Construction of functional brain connectivity networks from fMRI data with driving and modulatory inputs: an extended conditional Granger causality approach

We propose a numerical-based approach extending the conditional MVAR Granger causality (MVGC) analysis for the construction of directed connectivity networks in the presence of both exogenous/stimuli and modulatory inputs. The performance of the proposed scheme is validated using both synthetic stochastic data considering also the influence of haemodynamics latencies and a benchmark fMRI dataset related to the role of attention in the perception of visual motion. The particular fMRI dataset has been used in many studies to evaluate alternative model hypotheses using the Dynamic Causal Modelling (DCM) approach. Based on the use of the Bayes factor, we show that the obtained GC connectivity network compares well to a reference model that has been selected through DCM analysis among other candidate models. Thus, our findings suggest that the proposed scheme can be successfully used as a stand-alone or complementary to DCM approach to find directed causal connectivity patterns in task-related fMRI studies.

[1]  Constantinos I. Siettos,et al.  Children with well controlled epilepsy possess different spatio-temporal patterns of causal network connectivity during a visual working memory task , 2016, Cognitive Neurodynamics.

[2]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[3]  Karl J. Friston,et al.  The functional anatomy of attention to visual motion. A functional MRI study. , 1998, Brain : a journal of neurology.

[4]  C. Granger,et al.  Spurious regressions in econometrics , 1974 .

[5]  Dimitris Kugiumtzis,et al.  Correlation Networks for Identifying Changes in Brain Connectivity during Epileptiform Discharges and Transcranial Magnetic Stimulation , 2014, Sensors.

[6]  Mukesh Dhamala,et al.  Reduced Medial Prefrontal-Subcortical Connectivity in Dysphoria: Granger Causality Analyses of Rapid Functional Magnetic Resonance Imaging , 2015, Brain Connect..

[7]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[8]  Constantinos Siettos,et al.  Multiscale modeling of brain dynamics: from single neurons and networks to mathematical tools , 2016, Wiley interdisciplinary reviews. Systems biology and medicine.

[9]  Karl J. Friston,et al.  DCM for complex-valued data: Cross-spectra, coherence and phase-delays , 2012, NeuroImage.

[10]  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..

[11]  Antonis D. Savva,et al.  Assessment of dynamic functional connectivity in resting‐state fMRI using the sliding window technique , 2019, Brain and behavior.

[12]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

[13]  Ronen Talmon,et al.  Identifying preseizure state in intracranial EEG data using diffusion kernels. , 2013, Mathematical biosciences and engineering : MBE.

[14]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

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

[16]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[17]  Julius Georgiou,et al.  EEG-Based Automatic Classification of ‘Awake’ versus ‘Anesthetized’ State in General Anesthesia Using Granger Causality , 2012, PloS one.

[18]  Daniele Marinazzo,et al.  Functional and effective connectivity in EEG alpha and beta bands during intermittent flash stimulation in migraine with and without aura , 2013, Cephalalgia : an international journal of headache.

[19]  Anil K. Seth,et al.  The MVGC multivariate Granger causality toolbox: A new approach to Granger-causal inference , 2014, Journal of Neuroscience Methods.

[20]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[21]  K. Kendrick,et al.  Partial Granger causality—Eliminating exogenous inputs and latent variables , 2008, Journal of Neuroscience Methods.

[22]  A. Seth,et al.  Granger Causality Analysis in Neuroscience and Neuroimaging , 2015, The Journal of Neuroscience.

[23]  J. Tenenbaum,et al.  A global geometric framework for nonlinear dimensionality reduction. , 2000, Science.

[24]  Andrea Duggento,et al.  Multivariate Granger causality unveils directed parietal to prefrontal cortex connectivity during task-free MRI , 2018, Scientific Reports.

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

[26]  P. Lang,et al.  Re‐entrant projections modulate visual cortex in affective perception: Evidence from Granger causality analysis , 2009, Human brain mapping.

[27]  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.

[28]  Bharat B. Biswal,et al.  Resting state fMRI: A personal history , 2012, NeuroImage.

[29]  M. Boly,et al.  Granger Causality Analysis of Steady-State Electroencephalographic Signals during Propofol-Induced Anaesthesia , 2012, PloS one.

[30]  Constantinos I. Siettos,et al.  Granger causality analysis reveals distinct spatio-temporal connectivity patterns in motor and perceptual visuo-spatial working memory , 2014, Front. Comput. Neurosci..

[31]  Qing Gao,et al.  Evaluation of effective connectivity of motor areas during motor imagery and execution using conditional Granger causality , 2011, NeuroImage.

[32]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[33]  Edward T. Bullmore,et al.  On the use of correlation as a measure of network connectivity , 2012, NeuroImage.

[34]  Maurizio Corbetta,et al.  Measuring Granger Causality between Cortical Regions from Voxelwise fMRI BOLD Signals with LASSO , 2012, PLoS Comput. Biol..

[35]  Seppo P. Ahlfors,et al.  Lexical influences on speech perception: A Granger causality analysis of MEG and EEG source estimates , 2008, NeuroImage.

[36]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[37]  M. Brazier Spread of seizure discharges in epilepsy: anatomical and electrophysiological considerations. , 1972, Experimental neurology.

[38]  Anil K. Seth,et al.  Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling , 2013, NeuroImage.

[39]  Christopher P. Said,et al.  Top-down attention switches coupling between low-level and high-level areas of human visual cortex , 2012, Proceedings of the National Academy of Sciences.

[40]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[41]  Jianfeng Feng,et al.  Granger causality vs. dynamic Bayesian network inference: a comparative study , 2009, BMC Bioinformatics.

[42]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[43]  Mingzhou Ding,et al.  Analyzing information flow in brain networks with nonparametric Granger causality , 2008, NeuroImage.

[44]  Mark S. Cohen,et al.  Decreased small-world functional network connectivity and clustering across resting state networks in schizophrenia: an fMRI classification tutorial , 2013, Front. Hum. Neurosci..

[45]  Mikko Sams,et al.  Functional Magnetic Resonance Imaging Phase Synchronization as a Measure of Dynamic Functional Connectivity , 2012, Brain Connect..

[46]  Qiang Xu,et al.  Small-world directed networks in the human brain: Multivariate Granger causality analysis of resting-state fMRI , 2011, NeuroImage.

[47]  Gordon Pipa,et al.  Transfer entropy—a model-free measure of effective connectivity for the neurosciences , 2010, Journal of Computational Neuroscience.

[48]  W. Kuo,et al.  Increasing fMRI Sampling Rate Improves Granger Causality Estimates , 2014, PloS one.

[49]  Jianfeng Feng,et al.  A Novel Extended Granger Causal Model Approach Demonstrates Brain Hemispheric Differences during Face Recognition Learning , 2009, PLoS Comput. Biol..

[50]  Karl J. Friston,et al.  Analysing connectivity with Granger causality and dynamic causal modelling , 2013, Current Opinion in Neurobiology.

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

[52]  Anil K. Seth,et al.  A MATLAB toolbox for Granger causal connectivity analysis , 2010, Journal of Neuroscience Methods.

[53]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[54]  Bjorn Roelstraete,et al.  Does partial Granger causality really eliminate the influence of exogenous inputs and latent variables? , 2012, Journal of Neuroscience Methods.

[55]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[56]  D Marinazzo,et al.  Recovering directed networks in neuroimaging datasets using partially conditioned Granger causality , 2013, BMC Neuroscience.

[57]  George L. Gerstein,et al.  Identification of functionally related neural assemblies , 1978, Brain Research.

[58]  Dimitris Kugiumtzis,et al.  Non-uniform state space reconstruction and coupling detection , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[59]  Dongrong Xu,et al.  A conditional Granger causality model approach for group analysis in functional magnetic resonance imaging. , 2011, Magnetic resonance imaging.

[60]  Joachim Gross,et al.  The effect of filtering on Granger causality based multivariate causality measures , 2010, NeuroImage.

[61]  Karl J. Friston,et al.  Modelling functional integration: a comparison of structural equation and dynamic causal models , 2004, NeuroImage.

[62]  Li Yao,et al.  Altered Connectivity Pattern of Hubs in Default-Mode Network with Alzheimer's Disease: An Granger Causality Modeling Approach , 2011, PloS one.

[63]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[64]  S. Bressler,et al.  Granger Causality: Basic Theory and Application to Neuroscience , 2006, q-bio/0608035.

[65]  A. Seth,et al.  Behaviour of Granger causality under filtering: Theoretical invariance and practical application , 2011, Journal of Neuroscience Methods.

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

[67]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[68]  A. C. Papanicolaou,et al.  Modular Patterns of Phase Desynchronization Networks During a Simple Visuomotor Task , 2015, Brain Topography.

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

[70]  C. Stam,et al.  Phase lag index: Assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources , 2007, Human brain mapping.

[71]  Amiram Grinvald,et al.  Independent component analysis of high-resolution imaging data identifies distinct functional domains , 2007, NeuroImage.

[72]  Karl J. Friston,et al.  Bridging the Gap: Dynamic Causal Modeling and Granger Causality Analysis of Resting State Functional Magnetic Resonance Imaging , 2016, Brain Connect..