Mechanical morphogenesis and the development of neocortical organisation

The development and evolution of complex neocortical organisations is thought to result from the interaction of genetic and activity-dependent processes. Here we propose that a third type of process – mechanical morphogenesis – may also play an important role. We review recent theoretical and experimental results in non-linear physics showing how homogeneous growth can produce a rich variety of forms, in particular neocortical folding. The mechanical instabilities that produce these forms also induce heterogeneous patterns of stress at the scale of the organ. We review the evidence showing how these stresses can influence cell proliferation, migration and apoptosis, cell differentiation and shape, migration and axonal guidance, and could thus be able to influence regional neocortical identity and connectivity.

[1]  J. Lefévre,et al.  A reaction-diffusion model of the human brain development , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[2]  Amir Ayali,et al.  The regulative role of neurite mechanical tension in network development. , 2009, Biophysical journal.

[3]  Dennis Velakoulis,et al.  Morphology of the paracingulate sulcus and executive cognition in schizophrenia , 2006, Schizophrenia Research.

[4]  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.

[5]  Luka Pocivavsek,et al.  Beyond Wrinkles: Stress and Fold Localization in Thin Elastic Membranes , 2008 .

[6]  Leah Krubitzer,et al.  In Search of a Unifying Theory of Complex Brain Evolution , 2009, Annals of the New York Academy of Sciences.

[7]  Jean-Francois Mangin,et al.  Larger is twistier: Spectral analysis of gyrification (SPANGY) applied to adult brain size polymorphism , 2012, NeuroImage.

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

[9]  Y. Samson,et al.  "Sulcal root" generic model: a hypothesis to overcome the variability of the human cortex folding patterns. , 2005, Neurologia medico-chirurgica.

[10]  Jacques Prost,et al.  Supplements to : Isotropic stress reduces cell proliferation in tumor spheroids , 2011 .

[11]  Matthias P. Lutolf,et al.  Designing materials to direct stem-cell fate , 2009, Nature.

[12]  K. Franze The mechanical control of nervous system development , 2013, Development.

[13]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[14]  S. Sen,et al.  Matrix Elasticity Directs Stem Cell Lineage Specification , 2006, Cell.

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

[16]  Federico Calegari,et al.  Regulation of cerebral cortex size and folding by expansion of basal progenitors , 2013, The EMBO journal.

[17]  Xi-Qiao Feng,et al.  Effects of internal pressure and surface tension on the growth-induced wrinkling of mucosae. , 2014, Journal of the mechanical behavior of biomedical materials.

[18]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

[19]  George M. Whitesides,et al.  Spontaneous formation of ordered structures in thin films of metals supported on an elastomeric polymer , 1998, Nature.

[20]  Luca Muzio,et al.  Area identity shifts in the early cerebral cortex of Emx2−/− mutant mice , 2000, Nature Neuroscience.

[21]  Jochen Guck,et al.  Viscoelastic properties of individual glial cells and neurons in the CNS , 2006, Proceedings of the National Academy of Sciences.

[22]  Korbinian Brodmann,et al.  Brodmann's localization in the cerebral cortex : the principles of comparative localisation in the cerebral cortex based on cytoarchitectonics , 2006 .

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

[24]  A W Roe,et al.  Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[26]  Lisa A Flanagan,et al.  Neurite branching on deformable substrates , 2002, Neuroreport.

[27]  Leah Krubitzer,et al.  The Magnificent Compromise: Cortical Field Evolution in Mammals , 2007, Neuron.

[28]  Roberto Toro,et al.  On the Possible Shapes of the Brain , 2012, Evolutionary Biology.

[29]  L. Puelles Plan of the Developing Vertebrate Nervous System: Relating Embryology to the Adult Nervous System (Prosomere Model, Overview of Brain Organization) , 2013 .

[30]  P. Ciarletta,et al.  Buckling instability in growing tumor spheroids. , 2013, Physical review letters.

[31]  J. R. Newton,et al.  Acceleration of visually cued conditioned fear through the auditory pathway , 2004, Nature Neuroscience.

[32]  H. Barbas,et al.  Developmental mechanics of the primate cerebral cortex , 2005, Anatomy and Embryology.

[33]  M. A. García-Cabezas,et al.  A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. , 2011, Cerebral cortex.

[34]  A. McCulloch,et al.  Stress-dependent finite growth in soft elastic tissues. , 1994, Journal of biomechanics.

[35]  M. Sur,et al.  Deletion of Ten-m3 induces the formation of eye dominance domains in mouse visual cortex. , 2013, Cerebral cortex.

[36]  S. Pääbo,et al.  Great ape DNA sequences reveal a reduced diversity and an expansion in humans , 2001, Nature Genetics.

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

[38]  M. Sur,et al.  Visual behaviour mediated by retinal projections directed to the auditory pathway , 2000, Nature.

[39]  M. Sur,et al.  A map of visual space induced in primary auditory cortex. , 1990, Science.

[40]  T. Paus,et al.  Brain size and folding of the human cerebral cortex. , 2008, Cerebral cortex.

[41]  Luis Puelles,et al.  Forebrain Development: Prosomere Model , 2009 .

[42]  Roberto Toro,et al.  Geometric atlas: modeling the cortex as an organized surface , 2003, NeuroImage.

[43]  T. Tallinen,et al.  Gyrification from constrained cortical expansion , 2014, Proceedings of the National Academy of Sciences.

[44]  R. Turner,et al.  Microstructural Parcellation of the Human Cerebral Cortex: From Brodmann's Post-Mortem Map to in Vivo Mapping with High-Field Magnetic Resonance Imaging , 2013 .

[45]  Albert J. Keung,et al.  Substrate modulus directs neural stem cell behavior. , 2008, Biophysical journal.

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

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

[48]  T. Saif,et al.  Mechanical Tension Modulates Local and Global Vesicle Dynamics in Neurons , 2012, Cellular and molecular bioengineering.

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

[50]  Paul C. Fletcher,et al.  From genes to folds: a review of cortical gyrification theory , 2014, Brain Structure and Function.

[51]  J. Joanny,et al.  Instabilities of monolayered epithelia: shape and structure of villi and crypts. , 2011, Physical review letters.

[52]  Philip V. Bayly,et al.  Residual stress in the adult mouse brain , 2009, Biomechanics and modeling in mechanobiology.

[53]  R. Jain,et al.  Micro-Environmental Mechanical Stress Controls Tumor Spheroid Size and Morphology by Suppressing Proliferation and Inducing Apoptosis in Cancer Cells , 2009, PloS one.

[54]  Paul Steinmann,et al.  The role of mechanics during brain development. , 2014, Journal of the mechanics and physics of solids.

[55]  Magdalena Götz,et al.  Role of radial glial cells in cerebral cortex folding , 2014, Current Opinion in Neurobiology.

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

[57]  John L.R. Rubenstein,et al.  Patterning and Cell Type Specification in the Developing CNS and PNS , 2013 .

[58]  Camino de Juan Romero,et al.  Discrete domains of gene expression in germinal layers distinguish the development of gyrencephaly , 2015, The EMBO journal.

[59]  L. Mahadevan,et al.  Geometry and physics of wrinkling. , 2003, Physical review letters.

[60]  A. Kriegstein,et al.  Neurogenic radial glia in the outer subventricular zone of human neocortex , 2010, Nature.

[61]  L. Taber,et al.  Axons pull on the brain, but tension does not drive cortical folding. , 2010, Journal of biomechanical engineering.

[62]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[63]  M. Law,et al.  Eye-specific termination bands in tecta of three-eyed frogs. , 1978, Science.

[64]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[65]  Y. Burnod,et al.  A morphogenetic model for the development of cortical convolutions. , 2005, Cerebral cortex.

[66]  P V Bayly,et al.  A cortical folding model incorporating stress-dependent growth explains gyral wavelengths and stress patterns in the developing brain , 2013, Physical biology.

[67]  Magdalena Götz,et al.  Trnp1 Regulates Expansion and Folding of the Mammalian Cerebral Cortex by Control of Radial Glial Fate , 2013, Cell.

[68]  J. Bourgeois,et al.  Synaptogenesis, heterochrony and epigenesis in the mammalian neocortex , 1997, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[69]  L. Mahadevan,et al.  Unfolding the sulcus. , 2010, Physical review letters.

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

[71]  M. Trejo,et al.  Petal shapes of sympetalous flowers: the interplay between growth, geometry and elasticity , 2012 .

[72]  Dennis Velakoulis,et al.  Individual differences in anterior cingulate/paracingulate morphology are related to executive functions in healthy males. , 2004, Cerebral cortex.

[73]  J. Kaas Evolution of columns, modules, and domains in the neocortex of primates , 2012, Proceedings of the National Academy of Sciences.

[74]  Marion Ghibaudo,et al.  Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates , 2007, Proceedings of the National Academy of Sciences.

[75]  Benny Davidovitch,et al.  Prototypical model for tensional wrinkling in thin sheets , 2011, Proceedings of the National Academy of Sciences.

[76]  B. Fischl Estimating the Location of Brodmann Areas from Cortical Folding Patterns Using Histology and Ex Vivo MRI , 2013 .

[77]  P. Rakic,et al.  Decision by division: making cortical maps , 2009, Trends in Neurosciences.

[78]  Tadashi Hamasaki,et al.  EMX2 Regulates Sizes and Positioning of the Primary Sensory and Motor Areas in Neocortex by Direct Specification of Cortical Progenitors , 2004, Neuron.

[79]  E. Kuhl,et al.  A mechanical model predicts morphological abnormalities in the developing human brain , 2014, Scientific Reports.

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

[81]  R. Rivlin Large elastic deformations of isotropic materials IV. further developments of the general theory , 1948, Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences.

[82]  Sophia Mã ¶ ller,et al.  Biomechanics — Mechanical properties of living tissue , 1982 .

[83]  Gary F. Egan,et al.  Biomechanisms for modelling cerebral cortical folding , 2009, Medical Image Anal..

[84]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[85]  Dennis D.M. O'Leary,et al.  Chapter 4 – Area Patterning of the Mammalian Cortex , 2013 .

[86]  Alessandra Angelucci,et al.  Induction of visual orientation modules in auditory cortex , 2000, Nature.

[87]  R. Rivlin Large Elastic Deformations of Isotropic Materials , 1997 .

[88]  D. Bray,et al.  Axonal growth in response to experimentally applied mechanical tension. , 1984, Developmental biology.