Lagged and instantaneous dynamical influences related to brain structural connectivity

Contemporary neuroimaging methods can shed light on the basis of human neural and cognitive specializations, with important implications for neuroscience and medicine. Indeed, different MRI acquisitions provide different brain networks at the macroscale; whilst diffusion-weighted MRI (dMRI) provides a structural connectivity (SC) coincident with the bundles of parallel fibers between brain areas, functional MRI (fMRI) accounts for the variations in the blood-oxygenation-level-dependent T2* signal, providing functional connectivity (FC). Understanding the precise relation between FC and SC, that is, between brain dynamics and structure, is still a challenge for neuroscience. To investigate this problem, we acquired data at rest and built the corresponding SC (with matrix elements corresponding to the fiber number between brain areas) to be compared with FC connectivity matrices obtained by three different methods: directed dependencies by an exploratory version of structural equation modeling (eSEM), linear correlations (C) and partial correlations (PC). We also considered the possibility of using lagged correlations in time series; in particular, we compared a lagged version of eSEM and Granger causality (GC). Our results were two-fold: firstly, eSEM performance in correlating with SC was comparable to those obtained from C and PC, but eSEM (not C, nor PC) provides information about directionality of the functional interactions. Second, interactions on a time scale much smaller than the sampling time, captured by instantaneous connectivity methods, are much more related to SC than slow directed influences captured by the lagged analysis. Indeed the performance in correlating with SC was much worse for GC and for the lagged version of eSEM. We expect these results to supply further insights to the interplay between SC and functional patterns, an important issue in the study of brain physiology and function.

[1]  Ning Yang,et al.  Greater Than the Sum of Its Parts , 2010, IEEE Microwave Magazine.

[2]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  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..

[4]  M. Greicius,et al.  Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity , 2009, Brain Structure and Function.

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

[6]  D. Chialvo,et al.  Enhanced repertoire of brain dynamical states during the psychedelic experience , 2014, Human brain mapping.

[7]  David A. Pierce,et al.  Measurement of Linear Dependence and Feedback Between Multiple Time Series: Comment , 1982 .

[8]  Richard F. Betzel,et al.  Resting-brain functional connectivity predicted by analytic measures of network communication , 2013, Proceedings of the National Academy of Sciences.

[9]  Daniele Marinazzo,et al.  Information Transfer and Criticality in the Ising Model on the Human Connectome , 2014, PloS one.

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

[11]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

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

[13]  Habib Benali,et al.  A Theoretical Investigation of the Relationship between Structural Equation Modeling and Partial Correlation in Functional MRI Effective Connectivity , 2009, Comput. Intell. Neurosci..

[14]  Yves Rosseel,et al.  lavaan: An R Package for Structural Equation Modeling , 2012 .

[15]  R. Schlösser,et al.  Assessing the working memory network: Studies with functional magnetic resonance imaging and structural equation modeling , 2006, Neuroscience.

[16]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[17]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[18]  Andreas Ritter,et al.  Structural Equations With Latent Variables , 2016 .

[19]  Daniele Marinazzo,et al.  Information Flow Between Resting-State Networks , 2015, Brain Connect..

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

[21]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

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

[23]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[24]  Daniele Marinazzo,et al.  Synergy and redundancy in the Granger causal analysis of dynamical networks , 2014, New Journal of Physics.

[25]  O. Sporns,et al.  An Anatomical Substrate for Integration among Functional Networks in Human Cortex , 2013, The Journal of Neuroscience.

[26]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

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

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

[29]  DiezIbai,et al.  Information Flow Between Resting-State Networks , 2015 .

[30]  Keith Heberlein,et al.  Imaging human connectomes at the macroscale , 2013, Nature Methods.

[31]  E. Bullmore,et al.  How Good Is Good Enough in Path Analysis of fMRI Data? , 2000, NeuroImage.

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

[33]  Marcus E Raichle,et al.  A Paradigm Shift in Functional Brain Imaging , 2009, The Journal of Neuroscience.

[34]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[35]  Peter J Hellyer,et al.  The entropic brain: a theory of conscious states informed by neuroimaging research with psychedelic drugs , 2014, Front. Hum. Neurosci..

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

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

[38]  D. Chialvo,et al.  Ising-like dynamics in large-scale functional brain networks. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  Dante R Chialvo,et al.  Brain organization into resting state networks emerges at criticality on a model of the human connectome. , 2012, Physical review letters.

[40]  H. Akaike A new look at the statistical model identification , 1974 .

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

[42]  Olaf Sporns,et al.  What Is the Human Connectome , 2009 .

[43]  Joaquín Goñi,et al.  Multi-scale integration and predictability in resting state brain activity , 2014, Front. Neuroinform..

[44]  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.

[45]  Pablo Balenzuela,et al.  Criticality in Large-Scale Brain fMRI Dynamics Unveiled by a Novel Point Process Analysis , 2012, Front. Physio..

[46]  Bruce G. Pollock,et al.  Age-related decline in white matter tract integrity and cognitive performance: A DTI tractography and structural equation modeling study , 2012, Neurobiology of Aging.

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

[48]  Kathleen M. Gates,et al.  Extended unified SEM approach for modeling event-related fMRI data , 2011, NeuroImage.

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

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

[51]  Michel A. Picardo,et al.  GABAergic Hub Neurons Orchestrate Synchrony in Developing Hippocampal Networks , 2009, Science.

[52]  M. A. Muñoz,et al.  A novel brain partition highlights the modular skeleton shared by structure and function , 2014, Scientific Reports.

[53]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[54]  Dante R Chialvo,et al.  Disruption of transfer entropy and inter-hemispheric brain functional connectivity in patients with disorder of consciousness , 2013, Front. Neuroinform..

[55]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[56]  Wei Zhu,et al.  Unified structural equation modeling approach for the analysis of multisubject, multivariate functional MRI data , 2007, Human brain mapping.

[57]  Guorong Wu,et al.  A blind deconvolution approach to recover effective connectivity brain networks from resting state fMRI data , 2012, Medical Image Anal..

[58]  Andreas Horn,et al.  The structural–functional connectome and the default mode network of the human brain , 2014, NeuroImage.

[59]  Kathleen M. Gates,et al.  Automatic search for fMRI connectivity mapping: An alternative to Granger causality testing using formal equivalences among SEM path modeling, VAR, and unified SEM , 2010, NeuroImage.