A morphogenetic model for the development of cortical convolutions.

The convolutions of the mammalian cortex are one of its most intriguing characteristics. Their pattern is very distinctive for different species, and there seems to be a remarkable relationship between convolutions and the architectonic and functional regionalization of the cerebral cortex. Yet the mechanisms behind the development of convolutions and their association with the cortical regionalization are poorly understood. Here we propose a morphogenetic model for the development of cortical convolutions based on the structure of the cortex as a closed surface with glial and axonal fibres pulling radially, the fundamental mechanical properties of cortex and fibres (elasticity and plasticity), and the growth of the cortical surface. The computer simulations of this model suggest that convolutions are a natural consequence of cortical growth. The model reproduces several aspects of convolutional development, such as the relationship between cortical surface and brain volume among mammals, the period of compensation in the degree of convolution observed in gyrencephalic brains and the dependence of the degree of convolution on cortical thickness. We have also studied the effect of early cortical regionalization on the development of convolutions by introducing geometric, mechanic and growth asymmetries in the model. The morphogenetic model is thus able to reproduce the gradients in the degree of convolution, the development of primary, secondary and tertiary convolution, and the overproduction of sulci observed in animals with altered afferent cortical connections.

[1]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[2]  D. H. Barron,et al.  An experimental analysis of some factors involved in the development of the fissure pattern of the cerebral cortex , 1950 .

[3]  Fred A. Mettler External Morphology of the Primate Brain , 1950 .

[4]  N. Malamud,et al.  ATLAS OF NEUROPATHOLOGY , 1949, The Ulster Medical Journal.

[5]  N. Rashevsky,et al.  Mathematical biology , 1961, Connecticut medicine.

[6]  W. Welker,et al.  Physiological significance of sulci in somatic sensory cerebral cortex in mammals of the family procyonidae , 1963, The Journal of comparative neurology.

[7]  A. W. Rogers,et al.  The migration of neuroblasts in the developing cerebral cortex. , 1965, Journal of anatomy.

[8]  J. Turner The Central Nervous System , 1970 .

[9]  P. Rakić Guidance of neurons migrating to the fetal monkey neocortex. , 1971, Brain research.

[10]  H. J. Jerison Chapter 9 – Evolution of the Brain in Birds , 1973 .

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

[12]  P. Rakić Prenatal development of the visual system in rhesus monkey. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  F. Gilles,et al.  Gyral development of the human brain. , 1977, Annals of Neurology.

[14]  P. S. Goldman,et al.  Prenatal removal of frontal association cortex in the fetal rhesus monkey: Anatomical and functional consequences in postnatal life , 1978, Brain Research.

[15]  P S Goldman-Rakic,et al.  Morphological consequences of prenatal injury to the primate brain. , 1980, Progress in brain research.

[16]  P. Todd A geometric model for the cortical folding pattern of simple folded brains. , 1982, Journal of theoretical biology.

[17]  H. J. Jerison Allometry, Brain Size, Cortical Surface, and Convolutedness , 1982 .

[18]  I. Smart,et al.  Three dimensional growth of the mouse isocortex. , 1983, Journal of anatomy.

[19]  J. Sundsten,et al.  Folding of the cerebral cortex in mammals. A scaling model. , 1984, Brain, behavior and evolution.

[20]  J. Sundsten,et al.  Folding of the Cerebral Cortex in Mammals , 1984 .

[21]  I. Smart,et al.  Gyrus formation in the cerebral cortex in the ferret. I. Description of the external changes. , 1986, Journal of anatomy.

[22]  I. Smart,et al.  Gyrus formation in the cerebral cortex of the ferret. II. Description of the internal histological changes. , 1986, Journal of anatomy.

[23]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[24]  D. O'Leary,et al.  Do cortical areas emerge from a protocortex? , 1989, Trends in Neurosciences.

[25]  Henry Kennedy,et al.  Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input , 1989, Nature.

[26]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[27]  W. Welker Why Does Cerebral Cortex Fissure and Fold , 1990 .

[28]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[29]  K. Sanderson,et al.  Gradients of neurogenesis in possum neocortex. , 1990, Brain research. Developmental brain research.

[30]  T. O'Shea,et al.  Regional brain morphometry and lissencephaly in the Sirenia. , 1990, Brain, behavior and evolution.

[31]  Hofman Ma The fractal geometry of convoluted brains. , 1991 .

[32]  M A Hofman,et al.  The fractal geometry of convoluted brains. , 1991, Journal fur Hirnforschung.

[33]  H. Killackey,et al.  The effects of bilateral enucleation in the primate fetus on the parcellation of visual cortex. , 1991, Brain research. Developmental brain research.

[34]  P. Rakic Experimental manipulation of cerebral cortical areas in primates. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  M. Gulisano,et al.  Nested expression domains of four homeobox genes in developing rostral brain , 1992, Nature.

[36]  P. Brodal The Central Nervous System , 1992 .

[37]  V. Caviness,et al.  Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model , 1995, Trends in Neurosciences.

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

[39]  A. Schleicher,et al.  Quantitative analysis of gyrification of cerebral cortex in dogs. , 1996, Neurobiology.

[40]  Henry Kennedy,et al.  Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: Effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex , 1996, The Journal of comparative neurology.

[41]  K Amunts,et al.  Quantitative analysis of sulci in the human cerebral cortex: Development, regional heterogeneity, gender difference, asymmetry, intersubject variability and cortical architecture , 1997, Human brain mapping.

[42]  S Chada,et al.  Cytomechanics of neurite outgrowth from chick brain neurons. , 1997, Journal of cell science.

[43]  J. Prothero,et al.  Cortical scaling in mammals: a repeating units model. , 1997, Journal fur Hirnforschung.

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

[45]  P. Levitt,et al.  Patterning and specification of the cerebral cortex. , 1997, Annual review of neuroscience.

[46]  K. Zilles,et al.  Structural divisions and functional fields in the human cerebral cortex 1 Published on the World Wide Web on 20 February 1998. 1 , 1998, Brain Research Reviews.

[47]  P. Rakić,et al.  Changes in cell-cycle kinetics during the development and evolution of primate neocortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  C Marsault,et al.  Are the brains of monozygotic twins similar? A three-dimensional MR study. , 1998, AJNR. American journal of neuroradiology.

[49]  P. Rakić,et al.  Molecular gradients and compartments in the embryonic primate cerebral cortex. , 1999, Cerebral cortex.

[50]  D. O'Leary,et al.  Graded and Areal Expression Patterns of Regulatory Genes and Cadherins in Embryonic Neocortex Independent of Thalamocortical Input , 1999, The Journal of Neuroscience.

[51]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[52]  P. Rakić,et al.  Genetic control of cortical development. , 1999, Cerebral cortex.

[53]  J. Rubenstein,et al.  Early neocortical regionalization in the absence of thalamic innervation. , 1999, Science.

[54]  P. Rakic,et al.  The role of cell death in regulating the size and shape of the mammalian forebrain. , 1999, Cerebral cortex.

[55]  D. O'Leary,et al.  Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. , 2000, Science.

[56]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[57]  C Zhu,et al.  Cell mechanics: mechanical response, cell adhesion, and molecular deformation. , 2000, Annual review of biomedical engineering.

[58]  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.

[59]  D. Price,et al.  Radial migration in the cerebral cortex is enhanced by signals from thalamus , 2001, The European journal of neuroscience.

[60]  H. Kennedy,et al.  Cell-Cycle Kinetics of Neocortical Precursors Are Influenced by Embryonic Thalamic Axons , 2001, The Journal of Neuroscience.

[61]  E. Grove,et al.  Neocortex Patterning by the Secreted Signaling Molecule FGF8 , 2001, Science.

[62]  C. W. Ragsdale,et al.  Patterning the mammalian cerebral cortex , 2001, Current Opinion in Neurobiology.

[63]  S. Pallas Intrinsic and extrinsic factors that shape neocortical specification , 2001, Trends in Neurosciences.

[64]  Mark A. Changizi,et al.  Principles underlying mammalian neocortical scaling , 2001, Biological Cybernetics.

[65]  C. Garel,et al.  Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. , 2001, AJNR. American journal of neuroradiology.

[66]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[67]  P T Fox,et al.  Structure--function spatial covariance in the human visual cortex. , 2001, Cerebral cortex.

[68]  Nancy Andreasen,et al.  Brain volumes and surface morphology in monozygotic twins , 2001, NeuroImage.

[69]  D. O'Leary,et al.  Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex , 2002, Current Opinion in Neurobiology.

[70]  Anjen Chenn,et al.  Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors , 2002, Science.

[71]  J. Chun,et al.  Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding , 2003, Nature Neuroscience.

[72]  L. Krubitzer,et al.  Nature versus nurture revisited: an old idea with a new twist , 2003, Progress in Neurobiology.

[73]  J. Rubenstein,et al.  Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants , 2003, Development.

[74]  Pasko Rakic,et al.  Developmental and evolutionary adaptations of cortical radial glia. , 2003, Cerebral cortex.

[75]  C. Walsh,et al.  Increased neuronal production, enlarged forebrains and cytoarchitectural distortions in beta-catenin overexpressing transgenic mice. , 2003, Cerebral cortex.

[76]  Seong-Seng Tan,et al.  Constructing the mammalian neocortex: the role of intrinsic factors. , 2003, Developmental biology.

[77]  Zoltán Molnár,et al.  Thalamocortical development: how are we going to get there? , 2003, Nature Reviews Neuroscience.

[78]  E. Grove,et al.  Emx2 patterns the neocortex by regulating FGF positional signaling , 2003, Nature Neuroscience.

[79]  William B. Dobyns,et al.  G Protein-Coupled Receptor-Dependent Development of Human Frontal Cortex , 2004, Science.

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

[81]  Pasko Rakic,et al.  Genetic Control of Cortical Convolutions , 2004, Science.

[82]  G. Roth,et al.  Evolution of the brain and intelligence , 2005, Trends in Cognitive Sciences.

[83]  S. Shipp Structure and function of the cerebral cortex , 2007, Current Biology.

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