994). Phylogeny through brain traits: more characters for the analysis of mammalian evolution. Brain Behav. Evol. 43, 319-347.
59. Jones, E. G. (1975). Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. Comp. Neurol. 160, 205-268.
60. Jones, E. G. (2009). Origins of cortical interneurons: mouse vs monkey and human. Cereb. Cortex 19, 1953-1956.
61. Kaas, J. H., and Collins, C. E. (2001). Evolving ideas of brain evolution. Nature 411, 141-142.
62. Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., and Noguchi, J. (2010). Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 33, 121-129.
63. Katz, P. S., and Harris-Warrick, R. M. (1999). The evolution of neuronal circuits underlying species-specific behavior. Curr. Opin. Neurobiol. 9, 628-633.
64. Klein, R. G. (2009). Darwin and the recent African origin of modern humans. Proc. Natl. Acad. Sci. U.S.A. 106, 16007-16009.
65. Kohler, C., Everitt, B. J., Pearson, J., and Goldstein, M. (1983). Immunohistochemical evidence for a new group of catecholamine-containing neurons in the basal forebrain of the monkey. Neurosci. Lett. 37, 161-166.
66. Kosaka, T., Kosaka, K., Hataguchi, Y., Nagatsu, I., Wu, J. Y., Ottersen, O. P., Storm-Mathisen, J., and Hama, K. (1987). Catecholaminergic neurons containing GABA-like and/ or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp. Brain Res. 66, 191-210.
67. Kuljis, R. O., Martin-Vasallo, P., and Peress, N. S. (1989). Lewy bodies in tyrosine hydroxylase-synthesizing neurons of the human cerebral cortex. Neurosci. Lett. 106, 49-54.
68. Letinic, K., Zoncu, R., and Rakic, P. (2002). Origin of GABAergic neurons in the human neocortex. Nature 417, 645-649.
69. Lewis, D. A., Foote, S. L., Goldstein, M., and Morrison, J. H. (1988). The dopaminergic innervation of monkey prefrontal cortex: a tyrosine hydroxylase immunohistochemical study. Brain Res. 449, 225-243.
70. Marino, L. (1998). A comparison of encephalization between odontocete cetaceans and anthropoid primates. Brain Behav. Evol. 51, 230-238.
71. Mcbrearty, S., and Brooks, A. S. (2000). The revolution that wasn't: a new interpretation of the origin of modern human behavior. J. Hum. Evol. 39, 453-563.
72. McDougall, I., Brown, F. H., and Fleagle, J. G. (2005). Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433, 733-736.
73. Meinecke, D. L., and Peters, A. (1987). GABA immunoreactive neurons in rat visual cortex. J. Comp. Neurol. 261, 388-404.
74. Micheva, K. D., and Beaulieu, C. (1995). Postnatal development of GABA neurons in the rat somatosensory barrel cortex: a quantitative study. Eur. J. Neurosci. 7, 419-430.
75. Nissl, F. (1898). Nervenzellen und graue Substanz. Munch. med. Wschr. 45, 988-992, 1023-1029, 1060-1062.
76. Petanjek, Z., Kostović, I., and Esclapez, M. (2009). Primate-specific origins and migration of cortical GABAergic neurons. Front. Neuroanat. 3:26. doi:10.3389/neuro.05.026.2009
77. Peters, A., and Sethares, C. (1997). The organization of double bouquet cells in monkey striate cortex. J. Neurocytol. 26, 779-797.
78. Preuss, T. M., and Coleman, G. Q. (2002). Human-specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb. Cortex 12, 671-691.
79. Raghanti, M. A., Spocter, M. A., Butti, C., Hof, P. R., and Sherwood, C. C. (2010). A comparative perspective on minicolumns and inhibitory GABAergic interneurons in the neocortex. Front. Neuroanat. 4:3. doi: 10.3389/neuro.05.003.2010
80. Raghanti, M. A., Spocter, M. A., Stimpson, C. D., Erwin, J. M., Bonar, C. J., Allman, J. M., Hof, P. R., and Sherwood, C. C. (2009). Species-specific distributions of tyrosine hydroxylase-immunoreactive neurons in the prefrontal cortex of anthropoid primates. Neuroscience 158, 1551-1559.
81. Rakic, P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735.
82. Rakic, S., and Zecevic, N. (2003). Emerging complexity of layer I in human cerebral cortex. Cereb. Cortex 13, 1072-1083.
83. Reep, R. L., Johnson, J. I., Switzer, R. C., and Welker, W. I. (1989). Manatee cerebral cortex: cytoarchitecture of the frontal region in Trichechus manatus latirostris. Brain Behav. Evol. 34, 365-386.
84. Rockel, A. J., Hiorns, R. W., and Powell, T. P. (1980). The basic uniformity in structure of the neocortex. Brain 103, 221-244.
85. Rockland, K. S. (2010). Five points on columns. Front. Neuroanat. 4:22. doi:10.3389/fnana.2010.00022
86. Roth, G., and Dicke, U. (2005). Evolution of the brain and intelligence. Trends Cogn. Sci. (Regul. Ed.) 9, 250-257.
87. Skoglund, T. S., Pascher, R., and Berthold, C. H. (1996). Heterogeneity in the columnar number of neurons in different neocortical areas in the rat. Neurosci. Lett. 208, 97-100.
88. Spitzka, E. A. (1907). A study of the brains of six eminent scientist and scholars belonginig to the american anthropometric society, together with a description of the skull of professor E. D. Cope. (1907). Trans. Am. Soc. 21, 175-308.
89. Spruston, N. (2008). Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9, 206-221.
90. Sterio, J. (1984). The unbiased estimation of number and sizes of arbitrary particles using the dissector. J. Microsc. 134, 127-136.
91. Stolzenburg, J. U., Reichenbach, A., and Neumann, M. (1989). Size and density of glial and neuronal cells within the cerebral neocortex of various insectivorian species. Glia 2, 78-84.
92. Sultan, F. (2002). Analysis of mammalian brain architecture. Nature 415, 133-134.
93. Szentágothai, J. (1975). The 'module-concept' in cerebral cortex architecture. Brain Res. 95, 475-496.
94. Texier, P. J., Porraz, G., Parkington, J., Rigaud, J. P., Poggenpoel, C., Miller, C., Tribolo, C., Cartwright, C., Coudenneau, A., Klein, R., Steele, T., and Verna, C. (2010). A Howiesons Poort tradition of engraving ostrich eggshell containers dated to 60,000 years ago at Diepkloof Rock Shelter, South Africa. Proc. Natl. Acad. Sci. U.S.A. 107, 6180-6185.
95. Trottier, S., Geffard, M., and Evrard, B. (1989). Co-localization of tyrosine hydroxylase and GABA immunoreactivities in human cortical neurons. Neurosci. Lett. 106, 76-82.
96. Valverde, F. (1978). The organization of area 18 in the monkey. A golgi study. Anat. Embryol. 154, 305-334.
97. von Economo, C. (1926). Ein Koeffizient fur die Organisationshohe der Grosshirnrinde. Klin. Wsch. 5, 593-595.
98. Wang, Y., Brzozowska-Prechtl, A., and Karten, H. J. (2010). Laminar and columnar auditory cortex in avian brain. Proc. Natl. Acad. Sci. U.S.A. 107, 12676-12681.
99. Wilder, B. G. (1911). Exhibition of, and preliminary note upon, a brain of about one-half the average size from a white man of ordinary weight and intelligence. J. Nerv. Ment. Dis. 38, 95-97.
100. Xu, Q., de la Cruz, E., and Anderson, S. A. (2003). Cortical interneuron fate determination: diverse sources for distinct subtypes? Cereb. Cortex 13, 670-676.
101. Yopak, K. E., Lisney, T. J., Darlington, R. B., Collin, S. P., Montgomery, J. C., and Finlay, B. L. (2010). A conserved pattern of brain scaling from sharks to primates. Proc. Natl. Acad. Sci. U.S.A. 107, 12946-12951.
102. Yuste, R. (2010). Dendritic Spines. Cambridge, MA: MIT Press.