Longitudinal development of cortical thickness, folding, and fiber density networks in the first 2 years of life

Quantitatively characterizing the development of cortical anatomical networks during the early stage of life plays an important role in revealing the relationship between cortical structural connection and high‐level functional development. The development of correlation networks of cortical‐thickness, cortical folding, and fiber‐density is systematically analyzed in this article to study the relationship between different anatomical properties during the first 2 years of life. Specifically, longitudinal MR images of 73 healthy subjects from birth to 2 year old are used. For each subject at each time point, its measures of cortical thickness, cortical folding, and fiber density are projected to its cortical surface that has been partitioned into 78 cortical regions. Then, the correlation matrices for cortical thickness, cortical folding, and fiber density at each time point can be constructed, respectively, by computing the inter‐regional Pearson correlation coefficient (of any pair of ROIs) across all 73 subjects. Finally, the presence/absence pattern (i.e., binary pattern) of the connection network is constructed from each inter‐regional correlation matrix, and its statistical and anatomical properties are adopted to analyze the longitudinal development of anatomical networks. The results show that the development of anatomical network could be characterized differently by using different anatomical properties (i.e., using cortical thickness, cortical folding, or fiber density). Hum Brain Mapp 35:3726–3737, 2014. © 2013 Wiley Periodicals, Inc.

[1]  C. J. Stam,et al.  Functional connectivity patterns of human magnetoencephalographic recordings: a ‘small-world’ network? , 2004, Neuroscience Letters.

[2]  P. Ellen Grant,et al.  A methodology for analyzing curvature in the developing brain from preterm to adult , 2008, Int. J. Imaging Syst. Technol..

[3]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[4]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

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

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

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

[8]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[9]  Dinggang Shen,et al.  Altered Structural Connectivity in Neonates at Genetic Risk for Schizophrenia: a Combined Study Using Morphological and White Matter Networks , 2022 .

[10]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[11]  Lei Guo,et al.  A Computational Model of Cerebral Cortex Folding , 2009, MICCAI.

[12]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

[13]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[14]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[15]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[16]  Colin Studholme,et al.  Comparing 3D Gyrification Index and area-independent curvature-based measures in quantifying neonatal brain folding , 2007, SPIE Medical Imaging.

[17]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

[18]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[19]  Lei Guo,et al.  Automatic cortical sulcal parcellation based on surface principal direction flow field tracking , 2009, NeuroImage.

[20]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[21]  Alan C. Evans,et al.  Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI , 2006, NeuroImage.

[22]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[23]  Alan C. Evans,et al.  Comparing functional connectivity via thresholding correlations and singular value decomposition , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[25]  Wenbin Li,et al.  Enriched white matter connectivity networks for accurate identification of MCI patients , 2011, NeuroImage.

[26]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

[27]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[28]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

[29]  C. Stam,et al.  Small-world networks and functional connectivity in Alzheimer's disease. , 2006, Cerebral cortex.

[30]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

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

[32]  Andrea J. van Doorn,et al.  Surface shape and curvature scales , 1992, Image Vis. Comput..

[33]  Dinggang Shen,et al.  Temporal and Spatial Evolution of Brain Network Topology during the First Two Years of Life , 2011, PloS one.

[34]  C. Stam,et al.  Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis , 2006, Neuroscience Letters.

[35]  I. Scheffer,et al.  Genetic and neuroradiological heterogeneity of double cortex syndrome , 2000, Annals of neurology.

[36]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[37]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

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

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

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

[41]  Dinggang Shen,et al.  Altered Modular Organization of Structural Cortical Networks in Children with Autism , 2013, PloS one.

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

[43]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[44]  Alan C. Evans,et al.  Age- and Gender-Related Differences in the Cortical Anatomical Network , 2009, The Journal of Neuroscience.

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

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

[47]  Dinggang Shen,et al.  Accurate and Consistent 4D Segmentation of Serial Infant Brain MR Images , 2011, MBIA.

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

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

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

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

[52]  Alan C. Evans,et al.  Convergence and divergence of thickness correlations with diffusion connections across the human cerebral cortex , 2012, NeuroImage.

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