Identifying Sparse Connectivity Patterns in the brain using resting-state fMRI

The human brain processes information via multiple distributed networks. An accurate model of the brain's functional connectome is critical for understanding both normal brain function as well as the dysfunction present in neuropsychiatric illnesses. Current methodologies that attempt to discover the organization of the functional connectome typically assume spatial or temporal separation of the underlying networks. This assumption deviates from an intuitive understanding of brain function, which is that of multiple, inter-dependent spatially overlapping brain networks that efficiently integrate information pertinent to diverse brain functions. It is now increasingly evident that neural systems use parsimonious formations and functional representations to efficiently process information while minimizing redundancy. Hence we exploit recent advances in the mathematics of sparse modeling to develop a methodological framework aiming to understand complex resting-state fMRI connectivity data. By favoring networks that explain the data via a relatively small number of participating brain regions, we obtain a parsimonious representation of brain function in terms of multiple "Sparse Connectivity Patterns" (SCPs), such that differential presence of these SCPs explains inter-subject variability. In this manner the sparsity-based framework can effectively capture the heterogeneity of functional activity patterns across individuals while potentially highlighting multiple sub-populations within the data that display similar patterns. Our results from simulated as well as real resting state fMRI data show that SCPs are accurate and reproducible between sub-samples as well as across datasets. These findings substantiate existing knowledge of intrinsic functional connectivity and provide novel insights into the functional organization of the human brain.

[1]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[2]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[3]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[4]  Avrim Blum,et al.  Correlation Clustering , 2004, Machine Learning.

[5]  Anoop Cherian,et al.  Generalized Dictionary Learning for Symmetric Positive Definite Matrices with Application to Nearest Neighbor Retrieval , 2011, ECML/PKDD.

[6]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[7]  Shai Avidan,et al.  Spectral Bounds for Sparse PCA: Exact and Greedy Algorithms , 2005, NIPS.

[8]  Stephen M. Smith,et al.  Temporally-independent functional modes of spontaneous brain activity , 2012, Proceedings of the National Academy of Sciences.

[9]  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.

[10]  David M. Groppe,et al.  Neurophysiological Investigation of Spontaneous Correlated and Anticorrelated Fluctuations of the BOLD Signal , 2013, The Journal of Neuroscience.

[11]  Firdaus Janoos,et al.  State-Space Analysis of Working Memory in Schizophrenia: An FBIRN Study , 2013, Psychometrika.

[12]  Yong He,et al.  Stabilities of negative correlations between blood oxygen level‐dependent signals associated with sensory and motor cortices , 2007, Human brain mapping.

[13]  M E J Newman,et al.  Fast algorithm for detecting community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

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

[17]  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..

[18]  Christos Davatzikos,et al.  Discriminative Sparse Connectivity Patterns for Classification of fMRI Data , 2014, MICCAI.

[19]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

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

[21]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[22]  P. Golland,et al.  Whole brain resting state functional connectivity abnormalities in schizophrenia , 2012, Schizophrenia Research.

[23]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[25]  Josef Ling,et al.  Functional connectivity in mild traumatic brain injury , 2011, Human brain mapping.

[26]  Ben Taskar,et al.  Generative-Discriminative Basis Learning for Medical Imaging , 2012, IEEE Transactions on Medical Imaging.

[27]  Christos Davatzikos,et al.  Neuroimaging of the Philadelphia Neurodevelopmental Cohort , 2014, NeuroImage.

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

[29]  Vince D. Calhoun,et al.  ICA of functional MRI data: an overview. , 2003 .

[30]  J. Kruskal Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis , 1964 .

[31]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[32]  Martin J. McKeown,et al.  Group Replicator Dynamics: A Novel Group-Wise Evolutionary Approach for Sparse Brain Network Detection , 2012, IEEE Transactions on Medical Imaging.

[33]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

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

[35]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.

[36]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[37]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[38]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[39]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[40]  R. Gur,et al.  Association of enhanced limbic response to threat with decreased cortical facial recognition memory response in schizophrenia. , 2010, The American journal of psychiatry.

[41]  Alexandre d'Aspremont,et al.  Optimal Solutions for Sparse Principal Component Analysis , 2007, J. Mach. Learn. Res..

[42]  Dimitri Van De Ville,et al.  Principal components of functional connectivity: A new approach to study dynamic brain connectivity during rest , 2013, NeuroImage.

[43]  A. Hyvarinen,et al.  Fast ICA for noisy data using Gaussian moments , 1999, ISCAS'99. Proceedings of the 1999 IEEE International Symposium on Circuits and Systems VLSI (Cat. No.99CH36349).

[44]  V. Traag,et al.  Community detection in networks with positive and negative links. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[46]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[47]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[48]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Simon Baron-Cohen,et al.  Reduced functional connectivity within and between ‘social’ resting state networks in autism spectrum conditions , 2012, Social cognitive and affective neuroscience.

[50]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

[51]  Chris H. Q. Ding,et al.  K-means clustering via principal component analysis , 2004, ICML.

[52]  C. Ding,et al.  On the Equivalence of Nonnegative Matrix Factorization and K-means - Spectral Clustering , 2005 .

[53]  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.

[54]  Lester W. Mackey,et al.  Deflation Methods for Sparse PCA , 2008, NIPS.

[55]  Sune Lehmann,et al.  Link communities reveal multiscale complexity in networks , 2009, Nature.

[56]  G. Glover,et al.  Causal interactions between fronto-parietal central executive and default-mode networks in humans , 2013, Proceedings of the National Academy of Sciences.

[57]  Jean-Baptiste Poline,et al.  Brain covariance selection: better individual functional connectivity models using population prior , 2010, NIPS.

[58]  Olaf Sporns,et al.  Weight-conserving characterization of complex functional brain networks , 2011, NeuroImage.

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

[60]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[61]  Vassilios Morellas,et al.  Positive definite dictionary learning for region covariances , 2011, 2011 International Conference on Computer Vision.

[62]  Martin Rosvall,et al.  Maps of random walks on complex networks reveal community structure , 2007, Proceedings of the National Academy of Sciences.

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

[64]  J. Munkres ALGORITHMS FOR THE ASSIGNMENT AND TRANSIORTATION tROBLEMS* , 1957 .

[65]  Christos Davatzikos,et al.  Unsupervised Learning of Functional Network Dynamics in Resting State fMRI , 2013, IPMI.