Functional Connectivity Fingerprints at Rest Are Similar across Youths and Adults and Vary with Genetic Similarity

Summary Distinguishing individuals from brain connectivity, and studying the genetic influences on that identification across different ages, improves our basic understanding of functional brain network organization. We applied support vector machine classifiers to two datasets of twins (adult, pediatric) and two datasets of repeat-scan individuals (adult, pediatric). Classifiers were trained on resting state functional connectivity magnetic resonance imaging (rs-fcMRI) data and used to predict individuals and co-twin pairs from independent data. The classifiers successfully identified individuals from a previous scan with 100% accuracy, even when scans were separated by months. In twin samples, classifier accuracy decreased as genetic similarity decreased. Our results demonstrate that classification is stable within individuals, similar within families, and contains similar representations of functional connections over a few decades of life. Moreover, the degree to which these patterns of connections predict siblings' data varied by genetic relatedness, suggesting that genetic influences on rs-fcMRI connectivity are established early in life.

[1]  Brian S Caffo,et al.  Modular preprocessing pipelines can reintroduce artifacts into fMRI data , 2018, bioRxiv.

[2]  J. Maldjian,et al.  Effect of resting-state functional MR imaging duration on stability of graph theory metrics of brain network connectivity. , 2011, Radiology.

[3]  N. Dosenbach,et al.  The frontoparietal network: function, electrophysiology, and importance of individual precision mapping , 2018, Dialogues in clinical neuroscience.

[4]  Karl J. Friston,et al.  Heritability of the Effective Connectivity in the Resting‐State Default Mode Network , 2017, Cerebral cortex.

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

[6]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[7]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[8]  Koen V. Haak,et al.  Connectopic mapping with resting-state fMRI , 2016, NeuroImage.

[9]  Damien A. Fair,et al.  Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature , 2017, NeuroImage.

[10]  Theodore P. Zanto,et al.  Fronto-parietal network: flexible hub of cognitive control , 2013, Trends in Cognitive Sciences.

[11]  Evan M. Gordon,et al.  Long-term neural and physiological phenotyping of a single human , 2015, Nature Communications.

[12]  Stephen C. Strother,et al.  Support vector machines for temporal classification of block design fMRI data , 2005, NeuroImage.

[13]  Dante Mantini,et al.  Connectivity-based parcellation reveals distinct cortico-striatal connectivity fingerprints in Autism Spectrum Disorder , 2017, NeuroImage.

[14]  Oscar Miranda-Dominguez,et al.  Heritability of the human connectome: A connectotyping study , 2017, Network Neuroscience.

[15]  M. Raichle The brain's default mode network. , 2015, Annual review of neuroscience.

[16]  Efstathios D. Gennatas,et al.  Linked Sex Differences in Cognition and Functional Connectivity in Youth. , 2015, Cerebral cortex.

[17]  Jonathan D. Power,et al.  Evidence for Hubs in Human Functional Brain Networks , 2013, Neuron.

[18]  Daniel J Mitchell,et al.  Task Encoding across the Multiple Demand Cortex Is Consistent with a Frontoparietal and Cingulo-Opercular Dual Networks Distinction , 2016, The Journal of Neuroscience.

[19]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[20]  S. Petersen,et al.  Multivariate pattern classification of pediatric Tourette syndrome using functional connectivity MRI , 2016, Developmental science.

[21]  Elliot M. Tucker-Drob,et al.  The Texas Twin Project , 2012, Twin Research and Human Genetics.

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

[23]  David Wisniewski,et al.  Switch-Independent Task Representations in Frontal and Parietal Cortex , 2017, The Journal of Neuroscience.

[24]  Guido Gerig,et al.  Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness , 2017, PloS one.

[25]  E. Stein,et al.  Multiple Neuronal Networks Mediate Sustained Attention , 2003, Journal of Cognitive Neuroscience.

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

[27]  Anders M. Dale,et al.  The Adolescent Brain Cognitive Development (ABCD) study: Imaging acquisition across 21 sites , 2018, Developmental Cognitive Neuroscience.

[28]  Mary E. Meyerand,et al.  The effect of scan length on the reliability of resting-state fMRI connectivity estimates , 2013, NeuroImage.

[29]  Michael W. Cole,et al.  Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks , 2017, Proceedings of the National Academy of Sciences.

[30]  Xi-Nian Zuo,et al.  Assessing Variations in Areal Organization for the Intrinsic Brain: From Fingerprints to Reliability , 2016, bioRxiv.

[31]  Jason B. Mattingley,et al.  Functional brain networks related to individual differences in human intelligence at rest , 2016, Scientific Reports.

[32]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[33]  Haijing Niu,et al.  The development of functional network organization in early childhood and early adolescence: A resting-state fNIRS study , 2018, Developmental Cognitive Neuroscience.

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

[35]  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 .

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

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

[38]  J. Raven STANDARDIZATION OF PROGRESSIVE MATRICES, 1938 , 1941 .

[39]  Timothy O. Laumann,et al.  Functional Brain Networks Are Dominated by Stable Group and Individual Factors, Not Cognitive or Daily Variation , 2018, Neuron.

[40]  Damien A. Fair,et al.  Connectotyping: Model Based Fingerprinting of the Functional Connectome , 2014, PloS one.

[41]  Evan M. Gordon,et al.  Three Distinct Sets of Connector Hubs Integrate Human Brain Function. , 2018, Cell reports.

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

[43]  K. Hwang,et al.  The Contribution of Network Organization and Integration to the Development of Cognitive Control , 2015, PLoS biology.

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

[45]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[46]  N. Volkow,et al.  The conception of the ABCD study: From substance use to a broad NIH collaboration , 2017, Developmental Cognitive Neuroscience.

[47]  Steven E Petersen,et al.  Preparatory Engagement of Cognitive Control Networks Increases Late in Childhood , 2017, Cerebral cortex.

[48]  Dustin Scheinost,et al.  The individual functional connectome is unique and stable over months to years , 2017, NeuroImage.

[49]  Evan M. Gordon,et al.  On the Stability of BOLD fMRI Correlations , 2016, Cerebral cortex.

[50]  Karsten Specht,et al.  Resting States Are Resting Traits – An fMRI Study of Sex Differences and Menstrual Cycle Effects in Resting State Cognitive Control Networks , 2014, PloS one.

[51]  Mareike Kritzler,et al.  Emergence of Individuality in Genetically Identical Mice , 2013, Science.

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

[53]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[54]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

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

[56]  Evan M. Gordon,et al.  Individual Variability of the System‐Level Organization of the Human Brain , 2015, Cerebral cortex.

[57]  Darren J. Yeo,et al.  Prospective relations between resting-state connectivity of parietal subdivisions and arithmetic competence , 2017, Developmental Cognitive Neuroscience.

[58]  Wei Deng,et al.  Genetic influences on resting‐state functional networks: A twin study , 2015, Human brain mapping.

[59]  Lisa Byrge,et al.  High-accuracy individual identification using a “thin slice” of the functional connectome , 2019, Network Neuroscience.

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

[61]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[62]  Evan M. Gordon,et al.  Precision Functional Mapping of Individual Human Brains , 2017, Neuron.

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

[64]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[65]  O. Andreassen,et al.  Delayed stabilization and individualization in connectome development are related to psychiatric disorders , 2017, Nature Neuroscience.

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

[67]  Beatriz Luna,et al.  The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity , 2013, NeuroImage.