The human cerebral cortex is neither one nor many: neuronal distribution reveals two quantitatively different zones in the gray matter, three in the white matter, and explains local variations in cortical folding

Imagem de Miniatura
Arquivos
art_GRINBERG_The_human_cerebral_cortex_is_neither_one_nor_2013.PDF (2.95 MB)
Citações na Scopus
61
Tipo de produção
article
Data de publicação
2013
DOI
Scopus
Web of Science
PubMed
Título da Revista
ISSN da Revista
Título do Volume
Editora
FRONTIERS RESEARCH FOUNDATION
Autores
RIBEIRO, Pedro F. M.
VENTURA-ANTUNES, Lissa
GABI, Mariana
MOTA, Bruno
FERRETTI-REBUSTINI, Renata E. L.
HERCULANO-HOUZEL, Suzana
Citação
FRONTIERS IN NEUROANATOMY, v.7, article ID 28, 20p, 2013
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
The human prefrontal cortex has been considered different in several aspects and relatively enlarged compared to the rest of the cortical areas. Here we determine whether the white and gray matter of the prefrontal portion of the human cerebral cortex have similar or different cellular compositions relative to the rest of the cortical regions by applying the Isotropic Fractionator to analyze the distribution of neurons along the entire anteroposterior axis of the cortex, and its relationship with the degree of gyrification, number of neurons under the cortical surface, and other parameters. The prefrontal region shares with the remainder of the cerebral cortex (except for occipital cortex) the same relationship between cortical volume and number of neurons. In contrast, both occipital and prefrontal areas vary from other cortical areas in their connectivity through the white matter, with a systematic reduction of cortical connectivity through the white matter and an increase of the mean axon caliber along the anteroposterior axis. These two parameters explain local differences in the distribution of neurons underneath the cortical surface. We also show that local variations in cortical folding are neither a function of local numbers of neurons nor of cortical thickness, but correlate with properties of the white matter, and are best explained by the folding of the white matter surface. Our results suggest that the human cerebral cortex is divided in two zones (occipital and non-occipital) that differ in how neurons are distributed across their gray matter volume and in three zones (prefrontal, occipital, and non-occipital) that differ in how neurons are connected through the white matter. Thus, the human prefrontal cortex has the largest fraction of neuronal connectivity through the white matter and the smallest average axonal caliber in the white matter within the cortex, although its neuronal composition fits the pattern found for other, non-occipital areas.
Palavras-chave
human, occipital cortex, cortical expansion
URI
https://observatorio.fm.usp.br/handle/OPI/4261
Referências
  1. ABOITIZ F, 1992, BRAIN RES, V598, P143, DOI 10.1016/0006-8993(92)90178-C
  2. Andrews TJ, 1997, J NEUROSCI, V17, P2859
  3. Azevedo FAC, 2009, J COMP NEUROL, V513, P532, DOI 10.1002/cne.21974
  4. BARRES BA, 1994, NEURON, V12, P935, DOI 10.1016/0896-6273(94)90305-0
  5. Bernard A, 2012, NEURON, V73, P1083, DOI 10.1016/j.neuron.2012.03.002
  6. Bishop KM, 2000, SCIENCE, V288, P344, DOI 10.1126/science.288.5464.344
  7. Brodmann Karl, 1912, Anatomischer Anzeiger, V41
  8. Bush EC, 2004, P NATL ACAD SCI USA, V101, P3962, DOI 10.1073/pnas.0305760101
  9. Cahalane DJ, 2012, FRONT NEUROANAT, V6, P1, DOI 10.3389/fnana.2012.00028
  10. Caminiti R, 2009, P NATL ACAD SCI USA, V106, P19551, DOI 10.1073/pnas.0907655106
  11. Chen CH, 2012, SCIENCE, V335, P1634, DOI 10.1126/science.1215330
  12. Collins CE, 2010, P NATL ACAD SCI USA, V107, P15927, DOI 10.1073/pnas.1010356107
  13. Collins CE, 2013, BRAIN STRUCT FUNCT, V218, P805, DOI 10.1007/s00429-012-0430-5
  14. Dehay C, 2007, NAT REV NEUROSCI, V8, P438, DOI 10.1038/nrn2097
  15. de Sousa AA, 2010, J HUM EVOL, V58, P281, DOI 10.1016/j.jhevol.2009.11.011
  16. Elston GN, 2001, J NEUROSCI, V21
  17. Finlay BL, 1998, BRAIN BEHAV EVOLUT, V52, P232, DOI 10.1159/000006566
  18. Fjell AM, 2009, CEREB CORTEX, V19, P2001, DOI 10.1093/cercor/bhn232
  19. FRAHM HD, 1984, J HIRNFORSCH, V25, P537
  20. Fukuchi-Shimogori T, 2001, SCIENCE, V294, P1071, DOI 10.1126/science.1064252
  21. Garel S, 2003, DEVELOPMENT, V130, P1903, DOI 10.1242/dev.00416
  22. Grinberg Lea Tenenholz, 2007, Cell and Tissue Banking, V8, P151, DOI 10.1007/s10561-006-9022-z
  23. HAUG H, 1987, AM J ANAT, V180, P126, DOI 10.1002/aja.1001800203
  24. Herculano-Houzel S, 2011, BRAIN BEHAV EVOLUT, V78, P22, DOI 10.1159/000327318
  25. Herculano-Houzel S, 2012, P NATL ACAD SCI USA, V109, P10661, DOI 10.1073/pnas.1201895109
  26. Herculano-Houzel S, 2008, P NATL ACAD SCI USA, V105, P12593, DOI 10.1073/pnas.0805417105
  27. Herculano-Houzel S, 2007, P NATL ACAD SCI USA, V104, P3562, DOI 10.1073/pnas.0611396104
  28. Herculano-Houzel S, 2006, P NATL ACAD SCI USA, V103, P12138, DOI 10.1073/pnas.0604911103
  29. Herculano-Houzel S, 2005, J NEUROSCI, V25, P2518, DOI 10.1523/JNEUROSCI.4526-04.2005
  30. Herculano-Houzel S, 2011, BRAIN BEHAV EVOLUT, V78, P302, DOI 10.1159/000330825
  31. Herculano-Houzel S, 2009, FRONT HUM NEUROSCI, V3, DOI 10.3389/neuro.09.031.2009
  32. Herculano-Houzel S., 2011, HUMAN NEUROANATOMY, P2
  33. Herculano-Houzel S, 2012, SPRINGER NEUROMETHOD, V67, P391, DOI [10.1007/7657_ 2011_ 13, DOI 10.1007/7657_]
  34. Herculano-Houzel S, 2010, P NATL ACAD SCI USA, V107, P19008, DOI 10.1073/pnas.1012590107
  35. Hilgetag CC, 2006, PLOS COMPUT BIOL, V2, P146, DOI 10.1371/journal.pcbi.0020022
  36. HOFMAN MA, 1985, BRAIN BEHAV EVOLUT, V27, P28, DOI 10.1159/000118718
  37. Jacobs B, 2001, CEREB CORTEX, V11, P558, DOI 10.1093/cercor/11.6.558
  38. JERISON HJ, 1985, PHILOS T ROY SOC B, V308, P21, DOI 10.1098/rstb.1985.0007
  39. Kaas J. H, 2009, ENCY NEUROSCIENCE, P793, DOI 10.1016/B978-008045046-9.00948-7
  40. Kaas J H, 2000, Novartis Found Symp, V228, P188
  41. Karbowski J, 2003, J COMPUT NEUROSCI, V15, P347, DOI 10.1023/A:1027467911225
  42. MARTIN KAC, 1984, J PHYSIOL-LONDON, V356, P291
  43. Mota B, 2012, FRONT NEUROANAT, V6, DOI 10.3389/fnana.2012.00003
  44. MULLEN RJ, 1992, DEVELOPMENT, V116, P201
  45. O'Leary DDM, 2007, NEURON, V56, P252, DOI 10.1016/j.neuron.2007.10.010
  46. OLEARY DDM, 1989, TRENDS NEUROSCI, V12, P400, DOI 10.1016/0166-2236(89)90080-5
  47. Pillay P, 2007, EUR J NEUROSCI, V25, P2705, DOI 10.1111/j.1460-9568.2007.05524.x
  48. Poth C, 2005, BRAIN RES BULL, V66, P357, DOI 10.1016/j.brainresbull.2005.02.001
  49. Prothero J, 1997, J BRAIN RES, V38, P513
  50. RAKIC P, 1988, SCIENCE, V241, P170, DOI 10.1126/science.3291116
  51. Raz N, 2006, NEUROSCI BIOBEHAV R, V30, P730, DOI 10.1016/j.neubiorev.2006.07.001
  52. Rilling JK, 1999, J HUM EVOL, V37, P191, DOI 10.1006/jhev.1999.0313
  53. ROCKEL AJ, 1980, BRAIN, V103, P221, DOI 10.1093/brain/103.2.221
  54. Sansom SN, 2009, CSH PERSPECT BIOL, V1, DOI 10.1101/cshperspect.a002519
  55. Sarko DK, 2009, FRONT NEUROANAT, V3, DOI 10.3389/neuro.05.008.2009
  56. Schoenemann PT, 2005, NAT NEUROSCI, V8, P242, DOI 10.1038/nn1394
  57. Seelke A. M. H, 2012, NEUROSCI ABS, V894
  58. Semendeferi K, 2001, AM J PHYS ANTHROPOL, V114, P224, DOI 10.1002/1096-8644(200103)114:3<224::AID-AJPA1022>3.0.CO;2-I
  59. Semendeferi K, 2002, NAT NEUROSCI, V5, P272, DOI 10.1038/nn814
  60. Smaers JB, 2011, BRAIN BEHAV EVOLUT, V77, P67, DOI 10.1159/000323671
  61. Smaers JB, 2010, PLOS ONE, V5, DOI 10.1371/journal.pone.0009123
  62. STEPHAN H, 1981, FOLIA PRIMATOL, V35, P1, DOI 10.1159/000155963
  63. STOLZENBURG JU, 1989, GLIA, V2, P78, DOI 10.1002/glia.440020203
  64. Teffer K, 2012, PROG BRAIN RES, V195, P191, DOI 10.1016/B978-0-444-53860-4.00009-X
  65. Tomasi S, 2012, CEREB CORTEX, V22, P1463, DOI 10.1093/cercor/bhs011
  66. Welker W., 1990, Cerebral Cortex, V8B, P3
  67. Winkler AM, 2010, NEUROIMAGE, V53, P1135, DOI 10.1016/j.neuroimage.2009.12.028
  68. Zhang K, 2000, P NATL ACAD SCI USA, V97, P5621, DOI 10.1073/pnas.090504197
  69. ZILLES K, 1988, ANAT EMBRYOL, V179, P173, DOI 10.1007/BF00304699

Coleções
Artigos e Materiais de Revistas Científicas - FM/MPT
Artigos e Materiais de Revistas Científicas - FM/MCM
Artigos e Materiais de Revistas Científicas - HC/ICHC
Artigos e Materiais de Revistas Científicas - LIM/22