Structural and Maturational Covariance in Early Childhood Brain Development

Abstract Brain structural covariance networks (SCNs) composed of regions with correlated variation are altered in neuropsychiatric disease and change with age. Little is known about the development of SCNs in early childhood, a period of rapid cortical growth. We investigated the development of structural and maturational covariance networks, including default, dorsal attention, primary visual and sensorimotor networks in a longitudinal population of 118 children after birth to 2 years old and compared them with intrinsic functional connectivity networks. We found that structural covariance of all networks exhibit strong correlations mostly limited to their seed regions. By Age 2, default and dorsal attention structural networks are much less distributed compared with their functional maps. The maturational covariance maps, however, revealed significant couplings in rates of change between distributed regions, which partially recapitulate their functional networks. The structural and maturational covariance of the primary visual and sensorimotor networks shows similar patterns to the corresponding functional networks. Results indicate that functional networks are in place prior to structural networks, that correlated structural patterns in adult may arise in part from coordinated cortical maturation, and that regional co‐activation in functional networks may guide and refine the maturation of SCNs over childhood development.

[1]  Wei Gao,et al.  Functional Network Development During the First Year: Relative Sequence and Socioeconomic Correlations. , 2015, Cerebral cortex.

[2]  J. Gilmore,et al.  Dynamic Development of Regional Cortical Thickness and Surface Area in Early Childhood. , 2015, Cerebral cortex.

[3]  B. Harrison,et al.  Discrete Alterations of Brain Network Structural Covariance in Individuals at Ultra-High Risk for Psychosis , 2015, Biological Psychiatry.

[4]  P. Gluckman,et al.  Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants , 2015, Translational Psychiatry.

[5]  Angela R. Laird,et al.  Comparison of structural covariance with functional connectivity approaches exemplified by an investigation of the left anterior insula , 2014, NeuroImage.

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

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

[8]  Alan C. Evans Networks of anatomical covariance , 2013, NeuroImage.

[9]  Bruce Fischl,et al.  Genetic topography of brain morphology , 2013, Proceedings of the National Academy of Sciences.

[10]  Y. Saalmann,et al.  Functional and structural architecture of the human dorsal frontoparietal attention network , 2013, Proceedings of the National Academy of Sciences.

[11]  Alan C. Evans,et al.  Developmental changes in organization of structural brain networks. , 2013, Cerebral cortex.

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

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

[14]  Shuyu Li,et al.  Age-related changes in brain structural covariance networks , 2013, Front. Hum. Neurosci..

[15]  Dinggang Shen,et al.  Cerebral Cortex doi:10.1093/cercor/bhs043 Cerebral Cortex Advance Access published February 24, 2012 The Synchronization within and Interaction between the Default and Dorsal Attention Networks in Early Infancy , 2022 .

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

[17]  Jean-François Gagnon,et al.  The impact of aging on gray matter structural covariance networks , 2012, NeuroImage.

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

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

[20]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

[21]  Martin Styner,et al.  Quantitative tract-based white matter development from birth to age 2years , 2012, NeuroImage.

[22]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

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

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

[25]  Anders M. Dale,et al.  Genetic Influences on Cortical Regionalization in the Human Brain , 2011, Neuron.

[26]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

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

[28]  J. Piven,et al.  Early brain overgrowth in autism associated with an increase in cortical surface area before age 2 years. , 2011, Archives of general psychiatry.

[29]  Yong He,et al.  Age-related alterations in the modular organization of structural cortical network by using cortical thickness from MRI , 2011, NeuroImage.

[30]  G. Rees,et al.  The structural basis of inter-individual differences in human behaviour and cognition , 2011, Nature Reviews Neuroscience.

[31]  Yihong Yang,et al.  Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity , 2010, NeuroImage.

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

[33]  Efstathios D. Gennatas,et al.  Network-level structural covariance in the developing brain , 2010, Proceedings of the National Academy of Sciences.

[34]  Martin Styner,et al.  Prenatal and Neonatal Brain Structure and White Matter Maturation in Children at High Risk for Schizophrenia AJP in Advance , 2010 .

[35]  Bill Seeley,et al.  Neurodegenerative diseases target large-scale human brain networks , 2010, Alzheimer's & Dementia.

[36]  Rebecca C. Knickmeyer,et al.  Maturational trajectories of cortical brain development through the pubertal transition: unique species and sex differences in the monkey revealed through structural magnetic resonance imaging. , 2010, Cerebral cortex.

[37]  Anders M. Dale,et al.  Cortical Thickness Is Influenced by Regionally Specific Genetic Factors , 2010, Biological Psychiatry.

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

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

[41]  N. Kabani,et al.  Identification of genetically mediated cortical networks: a multivariate study of pediatric twins and siblings. , 2008, Cerebral cortex.

[42]  Alan C. Evans,et al.  Structural Insights into Aberrant Topological Patterns of Large-Scale Cortical Networks in Alzheimer's Disease , 2008, The Journal of Neuroscience.

[43]  S. Blakemore The social brain in adolescence , 2008, Nature Reviews Neuroscience.

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

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

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

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

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

[49]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Karl J. Friston,et al.  Structural Covariance in the Human Cortex , 2005, The Journal of Neuroscience.

[51]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[53]  John Suckling,et al.  For personal use. Only reproduce with permission from The Lancet Publishing Group. Effect of sunlight and season on serotonin turnover in the brain , 2002 .

[54]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[55]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[56]  J. Colombo The development of visual attention in infancy. , 2001, Annual review of psychology.

[57]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Karl J. Friston,et al.  Mapping of grey matter changes in schizophrenia 1 This work was presented, in part, at the VIth International Congress on Schizophrenia Research, Colorado Springs, Colorado, USA, April 1997. 1 , 1999, Schizophrenia Research.

[59]  Alan C. Evans,et al.  Detecting changes in nonisotropic images , 1999, Human brain mapping.

[60]  D. V. van Essen,et al.  Functional and structural mapping of human cerebral cortex: solutions are in the surfaces. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[61]  R. Murray,et al.  The dysplastic net hypothesis: an integration of developmental and dysconnectivity theories of schizophrenia , 1997, Schizophrenia Research.

[62]  D. Purves,et al.  Correlated Size Variations in Human Visual Cortex, Lateral Geniculate Nucleus, and Optic Tract , 1997, The Journal of Neuroscience.

[63]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[64]  Bruce Riska,et al.  SOME MODELS FOR DEVELOPMENT, GROWTH, AND MORPHOMETRIC CORRELATION , 1986, Evolution; international journal of organic evolution.

[65]  J. Sundsten,et al.  Folding of the Cerebral Cortex in Mammals , 1984 .

[66]  J. Sundsten,et al.  Folding of the cerebral cortex in mammals. A scaling model. , 1984, Brain, behavior and evolution.