Coevolution of gyral folding and structural connection patterns in primate brains.

Both cortical folding and structural connection patterns are more elaborated during the evolution of primate neocortex. For instance, cortical gyral shapes and structural connection patterns in humans are more complex and variable than those in chimpanzees and macaques. However, the intrinsic relationship between gyral folding and structural connection and their coevolution patterns across primates remain unclear. Here, our qualitative and quantitative analyses of in vivo diffusion tensor imaging (DTI) and structural magnetic resonance imaging (MRI) data consistently demonstrate that structural fiber connection patterns closely follow gyral folding patterns in the direction "tangent" to the cortical sphere, and this close relationship is well preserved in the neocortices of macaque, chimpanzee, and human brains, despite the progressively increasing complexity and variability of cortical folding and structural connection patterns. The findings suggest a hypothesis that a common axonal fiber pushing mechanism sculpts the curved patterns of gyri in the tangent direction during primate brain evolution. Our DTI/MRI data analysis provides novel insights into the structural architecture of primate brains, a new viewpoint of the relationship between cortical morphology and connection, and a basis for future elucidation of the functional implication of coevolution of cortical folding and structural connection patterns.

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

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

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

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

[5]  T. Insel,et al.  The primate neocortex in comparative perspective using magnetic resonance imaging. , 1999, Journal of human evolution.

[6]  James K Rilling,et al.  A quantitative morphometric comparative analysis of the primate temporal lobe. , 2002, Journal of human evolution.

[7]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

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

[9]  M. Sur,et al.  Patterning and Plasticity of the Cerebral Cortex , 2005, Science.

[10]  T. Deacon Fallacies of progression in theories of brain-size evolution , 1990, International Journal of Primatology.

[11]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[12]  E. Grove,et al.  Area and layer patterning in the developing cerebral cortex , 2006, Current Opinion in Neurobiology.

[13]  P. Schoenemann Evolution of the Size and Functional Areas of the Human Brain , 2006 .

[14]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[15]  Lei Guo,et al.  Brain tissue segmentation based on DTI data , 2007, NeuroImage.

[16]  Stephen T. C. Wong,et al.  Reconstruction of central cortical surface from brain MRI images: Method and application , 2007, NeuroImage.

[17]  Timothy E. J. Behrens,et al.  The evolution of the arcuate fasciculus revealed with comparative DTI , 2008, Nature Neuroscience.

[18]  Gil U. Lee,et al.  Topography and nanomechanics of live neuronal growth cones analyzed by atomic force microscopy. , 2009, Biophysical journal.

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

[20]  Karl J. Friston Modalities, Modes, and Models in Functional Neuroimaging , 2009, Science.

[21]  P. Rakic Evolution of the neocortex: Perspective from developmental biology , 2010 .

[22]  Lei Guo,et al.  Gyral folding pattern analysis via surface profiling , 2010, NeuroImage.

[23]  Lei Guo,et al.  A computational model of cerebral cortex folding. , 2010, Journal of theoretical biology.

[24]  Lei Guo,et al.  An automated pipeline for cortical sulcal fundi extraction , 2010, Medical Image Anal..

[25]  Degang Zhang,et al.  Automatic cortical surface parcellation based on fiber density information , 2010, 2010 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[26]  Paul M. Thompson,et al.  On the Genetic Architecture of Cortical Folding and Brain Volume in Primates , 2022 .

[27]  Arthur W. Toga,et al.  A web-based brain atlas of the vervet monkey, Chlorocebus aethiops , 2011, NeuroImage.

[28]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[29]  Degang Zhang,et al.  Discovering Dense and Consistent Landmarks in the Brain , 2011, IPMI.

[30]  Degang Zhang,et al.  Optimization of functional brain ROIs via maximization of consistency of structural connectivity profiles , 2011, ISBI.

[31]  Daniel P. Kennedy,et al.  Intact Bilateral Resting-State Networks in the Absence of the Corpus Callosum , 2011, The Journal of Neuroscience.

[32]  Dinggang Shen,et al.  Axonal fiber terminations concentrate on gyri. , 2012, Cerebral cortex.

[33]  Tarik F Haydar,et al.  The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. , 2012, Cerebral cortex.

[34]  Degang Zhang,et al.  Optimization of functional brain ROIs via maximization of consistency of structural connectivity profiles , 2011, NeuroImage.