Explicitly Linking Regional Activation and Function Connectivity: Community Structure of Weighted Networks with Continuous Annotation

A major challenge in neuroimaging is understanding the mapping of neurophysiological dynamics onto cognitive functions. Traditionally, these maps have been constructed by examining changes in the activity magnitude of regions related to task performance. Recently, network neuroscience has produced methods to map connectivity patterns among many regions to certain cognitive functions by drawing on tools from network science and graph theory. However, these two different views are rarely addressed simultaneously, largely because few tools exist that account for patterns between nodes while simultaneously considering activation of nodes. We address this gap by solving the problem of community detection on weighted networks with continuous (non-integer) annotations by deriving a generative probabilistic model. This model generates communities whose members connect densely to nodes within their own community, and whose members share similar annotation values. We demonstrate the utility of the model in the context of neuroimaging data gathered during a motor learning paradigm, where edges are task-based functional connectivity and annotations to each node are beta weights from a general linear model that encoded a linear decrease in blood-oxygen-level-dependent signal with practice. Interestingly, we observe that individuals who learn at a faster rate exhibit the greatest dissimilarity between functional connectivity and activation magnitudes, suggesting that activation and functional connectivity are distinct dimensions of neurophysiology that track behavioral change. More generally, the tool that we develop offers an explicit, mathematically principled link between functional activation and functional connectivity, and can readily be applied to a other similar problems in which one set of imaging data offers network data, and a second offers a regional attribute.

[1]  Emmanuel Abbe,et al.  Recovering Communities in the General Stochastic Block Model Without Knowing the Parameters , 2015, NIPS.

[2]  F. Donders On the speed of mental processes. , 1969, Acta psychologica.

[3]  Matthew R. G. Brown,et al.  Neural processes associated with antisaccade task performance investigated with event-related FMRI. , 2005, Journal of neurophysiology.

[4]  Jure Leskovec,et al.  Community Detection in Networks with Node Attributes , 2013, 2013 IEEE 13th International Conference on Data Mining.

[5]  D. Bassett,et al.  Functionalization of a protosynaptic gene expression network , 2012, Proceedings of the National Academy of Sciences.

[6]  L. Xu,et al.  Motor execution and motor imagery: A comparison of functional connectivity patterns based on graph theory , 2014, Neuroscience.

[7]  N. Volkow,et al.  Functional connectivity and brain activation: a synergistic approach. , 2014, Cerebral cortex.

[8]  R. L Gould,et al.  FMRI BOLD response to increasing task difficulty during successful paired associates learning , 2003, NeuroImage.

[9]  Barbora Micenková,et al.  Clustering attributed graphs: Models, measures and methods , 2015, Network Science.

[10]  Edward T. Bullmore,et al.  Small-World Brain Networks Revisited , 2016, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[11]  Kaustubh Supekar,et al.  Brain hyperconnectivity in children with autism and its links to social deficits. , 2013, Cell reports.

[12]  Mark E. J. Newman,et al.  Structure and inference in annotated networks , 2015, Nature Communications.

[13]  D. Bassett,et al.  Staged miRNA re-regulation patterns during reprogramming , 2013, Genome Biology.

[14]  Yuan Zhang,et al.  Community Detection in Networks with Node Features , 2015, Electronic Journal of Statistics.

[15]  Bryon A. Mueller,et al.  Altered resting state complexity in schizophrenia , 2012, NeuroImage.

[16]  E. Bullmore,et al.  Human brain networks in health and disease , 2009, Current opinion in neurology.

[17]  Varun Jog,et al.  Information-theoretic bounds for exact recovery in weighted stochastic block models using the Renyi divergence , 2015, ArXiv.

[18]  Mason A. Porter,et al.  Dynamic network centrality summarizes learning in the human brain , 2012, J. Complex Networks.

[19]  R. Poldrack Can cognitive processes be inferred from neuroimaging data? , 2006, Trends in Cognitive Sciences.

[20]  Jing Zhao,et al.  Prediction of Links and Weights in Networks by Reliable Routes , 2015, Scientific Reports.

[21]  R. Cabeza Cognitive neuroscience of aging: contributions of functional neuroimaging. , 2001, Scandinavian journal of psychology.

[22]  V. Paxson,et al.  Notices of the American Mathematical Society , 1998 .

[23]  Scott T Grafton,et al.  The Human Motor System Supports Sequence-Specific Representations over Multiple Training-Dependent Timescales. , 2015, Cerebral cortex.

[24]  Richard Coppola,et al.  Intra- and Inter-Frequency Brain Network Structure in Health and Schizophrenia , 2012, PloS one.

[25]  Jukka-Pekka Onnela,et al.  Taxonomies of networks from community structure. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[26]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  A. Malhotra,et al.  Antipsychotic treatment and functional connectivity of the striatum in first-episode schizophrenia. , 2015, JAMA psychiatry.

[28]  Cristopher Moore,et al.  Asymptotic analysis of the stochastic block model for modular networks and its algorithmic applications , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[29]  Danielle S Bassett,et al.  Evolution of network architecture in a granular material under compression. , 2016, Physical review. E.

[30]  S. Rossi,et al.  Efficiency of weak brain connections support general cognitive functioning , 2014, Human brain mapping.

[31]  Santo Fortunato,et al.  Network structure, metadata and the prediction of missing nodes , 2016, ArXiv.

[32]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Patrick Dupont,et al.  Motor learning-induced changes in functional brain connectivity as revealed by means of graph-theoretical network analysis , 2012, NeuroImage.

[34]  V. Calhoun,et al.  Disrupted correlation between low frequency power and connectivity strength of resting state brain networks in schizophrenia , 2013, Schizophrenia Research.

[35]  Thomas E. Nichols,et al.  Brain Network Analysis: Separating Cost from Topology Using Cost-Integration , 2011, PloS one.

[36]  E. Bullmore,et al.  The relationship between regional and inter‐regional functional connectivity deficits in schizophrenia , 2012, Human brain mapping.

[37]  Aaron Clauset,et al.  Learning Latent Block Structure in Weighted Networks , 2014, J. Complex Networks.

[38]  Danielle S. Bassett,et al.  Choosing Wavelet Methods, Filters, and Lengths for Functional Brain Network Construction , 2015, PloS one.

[39]  Benjamin J. Shannon,et al.  Brain aerobic glycolysis and motor adaptation learning , 2016, Proceedings of the National Academy of Sciences.

[40]  Danielle S. Bassett,et al.  Detecting hierarchical 3-D genome domain reconfiguration with network modularity , 2016, bioRxiv.

[41]  M. Ghilardi,et al.  Patterns of regional brain activation associated with different forms of motor learning , 2000, Brain Research.

[42]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[43]  Andrea Lancichinetti,et al.  Community detection algorithms: a comparative analysis: invited presentation, extended abstract , 2009, VALUETOOLS.

[44]  Liang Wang,et al.  Dynamic functional reorganization of the motor execution network after stroke. , 2010, Brain : a journal of neurology.

[45]  Emmanuel Abbe,et al.  Community detection in general stochastic block models: fundamental limits and efficient recovery algorithms , 2015, ArXiv.

[46]  Danielle S Bassett,et al.  Learning-induced autonomy of sensorimotor systems , 2014, Nature Neuroscience.

[47]  Danielle S Bassett,et al.  Extraction of force-chain network architecture in granular materials using community detection. , 2014, Soft matter.

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

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

[50]  Jari Saramäki,et al.  Adding network structure onto the map of collective behavior. , 2014, The Behavioral and brain sciences.

[51]  Danielle S. Bassett,et al.  Multi-scale brain networks , 2016, NeuroImage.

[52]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[53]  Santo Fortunato,et al.  Community detection in graphs , 2009, ArXiv.

[54]  B. J. Casey,et al.  What have we learned about cognitive development from neuroimaging? , 2006, Neuropsychologia.

[55]  Danielle S Bassett,et al.  Cross-linked structure of network evolution. , 2013, Chaos.

[56]  M E J Newman,et al.  Modularity and community structure in networks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Dustin Scheinost,et al.  The (in)stability of functional brain network measures across thresholds , 2015, NeuroImage.

[58]  Aaron Clauset,et al.  Adapting the Stochastic Block Model to Edge-Weighted Networks , 2013, ArXiv.

[59]  Brian C. Ross Mutual Information between Discrete and Continuous Data Sets , 2014, PloS one.

[60]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[61]  Mark E. J. Newman,et al.  Stochastic blockmodels and community structure in networks , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[62]  Mason A. Porter,et al.  Comparing Community Structure to Characteristics in Online Collegiate Social Networks , 2008, SIAM Rev..

[63]  Mason A. Porter,et al.  Task-Based Core-Periphery Organization of Human Brain Dynamics , 2012, PLoS Comput. Biol..

[64]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[65]  Kathryn B. Laskey,et al.  Stochastic blockmodels: First steps , 1983 .

[66]  Deborah Yurgelun-Todd,et al.  Stroop Performance in Normal Control Subjects: An fMRI Study , 2002, NeuroImage.

[67]  E. Bullmore,et al.  Whole-brain functional hypoconnectivity as an endophenotype of autism in adolescents , 2015, NeuroImage: Clinical.

[68]  M. Kawato,et al.  Functional MRI neurofeedback training on connectivity between two regions induces long-lasting changes in intrinsic functional network , 2015, Front. Hum. Neurosci..

[69]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[70]  P. Matthews,et al.  Distinguishable brain activation networks for short- and long-term motor skill learning. , 2005, Journal of neurophysiology.

[71]  Emmanuel Abbe,et al.  Exact Recovery in the Stochastic Block Model , 2014, IEEE Transactions on Information Theory.

[72]  M. Gazzaniga,et al.  Cognitive Neuroscience: The Biology of the Mind , 1998 .