Spatio-temporal modeling of connectome-scale brain network interactions via time-evolving graphs

ABSTRACT Many recent literature studies have revealed interesting dynamics patterns of functional brain networks derived from fMRI data. However, it has been rarely explored how functional networks spatially overlap (or interact) and how such connectome‐scale network interactions temporally evolve. To explore these unanswered questions, this paper presents a novel framework for spatio‐temporal modeling of connectome‐scale functional brain network interactions via two main effective computational methodologies. First, to integrate, pool and compare brain networks across individuals and their cognitive states under task performances, we designed a novel group‐wise dictionary learning scheme to derive connectome‐scale consistent brain network templates that can be used to define the common reference space of brain network interactions. Second, the temporal dynamics of spatial network interactions is modeled by a weighted time‐evolving graph, and then a data‐driven unsupervised learning algorithm based on the dynamic behavioral mixed‐membership model (DBMM) is adopted to identify behavioral patterns of brain networks during the temporal evolution process of spatial overlaps/interactions. Experimental results on the Human Connectome Project (HCP) task fMRI data showed that our methods can reveal meaningful, diverse behavior patterns of connectome‐scale network interactions. In particular, those networks’ behavior patterns are distinct across HCP tasks such as motor, working memory, language and social tasks, and their dynamics well correspond to the temporal changes of specific task designs. In general, our framework offers a new approach to characterizing human brain function by quantitative description for the temporal evolution of spatial overlaps/interactions of connectome‐scale brain networks in a standard reference space.

[1]  William H. Thompson,et al.  The frequency dimension of fMRI dynamic connectivity: Network connectivity, functional hubs and integration in the resting brain , 2015, NeuroImage.

[2]  Waqas Majeed,et al.  Spatiotemporal dynamics of low frequency BOLD fluctuations in rats and humans , 2011, NeuroImage.

[3]  Guimei Liu,et al.  Complex discovery from weighted PPI networks , 2009, Bioinform..

[4]  Delbert Dueck,et al.  Clustering by Passing Messages Between Data Points , 2007, Science.

[5]  Florence Thibaut,et al.  New ways of understanding brain neurocircuitry , 2018, Dialogues in clinical neuroscience.

[6]  Jieping Ye,et al.  Holistic Atlases of Functional Networks and Interactions Reveal Reciprocal Organizational Architecture of Cortical Function , 2015, IEEE Transactions on Biomedical Engineering.

[7]  Steven L. Bressler,et al.  Past Makes Future: Role of pFC in Prediction , 2015, Journal of Cognitive Neuroscience.

[8]  András Jánossy,et al.  “高磁場Gd3+電子スピン共鳴により測定したYBa2Cu4O8における磁場誘起低エネルギースピン励起”へのコメント , 2001 .

[9]  V. D. Calhoun,et al.  Increased spatial granularity of left brain activation and unique age/gender signatures: a 4D frequency domain approach to cerebral lateralization at rest , 2016, Brain Imaging and Behavior.

[10]  D. Shen,et al.  DICCCOL: dense individualized and common connectivity-based cortical landmarks. , 2013, Cerebral cortex.

[11]  Xin Zhang,et al.  Characterization of task-free and task-performance brain states via functional connectome patterns , 2013, Medical Image Anal..

[12]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[13]  Dajiang Zhu,et al.  Dynamic functional connectomics signatures for characterization and differentiation of PTSD patients , 2014, Human brain mapping.

[14]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[15]  C. Gilbert,et al.  Brain States: Top-Down Influences in Sensory Processing , 2007, Neuron.

[16]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[17]  Dinggang Shen,et al.  Reveal Consistent Spatial-Temporal Patterns from Dynamic Functional Connectivity for Autism Spectrum Disorder Identification , 2016, MICCAI.

[18]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

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

[20]  Jinglei Lv,et al.  A Multi-stage Sparse Coding Framework to Explore the Effects of Prenatal Alcohol Exposure , 2016, MICCAI.

[21]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[22]  J. Rissanen,et al.  Modeling By Shortest Data Description* , 1978, Autom..

[23]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[24]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

[25]  Malek Adjouadi,et al.  ICA-based connectivity on brain networks using fMRI , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[26]  O. Tervonen,et al.  Functional segmentation of the brain cortex using high model order group-PICA. , 2009, NeuroImage.

[27]  R. Kahn,et al.  Functional network topology associated with posttraumatic stress disorder in veterans , 2015, NeuroImage: Clinical.

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

[29]  Aaron Kucyi,et al.  Disrupted functional connectivity of cerebellar default network areas in attention‐deficit/hyperactivity disorder , 2015, Human brain mapping.

[30]  Christos Faloutsos,et al.  It's who you know: graph mining using recursive structural features , 2011, KDD.

[31]  J. M. Moran,et al.  Large-scale functional network overlap is a general property of brain functional organization: Reconciling inconsistent fMRI findings from general-linear-model-based analyses , 2016, Neuroscience & Biobehavioral Reviews.

[32]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

[33]  Junwei Han,et al.  Inferring functional interaction and transition patterns via dynamic bayesian variable partition models , 2013, Human brain mapping.

[34]  Heng Huang,et al.  Sparse representation of whole-brain fMRI signals for identification of functional networks , 2015, Medical Image Anal..

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

[36]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[37]  Shella D. Keilholz,et al.  The Neural Basis of Time-Varying Resting-State Functional Connectivity , 2014, Brain Connect..

[38]  Alex Arenas,et al.  Mapping Multiplex Hubs in Human Functional Brain Networks , 2016, Front. Neurosci..

[39]  Kathryn R. Cullen,et al.  Network analysis of functional brain connectivity in borderline personality disorder using resting-state fMRI , 2016, NeuroImage: Clinical.

[40]  Jinglei Lv,et al.  Temporal Concatenated Sparse Coding of Resting State fMRI Data Reveal Network Interaction Changes in mTBI , 2016, MICCAI.

[41]  Ryan A. Rossi,et al.  Modeling dynamic behavior in large evolving graphs , 2013, WSDM.

[42]  Guillermo Sapiro,et al.  Online Learning for Matrix Factorization and Sparse Coding , 2009, J. Mach. Learn. Res..

[43]  Yufeng Wang,et al.  Atomic dynamic functional interaction patterns for characterization of ADHD , 2014, Human brain mapping.

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

[45]  Tyge Dahl Hermansen,et al.  Human Development XI: The Structure of the Cerebral Cortex. Are There Really Modules in the Brain? , 2007, TheScientificWorldJournal.

[46]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[47]  Victor Solo,et al.  Brain Activity: Connectivity, Sparsity, and Mutual Information , 2015, IEEE Transactions on Medical Imaging.

[48]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[49]  C. Fiebach,et al.  Predicting errors from reconfiguration patterns in human brain networks , 2012, Proceedings of the National Academy of Sciences.

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

[51]  Chin-Hui Lee,et al.  Evaluation of sliding window correlation performance for characterizing dynamic functional connectivity and brain states , 2016, NeuroImage.