Developmental mechanics of the primate cerebral cortex

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.

[1]  S. Bok Histonomy of the cerebral cortex , 1959 .

[2]  P. Rakić,et al.  Neuronal migration, with special reference to developing human brain: a review. , 1973, Brain research.

[3]  A. Miodoński The angioarchitectonics and cytoarchitectonics (impregnation modo Golgi-Cox) structure of the fissural frontal neocortex in dog. , 1974, Folia biologica.

[4]  V. Caviness,et al.  Mechanical model of brain convolutional development. , 1975, Science.

[5]  F. Gilles,et al.  Gyral development of the human brain , 1977, Transactions of the American Neurological Association.

[6]  T. Powell,et al.  The basic uniformity in structure of the neocortex. , 1980, Brain : a journal of neurology.

[7]  H. J. G. Gundersen,et al.  The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis , 1988, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[8]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[9]  K Zilles,et al.  Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. , 1991, Cerebral cortex.

[10]  M Marín-Padilla,et al.  Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory , 1992, The Journal of comparative neurology.

[11]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[12]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[13]  T M Mayhew,et al.  The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development. , 1996, Journal of anatomy.

[14]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[15]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[16]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[17]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[18]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[19]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C C Hilgetag,et al.  Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. , 2001, Cerebral cortex.

[21]  R. Kahn,et al.  Quantitative genetic modeling of variation in human brain morphology. , 2001, Cerebral cortex.

[22]  Tyrone D. Cannon,et al.  Genetic influences on brain structure , 2001, Nature Neuroscience.

[23]  Jeffrey L. Krichmar,et al.  The Relationship Between Neuronal Shape and Neuronal Activity , 2002 .

[24]  Arthur W Toga,et al.  Cortical sulcal maps in autism. , 2003, Cerebral cortex.

[25]  S. Dehaene,et al.  Functional and Structural Alterations of the Intraparietal Sulcus in a Developmental Dyscalculia of Genetic Origin , 2003, Neuron.

[26]  N. Andreasen,et al.  Gyrification abnormalities in childhood- and adolescent-onset schizophrenia , 2003, Biological Psychiatry.

[27]  C. Büchel,et al.  White matter asymmetry in the human brain: a diffusion tensor MRI study. , 2004, Cerebral cortex.

[28]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[29]  W. Welker,et al.  Why Does Cerebral Cortex Fissure and Fold ? A Review of Determinants of Gyri and Sulci , 2022 .