Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity

Functional magnetic resonance imaging (fMRI) studies typically collapse data from many subjects, but brain functional organization varies between individuals. Here we establish that this individual variability is both robust and reliable, using data from the Human Connectome Project to demonstrate that functional connectivity profiles act as a 'fingerprint' that can accurately identify subjects from a large group. Identification was successful across scan sessions and even between task and rest conditions, indicating that an individual's connectivity profile is intrinsic, and can be used to distinguish that individual regardless of how the brain is engaged during imaging. Characteristic connectivity patterns were distributed throughout the brain, but the frontoparietal network emerged as most distinctive. Furthermore, we show that connectivity profiles predict levels of fluid intelligence: the same networks that were most discriminating of individuals were also most predictive of cognitive behavior. Results indicate the potential to draw inferences about single subjects on the basis of functional connectivity fMRI.

[1]  R. Cattell Intelligence : its structure, growth and action , 1987 .

[2]  M. Groot,et al.  A R T I C L E S COSMOLOGY AND GENESIS: THE ROAD TO HARMONY AND THE NEED FOR COSMOLOGICAL ALTERNATIVES , 1992 .

[3]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  K. Amunts,et al.  Brodmann's Areas 17 and 18 Brought into Stereotaxic Space—Where and How Variable? , 2000, NeuroImage.

[5]  Ian J. Deary,et al.  The Stability of Individual Differences in Mental Ability from Childhood to Old Age: Follow-up of the 1932 Scottish Mental Survey , 2000 .

[6]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[7]  Sharlene D. Newman,et al.  Frontal and parietal participation in problem solving in the Tower of London: fMRI and computational modeling of planning and high-level perception , 2003, Neuropsychologia.

[8]  L. Gottfredson,et al.  Intelligence: is it the epidemiologists' elusive "fundamental cause" of social class inequalities in health? , 2004, Journal of personality and social psychology.

[9]  Tianzi Jiang,et al.  Modulation of functional connectivity during the resting state and the motor task , 2004, Human brain mapping.

[10]  E. Duchesnay,et al.  A framework to study the cortical folding patterns , 2004, NeuroImage.

[11]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[12]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[13]  I J Deary,et al.  Childhood IQ in relation to obesity and weight gain in adult life: the National Child Development (1958) Study , 2005, International Journal of Obesity.

[14]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[15]  Roberto Colom,et al.  Intelligence predicts scholastic achievement irrespective of SES factors: Evidence from Brazil , 2007 .

[16]  Christa Neuper,et al.  Individual differences in mathematical competence predict parietal brain activation during mental calculation , 2007, NeuroImage.

[17]  Tarmo Strenze Intelligence and socioeconomic success: A meta-analytic review of longitudinal research ☆ , 2007 .

[18]  Noah A. Shamosh,et al.  Multiple Bases of Human Intelligence Revealed by Cortical Thickness and Neural Activation , 2008, The Journal of Neuroscience.

[19]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[20]  Edward T. Bullmore,et al.  Age-related changes in modular organization of human brain functional networks , 2009, NeuroImage.

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

[22]  Jeff H. Duyn,et al.  Modulation of spontaneous fMRI activity in human visual cortex by behavioral state , 2009, NeuroImage.

[23]  Dustin Scheinost,et al.  Unified Framework for Development, Deployment and Robust Testing of Neuroimaging Algorithms , 2011, Neuroinformatics.

[24]  T. Insel,et al.  Wesleyan University From the SelectedWorks of Charles A . Sanislow , Ph . D . 2010 Research Domain Criteria ( RDoC ) : Toward a New Classification Framework for Research on Mental Disorders , 2018 .

[25]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[26]  Timothy S. Coalson,et al.  A Surface-Based Analysis of Hemispheric Asymmetries and Folding of Cerebral Cortex in Term-Born Human Infants , 2010, The Journal of Neuroscience.

[27]  R. Todd Constable,et al.  Functional connectivity and alterations in baseline brain state in humans , 2010, NeuroImage.

[28]  D. Schacter,et al.  Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. , 2010, Cerebral cortex.

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

[30]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

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

[32]  G. Rees,et al.  The structural basis of inter-individual differences in human behaviour and cognition , 2011, Nature Reviews Neuroscience.

[33]  B. Biswal,et al.  Characterizing variation in the functional connectome: promise and pitfalls , 2012, Trends in Cognitive Sciences.

[34]  Michael W. Cole,et al.  Global Connectivity of Prefrontal Cortex Predicts Cognitive Control and Intelligence , 2012, The Journal of Neuroscience.

[35]  Dustin Scheinost,et al.  Intrinsic Brain Connectivity Related to Age in Young and Middle Aged Adults , 2012, PloS one.

[36]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

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

[38]  R. Gur,et al.  Development of Abbreviated Nine-Item Forms of the Raven’s Standard Progressive Matrices Test , 2012, Assessment.

[39]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[40]  B. Harrison,et al.  Brain Connectivity and Mental Illness , 2012, Front. Psychiatry.

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

[42]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[43]  Xenophon Papademetris,et al.  Groupwise whole-brain parcellation from resting-state fMRI data for network node identification , 2013, NeuroImage.

[44]  R. Cameron Craddock,et al.  Clinical applications of the functional connectome , 2013, NeuroImage.

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

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

[47]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[48]  T. Insel,et al.  Toward the future of psychiatric diagnosis: the seven pillars of RDoC , 2013, BMC Medicine.

[49]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

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

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

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

[53]  Satrajit S. Ghosh,et al.  Prediction as a Humanitarian and Pragmatic Contribution from Human Cognitive Neuroscience , 2015, Neuron.

[54]  Dustin Scheinost,et al.  Sex differences in normal age trajectories of functional brain networks , 2015, Human brain mapping.