Defining Individual-Specific Functional Neuroanatomy for Precision Psychiatry

Studies comparing diverse groups have shown that many psychiatric diseases involve disruptions across distributed large-scale networks of the brain. There is hope that functional magnetic resonance imaging (fMRI) functional connectivity techniques will shed light on these disruptions, providing prognostic and diagnostic biomarkers as well as targets for therapeutic interventions. However, to date, progress on clinical translation of fMRI methods has been limited. Here, we argue that this limited translation is driven by a combination of intersubject heterogeneity and the relatively low reliability of standard fMRI techniques at the individual level. We review a potential solution to these limitations: the use of new "precision" fMRI approaches that shift the focus of analysis from groups to single individuals through the use of extended data acquisition strategies. We begin by discussing the potential advantages of fMRI functional connectivity methods for improving our understanding of functional neuroanatomy and disruptions in psychiatric disorders. We then discuss the budding field of precision fMRI and findings garnered from this work. We demonstrate that precision fMRI can improve the reliability of functional connectivity measures, while showing high stability and sensitivity to individual differences. We close by discussing the application of these approaches to clinical settings.

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

[2]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[3]  Evan M. Gordon,et al.  Trait-like variants in human functional brain networks , 2019, Proceedings of the National Academy of Sciences.

[4]  Deanna M Barch,et al.  Resting-State Functional Connectivity in the Human Connectome Project: Current Status and Relevance to Understanding Psychopathology. , 2017, Harvard review of psychiatry.

[5]  Evan M. Gordon,et al.  Evidence for Two Independent Factors that Modify Brain Networks to Meet Task Goals. , 2016, Cell reports.

[6]  Carl D. Hacker,et al.  A Novel Data-Driven Approach to Preoperative Mapping of Functional Cortex Using Resting-State Functional Magnetic Resonance Imaging , 2013, Neurosurgery.

[7]  Stephen M Smith,et al.  The relationship between spatial configuration and functional connectivity of brain regions , 2017, bioRxiv.

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

[9]  M. Greicius,et al.  Decoding subject-driven cognitive states with whole-brain connectivity patterns. , 2012, Cerebral cortex.

[10]  R. Atun,et al.  Estimating the true global burden of mental illness. , 2016, The lancet. Psychiatry.

[11]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[12]  D. Barch,et al.  Brain Network Connectivity in Individuals with Schizophrenia and Their Siblings , 2011, Biological Psychiatry.

[13]  Jonathan D. Power,et al.  Customized head molds reduce motion during resting state fMRI scans , 2018, NeuroImage.

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

[15]  Dustin Scheinost,et al.  Influences on the Test–Retest Reliability of Functional Connectivity MRI and its Relationship with Behavioral Utility , 2017, Cerebral cortex.

[16]  J. Andrews-Hanna,et al.  Large-Scale Network Dysfunction in Major Depressive Disorder: A Meta-analysis of Resting-State Functional Connectivity. , 2015, JAMA psychiatry.

[17]  Julia M. Sheffield,et al.  Neuroscience and Biobehavioral Reviews Cognition and Resting-state Functional Connectivity in Schizophrenia , 2022 .

[18]  Abraham Z. Snyder,et al.  On time delay estimation and sampling error in resting-state fMRI , 2019, NeuroImage.

[19]  Samantha Michalka,et al.  Prediction of individualized task activation in sensory modality-selective frontal cortex with ‘connectome fingerprinting’ , 2018, NeuroImage.

[20]  Danielle S Bassett,et al.  Understanding the Emergence of Neuropsychiatric Disorders With Network Neuroscience. , 2018, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[21]  Matthew P. Normand Less Is More: Psychologists Can Learn More by Studying Fewer People , 2016, Front. Psychol..

[22]  M. Fox,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[23]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[24]  Rainer Goebel,et al.  Optimizing Functional Accuracy of TMS in Cognitive Studies: A Comparison of Methods , 2009, Journal of Cognitive Neuroscience.

[25]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[26]  Rodrigo M. Braga,et al.  Parallel Interdigitated Distributed Networks within the Individual Estimated by Intrinsic Functional Connectivity , 2017, Neuron.

[27]  Denise C. Park,et al.  Decreased segregation of brain systems across the healthy adult lifespan , 2014, Proceedings of the National Academy of Sciences.

[28]  D. Long Networks of the Brain , 2011 .

[29]  Petra Hermann,et al.  Resting State fMRI Functional Connectivity Analysis Using Dynamic Time Warping , 2017, Front. Neurosci..

[30]  Margaret A. Niznikiewicz,et al.  Neurobiological approaches to the study of clinical and genetic high risk for developing psychosis , 2019, Psychiatry Research.

[31]  B. Schlaggar,et al.  Considerations for MRI study design and implementation in pediatric and clinical populations , 2015, Developmental Cognitive Neuroscience.

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

[33]  Michael S. Okun,et al.  Coordinate-Based Lead Location Does Not Predict Parkinson's Disease Deep Brain Stimulation Outcome , 2014, PloS one.

[34]  Maxime Descoteaux,et al.  The Canadian Dementia Imaging Protocol: Harmonizing National Cohorts , 2018, Journal of magnetic resonance imaging : JMRI.

[35]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[36]  Carl D. Hacker,et al.  Resting state network estimation in individual subjects , 2013, NeuroImage.

[37]  S. Petersen,et al.  Brain Networks and Cognitive Architectures , 2015, Neuron.

[38]  A. Dale,et al.  From retinotopy to recognition: fMRI in human visual cortex , 1998, Trends in Cognitive Sciences.

[39]  R. Buckner,et al.  Task-free presurgical mapping using functional magnetic resonance imaging intrinsic activity. , 2009, Journal of neurosurgery.

[40]  N. Woodward,et al.  Resting-state networks in schizophrenia. , 2012, Current topics in medicinal chemistry.

[41]  Evan M. Gordon,et al.  Spatial and Temporal Organization of the Individual Human Cerebellum , 2018, Neuron.

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

[43]  D. Bassett,et al.  Emergence of system roles in normative neurodevelopment , 2015, Proceedings of the National Academy of Sciences.

[44]  Daniel E Jonas,et al.  Repetitive transcranial magnetic stimulation for treatment-resistant depression: a systematic review and meta-analysis. , 2014, The Journal of clinical psychiatry.

[45]  S. Riedel-Heller,et al.  Cost-of-illness studies of depression: a systematic review. , 2007, Journal of affective disorders.

[46]  Pierre-François D'Haese,et al.  The Optimal Pallidal Target in Deep Brain Stimulation for Dystonia: A Study Using a Functional Atlas Based on Nonlinear Image Registration , 2014, Stereotactic and Functional Neurosurgery.

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

[48]  Neil D. Woodward,et al.  Review of thalamocortical resting-state fMRI studies in schizophrenia , 2017, Schizophrenia Research.

[49]  V. Calhoun,et al.  Selective changes of resting-state networks in individuals at risk for Alzheimer's disease , 2007, Proceedings of the National Academy of Sciences.

[50]  A. Miyake,et al.  Individual differences in executive functions are almost entirely genetic in origin. , 2008, Journal of experimental psychology. General.

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

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

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

[54]  B T Thomas Yeo,et al.  The modular and integrative functional architecture of the human brain , 2015, Proceedings of the National Academy of Sciences.

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

[56]  Kevin J. Black,et al.  Atypical Functional Connectivity in Tourette Syndrome Differs Between Children and Adults , 2018, Biological Psychiatry.

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

[58]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[59]  Alvaro Pascual-Leone,et al.  Identification of reproducible individualized targets for treatment of depression with TMS based on intrinsic connectivity , 2013, NeuroImage.

[60]  Abraham Z. Snyder,et al.  Emergent Functional Network Effects in Parkinson Disease. , 2019, Cerebral cortex.

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

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

[63]  Steven E. Petersen,et al.  Task Control Signals in Pediatric Tourette Syndrome Show Evidence of Immature and Anomalous Functional Activity , 2009, Front. Hum. Neurosci..

[64]  Jessica A. Turner,et al.  Stronger default mode network connectivity is associated with poorer clinical insight in youth at ultra high-risk for psychotic disorders , 2017, Schizophrenia Research.

[65]  Jayashri Kulkarni,et al.  A Randomized Trial of rTMS Targeted with MRI Based Neuro-Navigation in Treatment-Resistant Depression , 2009, Neuropsychopharmacology.

[66]  M. Knapp,et al.  The global costs of schizophrenia. , 2004, Schizophrenia bulletin.

[67]  Gustavo Deco,et al.  Reliable local dynamics in the brain across sessions are revealed by whole‐brain modeling of resting state activity , 2019, Human brain mapping.

[68]  Vince D. Calhoun,et al.  Whole-brain connectivity dynamics reflect both task-specific and individual-specific modulation: A multitask study , 2017, NeuroImage.

[69]  John L. Bradshaw,et al.  The Neurodevelopmental Frontostriatal Disorders: Evolutionary Adaptiveness and Anomalous Lateralization , 2000, Brain and Language.

[70]  Timothy O. Laumann,et al.  An approach for parcellating human cortical areas using resting-state correlations , 2014, NeuroImage.

[71]  M. Raichle,et al.  Cortical network functional connectivity in the descent to sleep , 2009, Proceedings of the National Academy of Sciences.

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

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

[74]  T. Braver The variable nature of cognitive control: a dual mechanisms framework , 2012, Trends in Cognitive Sciences.

[75]  Daniel R. Little,et al.  Small is beautiful: In defense of the small-N design , 2018, Psychonomic Bulletin & Review.

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

[77]  Suzanne N Haber,et al.  Use of an Individual-Level Approach to Identify Cortical Connectivity Biomarkers in Obsessive-Compulsive Disorder. , 2019, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[78]  Elisabeth J. Ploran,et al.  Distinct Stages of Moment‐to‐Moment Processing in the Cinguloopercular and Frontoparietal Networks , 2017, Cerebral cortex.

[79]  Thomas E. Nichols,et al.  A positive-negative mode of population covariation links brain connectivity, demographics and behavior , 2015, Nature Neuroscience.

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

[81]  A. Dale,et al.  Functional analysis of primary visual cortex (V1) in humans. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

[85]  Timothy O. Laumann,et al.  Organization of Propagated Intrinsic Brain Activity in Individual Humans. , 2019, Cerebral cortex.

[86]  E. Bullmore,et al.  The hubs of the human connectome are generally implicated in the anatomy of brain disorders , 2014, Brain : a journal of neurology.

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

[88]  Satrajit S. Ghosh,et al.  The Healthy Brain Network Serial Scanning Initiative: a resource for evaluating inter-individual differences and their reliabilities across scan conditions and sessions , 2016, bioRxiv.

[89]  B. Schlaggar,et al.  Brain structure in pediatric Tourette syndrome , 2016, Molecular Psychiatry.

[90]  Charles J. Lynch,et al.  Precision Inhibitory Stimulation of Individual-Specific Cortical Hubs Disrupts Information Processing in Humans. , 2018, Cerebral cortex.

[91]  Michael C. Frank,et al.  Estimating the reproducibility of psychological science , 2015, Science.

[92]  Evan M. Gordon,et al.  Individual-specific features of brain systems identified with resting state functional correlations , 2017, NeuroImage.

[93]  Timothy Edward John Behrens,et al.  Task-free MRI predicts individual differences in brain activity during task performance , 2016, Science.

[94]  Eric C Leuthardt,et al.  Clinical Resting-state fMRI in the Preoperative Setting: Are We Ready for Prime Time? , 2016, Topics in magnetic resonance imaging : TMRI.

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

[96]  James F. Leckman,et al.  Phenomenology of tics and natural history of tic disorders , 2003, Brain and Development.

[97]  Andrew T. Drysdale,et al.  Resting-state connectivity biomarkers define neurophysiological subtypes of depression , 2016, Nature Medicine.

[98]  Abraham Z. Snyder,et al.  Altered Emotional Interference Processing in Affective and Cognitive-Control Brain Circuitry in Major Depression , 2008, Biological Psychiatry.

[99]  Abraham Z. Snyder,et al.  Real-time motion analytics during brain MRI improve data quality and reduce costs , 2017, NeuroImage.

[100]  Thomas R Insel,et al.  The NIMH experimental medicine initiative , 2015, World psychiatry : official journal of the World Psychiatric Association.

[101]  Bradley Goodyear,et al.  Reduced Intrinsic Connectivity of Amygdala in Adults with Major Depressive Disorder , 2014, Front. Psychiatry.

[102]  Elisabeth Bernhardt,et al.  Using neuroimaging to individualize TMS treatment for depression: Toward a new paradigm for imaging-guided intervention , 2017, NeuroImage.

[103]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[104]  Ann S. Choe,et al.  Reproducibility and Temporal Structure in Weekly Resting-State fMRI over a Period of 3.5 Years , 2015, PloS one.

[105]  Bing Chen,et al.  An open science resource for establishing reliability and reproducibility in functional connectomics , 2014, Scientific Data.

[106]  Simon B Eickhoff,et al.  Imaging-based parcellations of the human brain , 2018, Nature Reviews Neuroscience.

[107]  L. Zambrano-Vazquez,et al.  High-Fidelity Measures of Whole-Brain Functional Connectivity and White Matter Integrity Mediate Relationships between Traumatic Brain Injury and Post-Traumatic Stress Disorder Symptoms. , 2017, Journal of neurotrauma.

[108]  C. Beevers,et al.  Neural mechanisms of the cognitive model of depression , 2011, Nature Reviews Neuroscience.

[109]  Linda Geerligs,et al.  State and Trait Components of Functional Connectivity: Individual Differences Vary with Mental State , 2015, The Journal of Neuroscience.

[110]  T. Sejnowski,et al.  Perspectives on cognitive neuroscience. , 1988, Science.

[111]  Jonathan D. Power,et al.  Studying Brain Organization via Spontaneous fMRI Signal , 2014, Neuron.

[112]  Efstathios D. Gennatas,et al.  Common and Dissociable Mechanisms of Executive System Dysfunction Across Psychiatric Disorders in Youth. , 2016, The American journal of psychiatry.

[113]  Georg Langs,et al.  Performing group-level functional image analyses based on homologous functional regions mapped in individuals , 2019, PLoS biology.

[114]  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.

[115]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[116]  Jean M. Vettel,et al.  Controllability of structural brain networks , 2014, Nature Communications.

[117]  Biyu J. He,et al.  Loss of Resting Interhemispheric Functional Connectivity after Complete Section of the Corpus Callosum , 2008, The Journal of Neuroscience.

[118]  Christian F Beckmann,et al.  The relationship between spatial configuration and functional connectivity of brain regions revisited , 2019, bioRxiv.

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

[120]  Anissa Abi-Dargham,et al.  Schizophrenia, Dopamine and the Striatum: From Biology to Symptoms , 2019, Trends in Neurosciences.

[121]  Joseph W. Dubis,et al.  Spatial and Temporal Characteristics of Error-Related Activity in the Human Brain , 2015, The Journal of Neuroscience.

[122]  R. Buckner,et al.  Parcellating Cortical Functional Networks in Individuals , 2015, Nature Neuroscience.

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

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

[125]  Helen S. Mayberg,et al.  Defining the Neural Circuitry of Depression: Toward a New Nosology With Therapeutic Implications , 2007, Biological Psychiatry.

[126]  D. Yurgelun-Todd,et al.  Reproducibility of Single-Subject Functional Connectivity Measurements , 2011, American Journal of Neuroradiology.

[127]  Thomas E. Nichols,et al.  Scanning the horizon: towards transparent and reproducible neuroimaging research , 2016, Nature Reviews Neuroscience.

[128]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[129]  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.

[130]  Evan M. Gordon,et al.  Functional System and Areal Organization of a Highly Sampled Individual Human Brain , 2015, Neuron.

[131]  Damien A. Fair,et al.  Behavioral interventions for reducing head motion during MRI scans in children , 2018, NeuroImage.

[132]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[133]  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.

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

[135]  Mark W. Woolrich,et al.  Large-scale Probabilistic Functional Modes from resting state fMRI , 2015, NeuroImage.

[136]  S. Kühn,et al.  Day2day: investigating daily variability of magnetic resonance imaging measures over half a year , 2017, BMC Neuroscience.

[137]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[138]  Á. Pascual-Leone,et al.  Prospective Validation That Subgenual Connectivity Predicts Antidepressant Efficacy of Transcranial Magnetic Stimulation Sites , 2017, Biological Psychiatry.

[139]  A. Hariri The Emerging Importance of the Cerebellum in Broad Risk for Psychopathology , 2019, Neuron.

[140]  Heping Zhang,et al.  Basal Ganglia volumes in patients with Gilles de la Tourette syndrome. , 2003, Archives of general psychiatry.

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

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

[143]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

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

[145]  Jack L. Gallant,et al.  A Continuous Semantic Space Describes the Representation of Thousands of Object and Action Categories across the Human Brain , 2012, Neuron.

[146]  M Deanna,et al.  Resting-State Functional Connectivity in the Human Connectome Project: Current Status and Relevance to Understanding Psychopathology. , 2017 .

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

[148]  Mark D'Esposito,et al.  Focal Brain Lesions to Critical Locations Cause Widespread Disruption of the Modular Organization of the Brain , 2012, Journal of Cognitive Neuroscience.

[149]  Steven E Petersen,et al.  Evaluating the Prediction of Brain Maturity From Functional Connectivity After Motion Artifact Denoising. , 2019, Cerebral cortex.