Analysis of fMRI data using noise-diffusion network models: a new covariance-coding perspective

Since the middle of the 1990s, studies of resting-state fMRI/BOLD data have explored the correlation patterns of activity across the whole brain, which is referred to as functional connectivity (FC). Among the many methods that have been developed to interpret FC, a recently proposed model-based approach describes the propagation of fluctuating BOLD activity within the recurrently connected brain network by inferring the effective connectivity (EC). In this model, EC quantifies the strengths of directional interactions between brain regions, viewed from the proxy of BOLD activity. In addition, the tuning procedure for the model provides estimates for the local variability (input variances) to explain how the observed FC is generated. Generalizing, the network dynamics can be studied in the context of an input–output mapping—determined by EC—for the second-order statistics of fluctuating nodal activities. The present paper focuses on the following detection paradigm: observing output covariances, how discriminative is the (estimated) network model with respect to various input covariance patterns? An application with the model fitted to experimental fMRI data—movie viewing versus resting state—illustrates that changes in local variability and changes in brain coordination go hand in hand.

[1]  Patrice Abry,et al.  Interplay between functional connectivity and scale-free dynamics in intrinsic fMRI networks , 2014, NeuroImage.

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

[3]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[5]  Fred Wolf,et al.  Flexible information routing by transient synchrony , 2017, Nature Neuroscience.

[6]  Karl J. Friston,et al.  Effective connectivity: Influence, causality and biophysical modeling , 2011, NeuroImage.

[7]  J. Kurths,et al.  Exploring Brain Function from Anatomical Connectivity , 2011, Front. Neurosci..

[8]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

[9]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[10]  D. Heeger,et al.  In this issue , 2002, Nature Reviews Drug Discovery.

[11]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[12]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[13]  Luke J. Chang,et al.  A Sensitive and Specific Neural Signature for Picture-Induced Negative Affect , 2015, PLoS biology.

[14]  Adeel Razi,et al.  A DCM for resting state fMRI , 2014, NeuroImage.

[15]  Somwrita Sarkar,et al.  Inference of direct and multistep effective connectivities from functional connectivity of the brain and of relationships to cortical geometry , 2017, Journal of Neuroscience Methods.

[16]  Morten L. Kringelbach,et al.  Functional complexity emerging from anatomical constraints in the brain: the significance of network modularity and rich-clubs , 2016, Scientific Reports.

[17]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[18]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[19]  Rainer Goebel,et al.  Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. , 2003, Magnetic resonance imaging.

[20]  Morten L. Kringelbach,et al.  The most relevant human brain regions for functional connectivity: Evidence for a dynamical workspace of binding nodes from whole-brain computational modelling , 2017, NeuroImage.

[21]  Viktor K. Jirsa,et al.  The Virtual Brain: a simulator of primate brain network dynamics , 2013, Front. Neuroinform..

[22]  C. Mathys,et al.  Computational approaches to psychiatry , 2014, Current Opinion in Neurobiology.

[23]  David B. Grayden,et al.  Estimation of effective connectivity via data-driven neural modeling , 2014, Front. Neurosci..

[24]  Matthieu Gilson,et al.  Subject- and behavior-specific signatures extracted from fMRI data using whole-brain effective connectivity , 2017, bioRxiv.

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

[26]  Olaf Sporns,et al.  The human connectome: Origins and challenges , 2013, NeuroImage.

[27]  M. Kringelbach,et al.  Great Expectations: Using Whole-Brain Computational Connectomics for Understanding Neuropsychiatric Disorders , 2014, Neuron.

[28]  Mark P Richardson,et al.  Large scale brain models of epilepsy: dynamics meets connectomics , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[29]  B. Rosen,et al.  Functional Studies of the Human Brain Using High‐speed Magnetic Resonance Imaging , 1991, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[30]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[31]  Seungjin Choi,et al.  Natural Gradient Learning for Spatio-Temporal Decorrelation: Recurrent Network , 2000 .

[32]  Matthieu Gilson,et al.  Extracting orthogonal subject- and behavior-specific signatures from fMRI data using whole-brain effective connectivity (Version posted online February 12, 2018) , 2017 .

[33]  G. Tononi,et al.  Rethinking segregation and integration: contributions of whole-brain modelling , 2015, Nature Reviews Neuroscience.

[34]  Olaf Sporns,et al.  Can structure predict function in the human brain? , 2010, NeuroImage.

[35]  Matthieu Gilson,et al.  Effective connectivity inferred from fMRI transition dynamics during movie viewing points to a balanced reconfiguration of cortical interactions , 2017, NeuroImage.

[36]  A. Engel,et al.  Intrinsic Coupling Modes: Multiscale Interactions in Ongoing Brain Activity , 2013, Neuron.

[37]  Helen Shen,et al.  Neuroscience: Tuning the brain , 2014, Nature.

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

[39]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[40]  Habib Benali,et al.  Relating Structure and Function in the Human Brain: Relative Contributions of Anatomy, Stationary Dynamics, and Non-stationarities , 2014, PLoS Comput. Biol..

[41]  Helmut Ltkepohl,et al.  New Introduction to Multiple Time Series Analysis , 2007 .

[42]  Karl J. Friston,et al.  Structural and Functional Brain Networks: From Connections to Cognition , 2013, Science.

[43]  M. Raichle,et al.  Lag structure in resting-state fMRI. , 2014, Journal of neurophysiology.

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

[45]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

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

[47]  Viktor K. Jirsa,et al.  An automated pipeline for constructing personalized virtual brains from multimodal neuroimaging data , 2015, NeuroImage.

[48]  Duncan L. Turner,et al.  Real-time functional magnetic resonance imaging neurofeedback in motor neurorehabilitation , 2016, Current opinion in neurology.

[49]  Gustavo Deco,et al.  Role of local network oscillations in resting-state functional connectivity , 2011, NeuroImage.

[50]  Annette Witt,et al.  Dynamic Effective Connectivity of Inter-Areal Brain Circuits , 2011, PLoS Comput. Biol..

[51]  Biyu J. He Scale-Free Properties of the Functional Magnetic Resonance Imaging Signal during Rest and Task , 2011, The Journal of Neuroscience.

[52]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

[53]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[54]  Lucina Q. Uddin,et al.  Combining region- and network-level brain-behavior relationships in a structural equation model , 2018, NeuroImage.

[55]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

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

[57]  Matthew J. Brookes,et al.  The relationship between MEG and fMRI , 2014, NeuroImage.

[58]  Enzo Tagliazucchi,et al.  Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep , 2015, eLife.

[59]  Cleofé Peña-Gómez,et al.  Brain connectivity during resting state and subsequent working memory task predicts behavioural performance , 2012, Cortex.

[60]  Matthieu Gilson,et al.  Estimation of Directed Effective Connectivity from fMRI Functional Connectivity Hints at Asymmetries of Cortical Connectome , 2016, PLoS Comput. Biol..

[61]  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.