On development of functional brain connectivity in the young brain

Our brain is a complex network of structurally and functionally interconnected regions, shaped to efficiently process and integrate information. The development from a brain equipped with basic functionalities to an efficient network facilitating complex behavior starts during gestation and continues into adulthood. Resting-state functional MRI (rs-fMRI) enables the examination of developmental aspects of functional connectivity (FC) and functional brain networks. This review will discuss changes observed in the developing brain on the level of network FC from a gestational age of 20 weeks onwards. We discuss findings of resting-state fMRI studies showing that functional network development starts during gestation, creating a foundation for each of the resting-state networks (RSNs) to be established. Visual and sensorimotor areas are reported to develop first, with other networks, at different rates, increasing both in network connectivity and size over time. Reaching childhood, marked fine-tuning and specialization takes place in the regions necessary for higher-order cognitive functions.

[1]  Alan C. Evans,et al.  Brain Connectivity , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[2]  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.

[3]  Michael D. Greicius,et al.  Development of functional and structural connectivity within the default mode network in young children , 2010, NeuroImage.

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

[5]  Heping Zhang,et al.  A left cerebellar pathway mediates language in prematurely-born young adults , 2013, NeuroImage.

[6]  Petra S. Hüppi,et al.  Multimodality evaluation of the pediatric brain: DTI and its competitors , 2013, Pediatric Radiology.

[7]  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.

[8]  Abraham Z. Snyder,et al.  Functional connectivity MRI in infants: Exploration of the functional organization of the developing brain , 2011, NeuroImage.

[9]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[10]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

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

[12]  F. Lazeyras,et al.  Mapping the early cortical folding process in the preterm newborn brain. , 2008, Cerebral cortex.

[13]  K. Davis,et al.  Cognitive and default‐mode resting state networks: Do male and female brains “rest” differently? , 2010, Human brain mapping.

[14]  Gary H. Glover,et al.  Default-mode function and task-induced deactivation have overlapping brain substrates in children , 2008, NeuroImage.

[15]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[16]  Cornelis J. Stam,et al.  Genetic control of functional brain network efficiency in children , 2013, European Neuropsychopharmacology.

[17]  P. Fox,et al.  Genetic control over the resting brain , 2010, Proceedings of the National Academy of Sciences.

[18]  Doris Y. Tsao,et al.  Functional Connectivity in the Brain: Effects of Anesthesia , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[19]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[20]  Kaustubh Supekar,et al.  Systems Neuroscience Review Article , 2011 .

[21]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

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

[23]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

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

[25]  J. Shimony,et al.  Resting-State fMRI: A Review of Methods and Clinical Applications , 2013, American Journal of Neuroradiology.

[26]  Frederik Barkhof,et al.  Resting‐state networks in awake five‐ to eight‐year old children , 2012, Human brain mapping.

[27]  Peter Fransson,et al.  Spontaneous Brain Activity in the Newborn Brain During Natural Sleep—An fMRI Study in Infants Born at Full Term , 2009, Pediatric Research.

[28]  Colin Studholme,et al.  Cross-Hemispheric Functional Connectivity in the Human Fetal Brain , 2013, Science Translational Medicine.

[29]  Jeroen Hendrikse,et al.  Regional changes in brain perfusion during brain maturation measured non-invasively with Arterial Spin Labeling MRI in neonates. , 2013, European Journal of Radiology.

[30]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[31]  Nora D. Volkow,et al.  Functional connectivity hubs in the human brain , 2011, NeuroImage.

[32]  D. Prayer,et al.  Watching the fetal brain at ‘rest’ , 2012, International Journal of Developmental Neuroscience.

[33]  Kevin G. Guise,et al.  Functional connectivity of the sensorimotor area in naturally sleeping infants , 2008, Brain Research.

[34]  Cornelis J. Stam,et al.  The Brain Matures with Stronger Functional Connectivity and Decreased Randomness of Its Network , 2012, PloS one.

[35]  M. Verhoye,et al.  Functional Connectivity fMRI of the Rodent Brain: Comparison of Functional Connectivity Networks in Rat and Mouse , 2011, PloS one.

[36]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[37]  Rasmus M. Birn,et al.  The role of physiological noise in resting-state functional connectivity , 2012, NeuroImage.

[38]  C. Boesch,et al.  Structural and Neurobehavioral Delay in Postnatal Brain Development of Preterm Infants1 , 1996, Pediatric Research.

[39]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Parietal Cortex and Comparison with Human and Macaque Resting-State Functional Connectivity , 2011, The Journal of Neuroscience.

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

[41]  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 .

[42]  David A. Leopold,et al.  Ongoing physiological processes in the cerebral cortex , 2012, NeuroImage.

[43]  L. Ment,et al.  Imaging biomarkers of outcome in the developing preterm brain , 2009, The Lancet Neurology.

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

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

[46]  Sarah-Jayne Blakemore,et al.  Imaging brain development: The adolescent brain , 2012, NeuroImage.

[47]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

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

[49]  H. Chugani.  A critical period of brain development: studies of cerebral glucose utilization with PET. , 1998, Preventive medicine.

[50]  Hong Wang,et al.  Abnormal Cerebral Structure Is Present at Term in Premature Infants , 2005, Pediatrics.

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

[52]  J. Hajnal,et al.  Abnormal Cortical Development after Premature Birth Shown by Altered Allometric Scaling of Brain Growth , 2006, PLoS medicine.

[53]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

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

[55]  Vince D. Calhoun,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

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

[57]  Danielle S Bassett,et al.  Genetic Influences on Cost-Efficient Organization of Human Cortical Functional Networks , 2011, The Journal of Neuroscience.

[58]  Joseph S. Gati,et al.  Resting-state networks in the macaque at 7T , 2011, NeuroImage.

[59]  D. Margulies,et al.  Development of anterior cingulate functional connectivity from late childhood to early adulthood. , 2009, Cerebral cortex.

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

[61]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

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

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

[64]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[65]  S. Rombouts,et al.  A comprehensive study of whole-brain functional connectivity in children and young adults. , 2011, Cerebral cortex.

[66]  C. Rosazza,et al.  Resting-state brain networks: literature review and clinical applications , 2011, Neurological Sciences.

[67]  L. Becerra,et al.  Robust Reproducible Resting State Networks in the Awake Rodent Brain , 2011, PloS one.

[68]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[69]  P. Hüppi,et al.  Cortical Development in the Fetus and the Newborn: Advanced MR Techniques , 2011, Topics in magnetic resonance imaging : TMRI.