Development of human brain structural networks through infancy and childhood.

During human brain development through infancy and childhood, microstructural and macrostructural changes take place to reshape the brain's structural networks and better adapt them to sophisticated functional and cognitive requirements. However, structural topological configuration of the human brain during this specific development period is not well understood. In this study, diffusion magnetic resonance image (dMRI) of 25 neonates, 13 toddlers, and 25 preadolescents were acquired to characterize network dynamics at these 3 landmark cross-sectional ages during early childhood. dMRI tractography was used to construct human brain structural networks, and the underlying topological properties were quantified by graph-theory approaches. Modular organization and small-world attributes are evident at birth with several important topological metrics increasing monotonically during development. Most significant increases of regional nodes occur in the posterior cingulate cortex, which plays a pivotal role in the functional default mode network. Positive correlations exist between nodal efficiencies and fractional anisotropy of the white matter traced from these nodes, while correlation slopes vary among the brain regions. These results reveal substantial topological reorganization of human brain structural networks through infancy and childhood, which is likely to be the outcome of both heterogeneous strengthening of the major white matter tracts and pruning of other axonal fibers.

[1]  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.

[2]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[4]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

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

[6]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[7]  T. Prescott,et al.  The brainstem reticular formation is a small-world, not scale-free, network , 2006, Proceedings of the Royal Society B: Biological Sciences.

[8]  G. Vogel Mysteries of the brain. Can we make our brains more plastic? , 2012, Science.

[9]  M. L. Pucak,et al.  Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex , 1997, Neuroscience.

[10]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[11]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

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

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

[14]  P. Rakić,et al.  Axon overproduction and elimination in the anterior commissure of the developing rhesus monkey , 1994, The Journal of comparative neurology.

[15]  Daniel P. Kennedy,et al.  Mapping Early Brain Development in Autism , 2007, Neuron.

[16]  Lars T Westlye,et al.  Intellectual abilities and white matter microstructure in development: A diffusion tensor imaging study , 2010, Human brain mapping.

[17]  G M Innocenti,et al.  Growth and reshaping of axons in the establishment of visual callosal connections. , 1981, Science.

[18]  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.

[19]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[20]  M. Horsfield,et al.  Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[21]  Talma Hendler,et al.  Abnormal white matter integrity in young children with autism , 2011, Human brain mapping.

[22]  F. Turkheimer,et al.  Emergence of resting state networks in the preterm human brain , 2010, Proceedings of the National Academy of Sciences.

[23]  J. Soares,et al.  A preliminary investigation of corpus callosum and anterior commissure aberrations in aggressive youth with bipolar disorders. , 2012, Journal of child and adolescent psychopharmacology.

[24]  Yong He,et al.  Graph theoretical modeling of brain connectivity. , 2010, Current opinion in neurology.

[25]  Christian Beaulieu,et al.  Diffusion tensor imaging of neurodevelopment in children and young adults , 2005, NeuroImage.

[26]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

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

[28]  Rebecca C. Knickmeyer,et al.  Regional Gray Matter Growth, Sexual Dimorphism, and Cerebral Asymmetry in the Neonatal Brain , 2007, The Journal of Neuroscience.

[29]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

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

[31]  R. Gur,et al.  Age-related volumetric changes of brain gray and white matter in healthy infants and children. , 2001, Cerebral cortex.

[32]  P. Rakić,et al.  Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Takahiro Furuta,et al.  Inhibitory Gating of Vibrissal Inputs in the Brainstem , 2008, The Journal of Neuroscience.

[34]  K. Hwang,et al.  The development of hub architecture in the human functional brain network. , 2013, Cerebral cortex.

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

[36]  R. Guimerà,et al.  Modularity from fluctuations in random graphs and complex networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[38]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[39]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[40]  E. Bullmore,et al.  The Convergence of Maturational Change and Structural Covariance in Human Cortical Networks , 2013, The Journal of Neuroscience.

[41]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[42]  Khader M Hasan,et al.  Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. , 2007, Cerebral cortex.

[43]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[44]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[45]  Alan C. Evans,et al.  Uncovering Intrinsic Modular Organization of Spontaneous Brain Activity in Humans , 2009, PloS one.

[46]  L. Lotspeich,et al.  White matter structure in autism: preliminary evidence from diffusion tensor imaging , 2004, Biological Psychiatry.

[47]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[48]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[49]  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.

[50]  Patricia Gruner,et al.  White matter development in adolescence: diffusion tensor imaging and meta-analytic results. , 2012, Schizophrenia bulletin.

[51]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[52]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[53]  Hao Huang,et al.  White and gray matter development in human fetal, newborn and pediatric brains , 2006, NeuroImage.

[54]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[55]  O. Sporns,et al.  Identification and Classification of Hubs in Brain Networks , 2007, PloS one.

[56]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[58]  R. Buckner,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.2 Self-projection and the brain , 2022 .

[59]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[60]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[61]  E. Bullmore,et al.  Imaging structural co-variance between human brain regions , 2013, Nature Reviews Neuroscience.

[62]  Jonathan D. Power,et al.  The Development of Human Functional Brain Networks , 2010, Neuron.

[63]  O. Sporns,et al.  White matter maturation reshapes structural connectivity in the late developing human brain , 2010, Proceedings of the National Academy of Sciences.

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

[65]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[66]  C. Nelson,et al.  Handbook of Developmental Cognitive Neuroscience , 2001 .

[67]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[68]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

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

[70]  D. Sharp,et al.  The role of the posterior cingulate cortex in cognition and disease. , 2014, Brain : a journal of neurology.

[71]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[72]  Dennis Drotar A Young Mind in a Growing Brain , 2007 .

[73]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[74]  Giorgio M. Innocenti,et al.  Exuberance in the development of cortical networks , 2005, Nature Reviews Neuroscience.

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

[76]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[77]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

[78]  J. Lerch,et al.  Patterns of Coordinated Anatomical Change in Human Cortical Development: A Longitudinal Neuroimaging Study of Maturational Coupling , 2011, Neuron.

[79]  H. Kinney,et al.  Myelination in the developing human brain: Biochemical correlates , 1994, Neurochemical Research.

[80]  Yong He,et al.  Sex- and brain size-related small-world structural cortical networks in young adults: a DTI tractography study. , 2011, Cerebral cortex.

[81]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[82]  J. Fawcett,et al.  Regressive events in neurogenesis. , 1984, Science.

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

[84]  Leon Danon,et al.  Comparing community structure identification , 2005, cond-mat/0505245.

[85]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[86]  Alan C. Evans,et al.  Callosal fiber length and interhemispheric connectivity in adults with autism: Brain overgrowth and underconnectivity , 2012, Human brain mapping.

[87]  Massimo Marchiori,et al.  Error and attacktolerance of complex network s , 2004 .