Abstract
The idea that the brain is shaped through the interplay of predetermined ontogenetic factors and mechanisms of self-organization has a long tradition in biology, going back to the late-nineteenth century. Here we illustrate the substantial impact of mechanical forces on the development, morphology, and functioning of the primate cerebral cortex. Based on the analysis of quantitative structural data for prefrontal cortices of the adult rhesus monkey, we demonstrate that (1) the characteristic shape of cortical convolutions can be explained by the global minimization of axonal tension in corticocortical projections; (2) mechanical forces resulting from cortical folding have a significant impact on the relative and absolute thickness of cortical layers in gyri and sulci; (3) folding forces may affect the cellular migration during cortical development, resulting in a significantly larger number of neurons in gyral compared to non-gyral regions; and (4) mechanically induced variations of morphology at the cellular level may result in different modes of neuronal functioning in gyri and sulci. These results underscore the significant contribution of mechanical forces during the self-organization of the primate cerebral cortex. Taking such factors into account within a framework of developmental mechanics can lead to a better understanding of how genetic specification, the layout of connections, brain shape as well as brain function are linked in normal and pathologically transformed brains.
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Armstrong E, Curtis M, Buxhoeveden DP, Fregoe C, Zilles K, Casanova MF, McCarthy WF (1991) Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. Cereb Cortex 1:426–432
Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63
Baare WF, Hulshoff Pol HE, Boomsma DI, Posthuma D, de Geus EJ, Schnack HG, van Haren NE, van Oel CJ, Kahn RS (2001) Quantitative genetic modeling of variation in human brain morphology. Cereb Cortex 11:816–824
Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375
Bok ST (1959) Histonomy of the cerebral cortex. Elsevier, Amsterdam
Büchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14:945–951
Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1:86–93
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194
Dombrowski SM, Hilgetag CC, Barbas H (2001) Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb Cortex 11:975–988
Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055
Fischl B, Sereno MI, Dale AM (1999a) Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207
Fischl B, Sereno MI, Tootell RB, Dale AM (1999b) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284
Goldman-Rakic PS, Rakic P (1984) Experimental modification of gyral patterns. In: Geschwind N, Galaburda A (eds) Cerebral dominance. Harvard University Press, Cambridge, pp 179–192
Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B et al. (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Apmis 96:857–881
Hilgetag CC, Barbas H (2002) Contribution of mechanical factors to shaping primate cortical architecture. In: International conference on cognitive and neural systems *02, Boston University
Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179–1209
His W (1874) Unsere Körperform und das physiologische Problem ihrer Entstehung. F. C. W. Vogel, Leipzig
Krichmar JL, Nasuto SJ (2002) The relationship between neuronal shape and neuronal activity. In: Ascoli G (ed) Computational Neuroanatomy. Humana Press, Totowa, pp 105–125
Levitt JG, Blanton RE, Smalley S, Thompson PM, Guthrie D, McCracken JT, Sadoun T, Heinichen L, Toga AW (2003) Cortical sulcal maps in autism. Cereb Cortex 13:728–735
Marin-Padilla M (1992) Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 321:223–240
Mayhew TM, Mwamengele GL, Dantzer V, Williams S (1996) The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development. J Anat 188 (Pt 1):53–58
Miodonski A (1974) The angioarchitectonics and cytoarchitectonics (impregnation modo Golgi-Cox) structure of the fissural frontal neocortex in dog. Folia Biol (Krakow) 22:237–279
Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, Le Bihan D, Cohen L, Dehaene S (2003) Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron 40:847–858
Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383–388
Richman DP, Stewart RM, Hutchinson JW, Caviness VS Jr (1975) Mechanical model of brain convolutional development. Science 189:18–21
Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in the structure of the neocortex. Brain 103:221–244
Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35
Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen VP, Huttunen M, Lonnqvist J, Standertskjold-Nordenstam CG, Kaprio J, Khaledy M, Dail R, Zoumalan CI, Toga AW (2001) Genetic influences on brain structure. Nat Neurosci 4:1253–1258
Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318
Welker W (1990) Why does cerebral cortex fissure and fold? A review of determinants of gyri and sulci. In: Comparative structure and evolution of cerebral cortex, Part II, vol 8B. Plenum, New York, pp 3–136
White T, Andreasen NC, Nopoulos P, Magnotta V (2003) Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biol Psychiatry 54:418–426
Zilles K, Armstrong E, Schleicher A, Kretschmann HJ (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl) 179:173–179
Acknowledgements
We thank Ms. Louise Hurst for carrying out the NEURON simulations depicted in Fig. 4, Mr. Oleg Gusyatin for reconstructing the rhesus monkey brain and globally calculating the thickness of gyral and sulcal cortex, as well as Dr. Basilis Zikopoulos for help with Fig. 3. The research was supported in part by NIH grants from NIMH and NINDS.
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Experiments involving animals were conducted according to the NIH guide for the Care and Use of Laboratory animals (NIH pub. 86–23, revised 1996), and experimental protocols were approved by the IACUC at Boston University School of Medicine., Harvard Medical School., and New England Primate Research Center
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Hilgetag, C.C., Barbas, H. Developmental mechanics of the primate cerebral cortex. Anat Embryol 210, 411–417 (2005). https://doi.org/10.1007/s00429-005-0041-5
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DOI: https://doi.org/10.1007/s00429-005-0041-5