Mapping Longitudinal Development of Local Cortical Gyrification in Infants from Birth to 2 Years of Age

Human cortical folding is believed to correlate with cognitive functions. This likely correlation may have something to do with why abnormalities of cortical folding have been found in many neurodevelopmental disorders. However, little is known about how cortical gyrification, the cortical folding process, develops in the first 2 years of life, a period of dynamic and regionally heterogeneous cortex growth. In this article, we show how we developed a novel infant-specific method for mapping longitudinal development of local cortical gyrification in infants. By using this method, via 219 longitudinal 3T magnetic resonance imaging scans from 73 healthy infants, we systemically and quantitatively characterized for the first time the longitudinal cortical global gyrification index (GI) and local GI (LGI) development in the first 2 years of life. We found that the cortical GI had age-related and marked development, with 16.1% increase in the first year and 6.6% increase in the second year. We also found marked and regionally heterogeneous cortical LGI development in the first 2 years of life, with the high-growth regions located in the association cortex, whereas the low-growth regions located in sensorimotor, auditory, and visual cortices. Meanwhile, we also showed that LGI growth in most cortical regions was positively correlated with the brain volume growth, which is particularly significant in the prefrontal cortex in the first year. In addition, we observed gender differences in both cortical GIs and LGIs in the first 2 years, with the males having larger GIs than females at 2 years of age. This study provides valuable information on normal cortical folding development in infancy and early childhood.

[1]  Dinggang Shen,et al.  Longitudinal development of cortical thickness, folding, and fiber density networks in the first 2 years of life , 2014, Human brain mapping.

[2]  Dinggang Shen,et al.  Mapping longitudinal hemispheric structural asymmetries of the human cerebral cortex from birth to 2 years of age. , 2014, Cerebral cortex.

[3]  Dinggang Shen,et al.  Measuring the dynamic longitudinal cortex development in infants by reconstruction of temporally consistent cortical surfaces , 2014, NeuroImage.

[4]  Yaozong Gao,et al.  Segmentation of neonatal brain MR images using patch-driven level sets , 2014, NeuroImage.

[5]  J. Gilmore,et al.  Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. , 2013, Cerebral cortex.

[6]  Dinggang Shen,et al.  Development of Cortical Anatomical Properties from Early Childhood to Early Adulthood , 2022 .

[7]  Alex Martin,et al.  Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. , 2013, Brain : a journal of neurology.

[8]  Katrin Amunts,et al.  Development of cortical folding during evolution and ontogeny , 2013, Trends in Neurosciences.

[9]  Guillermo Sapiro,et al.  Geometric computation of human gyrification indexes from magnetic resonance images , 2013, Human brain mapping.

[10]  Lei Wang,et al.  Novel Surface-Smoothing Based Local Gyrification Index , 2013, IEEE Transactions on Medical Imaging.

[11]  J. Gilmore,et al.  Longitudinally guided level sets for consistent tissue segmentation of neonates , 2013, Human brain mapping.

[12]  D. Shen,et al.  DICCCOL: dense individualized and common connectivity-based cortical landmarks. , 2013, Cerebral cortex.

[13]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[14]  Dinggang Shen,et al.  iBEAT: A Toolbox for Infant Brain Magnetic Resonance Image Processing , 2012, Neuroinformatics.

[15]  M. Styner,et al.  Longitudinal development of cortical and subcortical gray matter from birth to 2 years. , 2012, Cerebral cortex.

[16]  P. Liddle,et al.  Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study. , 2012, Journal of psychiatry & neuroscience : JPN.

[17]  Dinggang Shen,et al.  A computational growth model for measuring dynamic cortical development in the first year of life. , 2012, Cerebral cortex.

[18]  Dinggang Shen,et al.  journal homepage: www.elsevier.com/locate/ynimg , 2022 .

[19]  A. Evans,et al.  Development of Cortical Surface Area and Gyrification in Attention-Deficit/Hyperactivity Disorder , 2012, Biological Psychiatry.

[20]  Dinggang Shen,et al.  Consistent reconstruction of cortical surfaces from longitudinal brain MR images , 2012, NeuroImage.

[21]  Dinggang Shen,et al.  Development Trends of White Matter Connectivity in the First Years of Life , 2011, PloS one.

[22]  G. Šimić,et al.  Extraordinary neoteny of synaptic spines in the human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[23]  Armin Raznahan,et al.  How Does Your Cortex Grow? , 2011, The Journal of Neuroscience.

[24]  J. Gilmore,et al.  Infant Brain Atlases from Neonates to 1- and 2-Year-Olds , 2011, PloS one.

[25]  Dinggang Shen,et al.  Brain anatomical networks in early human brain development , 2011, NeuroImage.

[26]  H. Lagercrantz,et al.  The functional architecture of the infant brain as revealed by resting-state fMRI. , 2011, Cerebral cortex.

[27]  Christian Gaser,et al.  The visual cortex in schizophrenia: alterations of gyrification rather than cortical thickness—a combined cortical shape analysis , 2011, Brain Structure and Function.

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

[29]  Moo K. Chung,et al.  General multivariate linear modeling of surface shapes using SurfStat , 2010, NeuroImage.

[30]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.

[31]  Dinggang Shen,et al.  ABSORB: Atlas building by self-organized registration and bundling , 2010, NeuroImage.

[32]  Antonio Y Hardan,et al.  Cortical Gyrification in Autistic and Asperger Disorders: A Preliminary Magnetic Resonance Imaging Study , 2010, Journal of child neurology.

[33]  Nicholas Ayache,et al.  Spherical Demons: Fast Diffeomorphic Landmark-Free Surface Registration , 2010, IEEE Transactions on Medical Imaging.

[34]  Timothy S. Coalson,et al.  A Surface-Based Analysis of Hemispheric Asymmetries and Folding of Cerebral Cortex in Term-Born Human Infants , 2010, The Journal of Neuroscience.

[35]  G. Sapiro,et al.  The development of gyrification in childhood and adolescence , 2010, Brain and Cognition.

[36]  Dinggang Shen,et al.  Neonatal brain image segmentation in longitudinal MRI studies , 2010, NeuroImage.

[37]  Paul M. Thompson,et al.  Mapping the regional influence of genetics on brain structure variability — A Tensor-Based Morphometry study , 2009, NeuroImage.

[38]  Dinggang Shen,et al.  Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects , 2009, Proceedings of the National Academy of Sciences.

[39]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[40]  Rebecca C. Knickmeyer,et al.  A Structural MRI Study of Human Brain Development from Birth to 2 Years , 2008, The Journal of Neuroscience.

[41]  J K Smith,et al.  Functional Connectivity MR Imaging Reveals Cortical Functional Connectivity in the Developing Brain , 2008, American Journal of Neuroradiology.

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

[43]  Eileen Luders,et al.  Mapping the relationship between cortical convolution and intelligence: effects of gender. , 2008, Cerebral cortex.

[44]  Alan C. Evans,et al.  Neurodevelopmental Trajectories of the Human Cerebral Cortex , 2008, The Journal of Neuroscience.

[45]  Milos Judas,et al.  Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. , 2008, Cerebral cortex.

[46]  Meritxell Bach Cuadra,et al.  A Surface-Based Approach to Quantify Local Cortical Gyrification , 2008, IEEE Transactions on Medical Imaging.

[47]  Peter Fransson,et al.  Resting-state networks in the infant brain , 2007, Proceedings of the National Academy of Sciences.

[48]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[49]  Dinggang Shen,et al.  Simulating deformations of MR brain images for validation of atlas-based segmentation and registration algorithms , 2006, NeuroImage.

[50]  Paul M. Thompson,et al.  Increased local gyrification mapped in Williams syndrome , 2006, NeuroImage.

[51]  Dinggang Shen,et al.  Learning-based deformable registration of MR brain images , 2006, IEEE Transactions on Medical Imaging.

[52]  M. Petrides.  Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[54]  K. Worsley,et al.  Unified univariate and multivariate random field theory , 2004, NeuroImage.

[55]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[57]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[58]  Dinggang Shen,et al.  HAMMER: hierarchical attribute matching mechanism for elastic registration , 2002, IEEE Transactions on Medical Imaging.

[59]  I. Aharon,et al.  Three‐dimensional mapping of cortical thickness using Laplace's Equation , 2000, Human brain mapping.

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

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

[62]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[63]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[64]  D. V. van Essen,et al.  Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas , 1997, The Journal of Neuroscience.

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

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

[67]  T. R. Blakeslee,et al.  The Infant Brain , 1891, Hall's journal of health.

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

[69]  P. Goldman-Rakic,et al.  Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. , 1994, Progress in brain research.

[70]  P. Huttenlocher.  Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

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

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

[73]  P. Goldman-Rakic.  Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[74]  M. Phelps,et al.  Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. , 1986, Science.

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

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