Accurate age classification of 6 and 12 month-old infants based on resting-state functional connectivity magnetic resonance imaging data

Human large-scale functional brain networks are hypothesized to undergo significant changes over development. Little is known about these functional architectural changes, particularly during the second half of the first year of life. We used multivariate pattern classification of resting-state functional connectivity magnetic resonance imaging (fcMRI) data obtained in an ongoing , multi-site, longitudinal study of brain and behavioral development to explore whether fcMRI data contained information sufficient to classify infant age. Analyses carefully account for the effects of fcMRI motion artifact. Support vector machines (SVMs) classified 6 versus 12 month-old infants (128 datasets) above chance based on fcMRI Infant Development Multivariate pattern analysis (MVPA) Support vector machine (SVM) Functional brain networks data alone. Results demonstrate significant changes in measures of brain functional organization that coincide with a special period of dramatic change in infant motor, cognitive, and social development. Explorations of the most different correlations used for SVM lead to two different interpretations about functional connections that support 6 versus 12-month age categorization.

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

[2]  G. Saxe Culture and Cognitive Development , 2015 .

[3]  Scott P. Johnson,et al.  The broader autism phenotype in infancy: when does it emerge? , 2014, Journal of the American Academy of Child and Adolescent Psychiatry.

[4]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[5]  Vince D. Calhoun,et al.  Functional connectivity in the developing brain: A longitudinal study from 4 to 9months of age , 2014, NeuroImage.

[6]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[7]  Christos Davatzikos,et al.  Heterogeneous impact of motion on fundamental patterns of developmental changes in functional connectivity during youth , 2013, NeuroImage.

[8]  Karina J. Kersbergen,et al.  On development of functional brain connectivity in the young brain , 2013, Front. Hum. Neurosci..

[9]  Lonnie Zwaigenbaum,et al.  Early identification of autism spectrum disorders , 2013, Behavioural Brain Research.

[10]  Guido Gerig,et al.  White matter microstructure and atypical visual orienting in 7-month-olds at risk for autism. , 2013, The American journal of psychiatry.

[11]  Stanislas Dehaene,et al.  A Neural Marker of Perceptual Consciousness in Infants , 2013, Science.

[12]  Guido Gerig,et al.  Frontolimbic neural circuitry at 6 months predicts individual differences in joint attention at 9 months. , 2013, Developmental science.

[13]  Elizabeth A Stuart,et al.  Latent class analysis of early developmental trajectory in baby siblings of children with autism. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[14]  Alan C. Evans,et al.  Brain volume findings in 6-month-old infants at high familial risk for autism. , 2012, The American journal of psychiatry.

[15]  Guido Gerig,et al.  Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. , 2012, The American journal of psychiatry.

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

[17]  S. Lawrie,et al.  A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders , 2012, Neuroscience & Biobehavioral Reviews.

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

[19]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

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

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

[22]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[23]  S. Petersen,et al.  Concepts and principles in the analysis of brain networks , 2011, Annals of the New York Academy of Sciences.

[24]  Mark H. Johnson,et al.  Mapping Infant Brain Myelination with Magnetic Resonance Imaging , 2011, The Journal of Neuroscience.

[25]  D. Louis Collins,et al.  Unbiased average age-appropriate atlases for pediatric studies , 2011, NeuroImage.

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

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

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

[29]  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.

[30]  C. Lord,et al.  Standardizing ADOS Scores for a Measure of Severity in Autism Spectrum Disorders , 2009, Journal of autism and developmental disorders.

[31]  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.

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

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

[34]  Gunnar Rätsch,et al.  Support Vector Machines and Kernels for Computational Biology , 2008, PLoS Comput. Biol..

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

[36]  Damien A. Fair,et al.  Defining functional areas in individual human brains using resting functional connectivity MRI , 2008, NeuroImage.

[37]  C. Lord,et al.  The Autism Diagnostic Observation Schedule: Revised Algorithms for Improved Diagnostic Validity , 2007, Journal of autism and developmental disorders.

[38]  Abraham Z Snyder,et al.  Registration of [18F]FDG microPET and small-animal MRI. , 2005, Nuclear medicine and biology.

[39]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[40]  Bernhard Schölkopf,et al.  A tutorial on support vector regression , 2004, Stat. Comput..

[41]  D. Seese,et al.  Algorithms for Spectral Analysis of Irregularly Sampled Time Series , 2004 .

[42]  P. Kuhl,et al.  Foreign-language experience in infancy: Effects of short-term exposure and social interaction on phonetic learning , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  O. Pascalis,et al.  Is Face Processing Species-Specific During the First Year of Life? , 2002, Science.

[44]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[45]  Mark H. Johnson Functional brain development in humans , 2001, Nature Reviews Neuroscience.

[46]  Michael W. Spratling,et al.  Gamma oscillations and object processing in the infant brain. , 2000, Science.

[47]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[48]  David J. Hawkes,et al.  Voxel similarity measures for 3-D serial MR brain image registration , 1999, IEEE Transactions on Medical Imaging.

[49]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[50]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[51]  Ron Kohavi,et al.  A Study of Cross-Validation and Bootstrap for Accuracy Estimation and Model Selection , 1995, IJCAI.

[52]  J. Bruner,et al.  The capacity for joint visual attention in the infant , 1975, Nature.

[53]  H. Roffwarg,et al.  Ontogenetic development of the human sleep-dream cycle. , 1966, Science.

[54]  J. Gilmore,et al.  The Synchronization within and Interaction between the Default and Dorsal Attention Networks in Early Infancy , 2012 .

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

[56]  M. Greicius,et al.  Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity , 2009, Brain Structure and Function.