Shared and unique brain network features predict cognition, personality and mental health in childhood

The manner through which individual differences in brain network organization track population-level behavioral variability is a fundamental question in systems neuroscience. Recent work suggests that resting-state and task-state functional connectivity can predict specific traits at the individual level. However, the focus of most studies on single behavioral traits has come at the expense of capturing broader relationships across behaviors. Here, we utilized a large-scale dataset of 1858 typically developing children to estimate whole-brain functional network organization that is predictive of individual differences in cognition, impulsivity-related personality, and mental health during rest and task states. Predictive network features were distinct across the broad behavioral domains: cognition, personality and mental health. On the other hand, traits within each behavioral domain were predicted by highly similar network features. This is surprising given decades of research emphasizing that distinct brain networks support different mental processes. Although tasks are known to modulate the functional connectome, we found that predictive network features were similar between resting and task states. Overall, our findings reveal shared brain network features that account for individual variation within broad domains of behavior in childhood, yet are unique to different behavioral domains.

[1]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[2]  Efstathios D. Gennatas,et al.  Connectome-Wide Network Analysis of Youth with Psychosis Spectrum Symptoms , 2015, Molecular Psychiatry.

[3]  Jessica A. Turner,et al.  Task-induced brain connectivity promotes the detection of individual differences in brain-behavior relationships , 2019, NeuroImage.

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

[5]  Ahmad R. Hariri,et al.  General functional connectivity: Shared features of resting-state and task fMRI drive reliable and heritable individual differences in functional brain networks , 2018, NeuroImage.

[6]  Simon B Eickhoff,et al.  Neuroimaging-based prediction of mental traits: Road to utopia or Orwell? , 2019, PLoS biology.

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

[8]  L. Steinberg Cognitive and affective development in adolescence , 2005, Trends in Cognitive Sciences.

[9]  Adriana Galvan,et al.  The adolescent brain. , 2008, Developmental review : DR.

[10]  Jonathan D. Power,et al.  Network measures predict neuropsychological outcome after brain injury , 2014, Proceedings of the National Academy of Sciences.

[11]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[12]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

[13]  Charles J. Lynch,et al.  Salience network-based classification and prediction of symptom severity in children with autism. , 2013, JAMA psychiatry.

[14]  Dustin Scheinost,et al.  Resting-state functional connectivity predicts neuroticism and extraversion in novel individuals , 2018, Social cognitive and affective neuroscience.

[15]  Richard F. Betzel,et al.  Linked dimensions of psychopathology and connectivity in functional brain networks , 2017, bioRxiv.

[16]  L. Spear,et al.  Adolescent neurodevelopment. , 2013, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[17]  Tyrone D. Cannon,et al.  Prodromal psychosis screening in adolescent psychiatry clinics , 2012, Early intervention in psychiatry.

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

[19]  A. Meyer-Lindenberg,et al.  Machine Learning for Precision Psychiatry: Opportunities and Challenges. , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[20]  Jingwei Li,et al.  Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity , 2019, bioRxiv.

[21]  B T Thomas Yeo,et al.  Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  S. Corkin What's new with the amnesic patient H.M.? , 2002, Nature Reviews Neuroscience.

[23]  T. Robbins,et al.  Neurobehavioral mechanisms of impulsivity: Fronto-striatal systems and functional neurochemistry , 2008, Pharmacology Biochemistry and Behavior.

[24]  Mark A. Elliott,et al.  Being right is its own reward: Load and performance related ventral striatum activation to correct responses during a working memory task in youth , 2012, NeuroImage.

[25]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[26]  Christopher L. Asplund,et al.  Functional Specialization and Flexibility in Human Association Cortex. , 2015, Cerebral cortex.

[27]  S. Eickhoff,et al.  Predicting personality from network-based resting-state functional connectivity , 2018, Brain Structure and Function.

[28]  John B. Carroll,et al.  The Higher-stratum Structure of Cognitive Abilities: Current Evidence Supports g and About Ten Broad Factors , 2003 .

[29]  A. Holmes,et al.  The Myth of Optimality in Clinical Neuroscience , 2018, Trends in Cognitive Sciences.

[30]  G. Glover,et al.  Earlier Development of the Accumbens Relative to Orbitofrontal Cortex Might Underlie Risk-Taking Behavior in Adolescents , 2006, The Journal of Neuroscience.

[31]  JaneR . Taylor,et al.  Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli , 1999, Psychopharmacology.

[32]  D. Barch,et al.  Adolescent neurocognitive development and impacts of substance use: Overview of the adolescent brain cognitive development (ABCD) baseline neurocognition battery , 2018, Developmental Cognitive Neuroscience.

[33]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[34]  Dustin Scheinost,et al.  Dynamic functional connectivity during task performance and rest predicts individual differences in attention across studies , 2019, NeuroImage.

[35]  G. Pearlson,et al.  Diminished Frontostriatal Activity During Processing of Monetary Rewards and Losses in Pathological Gambling , 2012, Biological Psychiatry.

[36]  David Watson,et al.  The Hierarchical Taxonomy of Psychopathology (HiTOP): A Dimensional Alternative to Traditional Nosologies , 2017, Journal of abnormal psychology.

[37]  Timothy O. Laumann,et al.  Generation and Evaluation of a Cortical Area Parcellation from Resting-State Correlations. , 2016, Cerebral cortex.

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

[39]  D. Zald,et al.  Dopaminergic Network Differences in Human Impulsivity , 2010, Science.

[40]  Joseph Glicksohn,et al.  The construct of impulsivity revisited , 2007 .

[41]  Danielle S. Bassett,et al.  A mechanistic model of connector hubs, modularity and cognition , 2018, Nature Human Behaviour.

[42]  R. Murray,et al.  Association between symptom dimensions and categorical diagnoses of psychosis: a cross-sectional and longitudinal investigation. , 2014, Schizophrenia bulletin.

[43]  B. J. Casey,et al.  vlPFC–vmPFC–Amygdala Interactions Underlie Age-Related Differences in Cognitive Regulation of Emotion , 2016, Cerebral cortex.

[44]  T. Ge,et al.  Resting brain dynamics at different timescales capture distinct aspects of human behavior , 2019, Nature Communications.

[45]  Meiling Li,et al.  Individual-specific functional connectivity markers track dimensional and categorical features of psychotic illness , 2018, Molecular Psychiatry.

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

[47]  Anders M. Dale,et al.  Image processing and analysis methods for the Adolescent Brain Cognitive Development Study , 2018, NeuroImage.

[48]  C. Gienger Wechsler Intelligence Scale for Children – Fifth Edition (WISC-V) , 2018 .

[49]  Krzysztof J. Gorgolewski,et al.  The Dynamics of Functional Brain Networks: Integrated Network States during Cognitive Task Performance , 2015, Neuron.

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

[51]  M. Chun,et al.  A neuromarker of sustained attention from whole-brain functional connectivity , 2015, Nature Neuroscience.

[52]  Dustin Scheinost,et al.  Combining multiple connectomes improves predictive modeling of phenotypic measures , 2019, NeuroImage.

[53]  A. M. Dale,et al.  A hybrid approach to the skull stripping problem in MRI , 2004, NeuroImage.

[54]  Justin T. Baker,et al.  Functional connectomics of affective and psychotic pathology , 2018, Proceedings of the National Academy of Sciences.

[55]  Dustin Scheinost,et al.  Connectome-based predictive modeling of attention: Comparing different functional connectivity features and prediction methods across datasets , 2018, NeuroImage.

[56]  Doris Y. Tsao,et al.  Functional Compartmentalization and Viewpoint Generalization Within the Macaque Face-Processing System , 2010, Science.

[57]  Todd A. Hare,et al.  A Developmental Shift from Positive to Negative Connectivity in Human Amygdala–Prefrontal Circuitry , 2013, The Journal of Neuroscience.

[58]  Yong Liu,et al.  Core networks and their reconfiguration patterns across cognitive loads , 2018, Human brain mapping.

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

[60]  P. Fox,et al.  Identification of a common neurobiological substrate for mental illness. , 2015, JAMA psychiatry.

[61]  M. Milham,et al.  Clinically Useful Brain Imaging for Neuropsychiatry: How Can We Get There? , 2017, bioRxiv.

[62]  Tanya M. Evans,et al.  Brain Structural Integrity and Intrinsic Functional Connectivity Forecast 6 Year Longitudinal Growth in Children's Numerical Abilities , 2015, The Journal of Neuroscience.

[63]  T. Paus,et al.  Why do many psychiatric disorders emerge during adolescence? , 2008, Nature Reviews Neuroscience.

[64]  Brian Knutson,et al.  Incentive-Elicited Brain Activation in Adolescents: Similarities and Differences from Young Adults , 2004, The Journal of Neuroscience.

[65]  Eibe Frank,et al.  Evaluating the Replicability of Significance Tests for Comparing Learning Algorithms , 2004, PAKDD.

[66]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[67]  Yoshua Bengio,et al.  Inference for the Generalization Error , 1999, Machine Learning.

[68]  Sheri L. Johnson,et al.  The 7 up 7 down inventory: a 14-item measure of manic and depressive tendencies carved from the General Behavior Inventory. , 2013, Psychological assessment.

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

[70]  Sandhya Ramrakha,et al.  The p Factor , 2014, Clinical psychological science : a journal of the Association for Psychological Science.

[71]  Christos Davatzikos,et al.  Individual Variation in Functional Topography of Association Networks in Youth , 2020, Neuron.

[72]  Mert R. Sabuncu,et al.  Deep neural networks and kernel regression achieve comparable accuracies for functional connectivity prediction of behavior and demographics , 2020, NeuroImage.

[73]  Dustin Scheinost,et al.  The Functional Brain Organization of an Individual Allows Prediction of Measures of Social Abilities Transdiagnostically in Autism and Attention-Deficit/Hyperactivity Disorder , 2019, Biological Psychiatry.

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

[75]  Danilo Bzdok,et al.  Semi-Supervised Factored Logistic Regression for High-Dimensional Neuroimaging Data , 2015, NIPS.

[76]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[77]  E. Sanz-Arigita,et al.  Brain functional connectivity changes in children that differ in impulsivity temperamental trait , 2014, Front. Behav. Neurosci..

[78]  Bruce N Cuthbert,et al.  The NIMH Research Domain Criteria Initiative: Background, Issues, and Pragmatics. , 2016, Psychophysiology.

[79]  O. Andreassen,et al.  Brain Connectome Mapping of Complex Human Traits and Their Polygenic Architecture Using Machine Learning , 2019, Biological Psychiatry.

[80]  V. Menon Large-scale brain networks and psychopathology: a unifying triple network model , 2011, Trends in Cognitive Sciences.

[81]  G. Pearlson,et al.  Clinical phenotypes of psychosis in the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP). , 2013, The American journal of psychiatry.

[82]  Michael W. Cole,et al.  Higher Intelligence Is Associated with Less Task-Related Brain Network Reconfiguration , 2016, The Journal of Neuroscience.

[83]  Dan J Stein,et al.  Development of lifetime comorbidity in the World Health Organization world mental health surveys. , 2011, Archives of general psychiatry.

[84]  Amin Karbasi,et al.  Individualized functional networks reconfigure with cognitive state , 2020, NeuroImage.

[85]  Penny Dade,et al.  Encyclopedia of Autism Spectrum Disorders , 2013 .

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

[87]  Danilo Bzdok,et al.  Formal Models of the Network Co-occurrence Underlying Mental Operations , 2016, PLoS Comput. Biol..

[88]  Nancy Kanwisher,et al.  Language-Selective and Domain-General Regions Lie Side by Side within Broca’s Area , 2012, Current Biology.

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

[90]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[91]  R. Poldrack,et al.  Somatosensory-Motor Dysconnectivity Spans Multiple Transdiagnostic Dimensions of Psychopathology , 2019, Biological Psychiatry.

[92]  Bruce Fischl,et al.  Geometrically Accurate Topology-Correction of Cortical Surfaces Using Nonseparating Loops , 2007, IEEE Transactions on Medical Imaging.

[93]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[94]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[95]  C. Sripada,et al.  Prediction of neurocognition in youth from resting state fMRI , 2019, Molecular Psychiatry.

[96]  D. Barch,et al.  Resting-State Functional Connectivity and Psychotic-like Experiences in Childhood: Results From the Adolescent Brain Cognitive Development Study , 2019, Biological Psychiatry.

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

[98]  R. Halari,et al.  A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention , 2012, Cortex.

[99]  B. Luna,et al.  Adolescence as a neurobiological critical period for the development of higher-order cognition , 2018, Neuroscience & Biobehavioral Reviews.

[100]  Edward T Bullmore,et al.  Probing Compulsive and Impulsive Behaviors, from Animal Models to Endophenotypes: A Narrative Review , 2010, Neuropsychopharmacology.

[101]  F. Volkmar Encyclopedia of autism spectrum disorders , 2013 .

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

[103]  Brian Knutson,et al.  Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics , 2009, Biological Psychiatry.

[104]  Paola Galdi,et al.  Resting-State Functional Brain Connectivity Best Predicts the Personality Dimension of Openness to Experience , 2018, Personality Neuroscience.

[105]  B T Thomas Yeo,et al.  Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. , 2014, JAMA psychiatry.

[106]  Evan M. Gordon,et al.  Local-Global Parcellation of the Human Cerebral Cortex From Intrinsic Functional Connectivity MRI , 2017, bioRxiv.

[107]  L. Rescorla,et al.  The Achenbach System of Empirically Based Assessment. , 2016 .

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

[109]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[110]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[111]  Terry L. Jernigan,et al.  Demographic, physical and mental health assessments in the adolescent brain and cognitive development study: Rationale and description , 2017, Developmental Cognitive Neuroscience.

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

[113]  Randy L. Buckner,et al.  Situating the left-lateralized language network in the broader organization of multiple specialized large-scale distributed networks , 2019, bioRxiv.

[114]  D. Lynam UPPS-P Impulsive Behavior Scale--Short English Version , 2014 .

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

[116]  Caterina Gratton,et al.  Double dissociation of two cognitive control networks in patients with focal brain lesions , 2010, Proceedings of the National Academy of Sciences.

[117]  Daniel S. Margulies,et al.  In need of constraint: Understanding the role of the cingulate cortex in the impulsive mind , 2017, NeuroImage.

[118]  Andres Hoyos Idrobo,et al.  Assessing and tuning brain decoders: Cross-validation, caveats, and guidelines , 2016, NeuroImage.

[119]  J. Gray,et al.  Meditation experience is associated with differences in default mode network activity and connectivity , 2011, Proceedings of the National Academy of Sciences.

[120]  Michael W. Cole,et al.  The Frontoparietal Control System , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[121]  Benjamin J. Shannon,et al.  Premotor functional connectivity predicts impulsivity in juvenile offenders , 2011, Proceedings of the National Academy of Sciences.

[122]  John P. A. Ioannidis,et al.  Exploration, Inference, and Prediction in Neuroscience and Biomedicine , 2019, Trends in Neurosciences.

[123]  Katherine R. Luking,et al.  Revising the BIS/BAS Scale to study development: Measurement invariance and normative effects of age and sex from childhood through adulthood. , 2016, Psychological assessment.

[124]  Moriah E. Thomason,et al.  Age-related changes in the structure and function of prefrontal cortex–amygdala circuitry in children and adolescents: A multi-modal imaging approach , 2014, NeuroImage.

[125]  Bart Larsen,et al.  Development of White Matter Microstructure and Intrinsic Functional Connectivity Between the Amygdala and Ventromedial Prefrontal Cortex: Associations With Anxiety and Depression , 2017, Biological Psychiatry.

[126]  Dustin Scheinost,et al.  Task-induced brain state manipulation improves prediction of individual traits , 2018, Nature Communications.

[127]  Serge A. R. B. Rombouts,et al.  Adolescent risky decision-making: Neurocognitive development of reward and control regions , 2010, NeuroImage.

[128]  Joel Nothman,et al.  SciPy 1.0-Fundamental Algorithms for Scientific Computing in Python , 2019, ArXiv.

[129]  Xi-Nian Zuo,et al.  Spatial Topography of Individual-Specific Cortical Networks Predicts Human Cognition, Personality, and Emotion. , 2019, Cerebral cortex.

[130]  J. Ford,et al.  Default mode network activity and connectivity in psychopathology. , 2012, Annual review of clinical psychology.

[131]  Sheng Zhang,et al.  Decreased saliency processing as a neural measure of Barratt impulsivity in healthy adults , 2012, NeuroImage.

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

[133]  A. Mechelli,et al.  Common Dysfunction of Large-Scale Neurocognitive Networks Across Psychiatric Disorders , 2019, Biological Psychiatry.

[134]  Timothy O. Laumann,et al.  Identifying reproducible individual differences in childhood functional brain networks: An ABCD study , 2019, Developmental Cognitive Neuroscience.

[135]  O. Spreen,et al.  A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary , 1991 .

[136]  D. Barch,et al.  O9. Delineating and Validating Major Dimensions of Psychopathology in the Adolescent Brain Cognitive Development (ABCD) Study , 2019, Biological Psychiatry.

[137]  Jessica R. Cohen,et al.  The Segregation and Integration of Distinct Brain Networks and Their Relationship to Cognition , 2016, The Journal of Neuroscience.

[138]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[139]  Mert R. Sabuncu,et al.  Global signal regression strengthens association between resting-state functional connectivity and behavior , 2019, NeuroImage.