Using structural connectivity to augment community structure in EEG functional connectivity

Recently, EEG recording techniques and source analysis have improved, making it feasible to tap into fast network dynamics. Yet, analyzing whole-cortex EEG signals in source space is not standard, partly because EEG suffers from volume conduction: Functional connectivity (FC) reflecting genuine functional relationships is impossible to disentangle from spurious FC introduced by volume conduction. Here, we investigate the relationship between white matter structural connectivity (SC) and large-scale network structure encoded in EEG-FC. We start by confirming that FC (power envelope correlations) is predicted by SC beyond the impact of Euclidean distance, in line with the assumption that SC mediates genuine FC. We then use information from white matter structural connectivity in order to smooth the EEG signal in the space spanned by graphs derived from SC. Thereby, FC between nearby, structurally connected brain regions increases while FC between nonconnected regions remains unchanged, resulting in an increase in genuine, SC-mediated FC. We analyze the induced changes in FC, assessing the resemblance between EEG-FC and volume-conduction- free fMRI-FC, and find that smoothing increases resemblance in terms of overall correlation and community structure. This result suggests that our method boosts genuine FC, an outcome that is of interest for many EEG network neuroscience questions.

[1]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[2]  Richard F. Betzel,et al.  Distance-dependent consensus thresholds for generating group-representative structural brain networks , 2019, Network Neuroscience.

[3]  Li Ke,et al.  On σ-mapping , 2000 .

[4]  Matti S. Hämäläinen,et al.  EEG functional connectivity is partially predicted by underlying white matter connectivity , 2015, NeuroImage.

[5]  Hamid Reza Mohseni,et al.  Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations , 2014, NeuroImage.

[6]  Mark W. Woolrich,et al.  Measuring functional connectivity in MEG: A multivariate approach insensitive to linear source leakage , 2012, NeuroImage.

[7]  Jorge Bosch-Bayard,et al.  Innovations orthogonalization: a solution to the major pitfalls of EEG/MEG “leakage correction” , 2017, bioRxiv.

[8]  Alain Giron,et al.  Predicting functional connectivity from structural connectivity via computational models using MRI: An extensive comparison study , 2015, NeuroImage.

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

[10]  Jordi García-Ojalvo,et al.  Relating structural and functional anomalous connectivity in the aging brain via neural mass modeling , 2010, NeuroImage.

[11]  Stephen M. Smith,et al.  Multiplexed Echo Planar Imaging for Sub-Second Whole Brain FMRI and Fast Diffusion Imaging , 2010, PloS one.

[12]  Christoph M. Michel,et al.  Directed Functional Brain Connectivity Based on EEG Source Imaging: Methodology and Application to Temporal Lobe Epilepsy , 2016, IEEE Transactions on Biomedical Engineering.

[13]  Joerg F. Hipp,et al.  Measuring the cortical correlation structure of spontaneous oscillatory activity with EEG and MEG , 2016, NeuroImage.

[14]  Viktor K. Jirsa,et al.  Complementary contributions of concurrent EEG and fMRI connectivity for predicting structural connectivity , 2017, NeuroImage.

[15]  Alan Connelly,et al.  MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation , 2019, NeuroImage.

[16]  Bastian Cheng,et al.  Modeling of Large-Scale Functional Brain Networks Based on Structural Connectivity from DTI: Comparison with EEG Derived Phase Coupling Networks and Evaluation of Alternative Methods along the Modeling Path , 2016, bioRxiv.

[17]  Stamatios N. Sotiropoulos,et al.  An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging , 2016, NeuroImage.

[18]  P. Hagmann,et al.  Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[19]  Chun-Hung Yeh,et al.  MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation , 2019, NeuroImage.

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

[21]  Ben Jeurissen,et al.  Diffusion MRI fiber tractography of the brain , 2019, NMR in biomedicine.

[22]  J. Schoffelen,et al.  Source connectivity analysis with MEG and EEG , 2009, Human brain mapping.

[23]  N. Wenderoth,et al.  Detecting large‐scale networks in the human brain using high‐density electroencephalography , 2017, Human brain mapping.

[24]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[25]  Kevin Whittingstall,et al.  Effects of dipole position, orientation and noise on the accuracy of EEG source localization , 2003, Biomedical engineering online.

[26]  Farras Abdelnour,et al.  Functional brain connectivity is predictable from anatomic network's Laplacian eigen-structure , 2018, NeuroImage.

[27]  Richard N. Henson,et al.  Adaptive Cortical Parcellations for Source Reconstructed EEG/MEG Connectomes , 2017 .

[28]  Jukka Kortelainen,et al.  Experimental comparison of connectivity measures with simulated EEG signals , 2012, Medical & Biological Engineering & Computing.

[29]  C M Michel,et al.  Estimating EEG Source Dipole Orientation Based on Singular-value Decomposition for Connectivity Analysis , 2018, Brain Topography.

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

[31]  Marco Ganzetti,et al.  Detecting Large-Scale Brain Networks Using EEG: Impact of Electrode Density, Head Modeling and Source Localization , 2018, Front. Neuroinform..

[32]  J. A. Scott Kelso,et al.  Brain coordination dynamics: True and false faces of phase synchrony and metastability , 2009, Progress in Neurobiology.

[33]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[34]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[35]  Derek K. Jones Challenges and limitations of quantifying brain connectivity in vivo with diffusion MRI , 2010 .

[36]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[37]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[38]  Steen Moeller,et al.  The Human Connectome Project: A data acquisition perspective , 2012, NeuroImage.

[39]  Edwin van Dellen,et al.  Structural degree predicts functional network connectivity: A multimodal resting-state fMRI and MEG study , 2014, NeuroImage.

[40]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[41]  G. Deco,et al.  Inversion of a large-scale circuit model reveals a cortical hierarchy in the dynamic resting human brain , 2019, Science Advances.

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

[43]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[44]  Piet Van Mieghem,et al.  A Mapping Between Structural and Functional Brain Networks , 2016, Brain Connect..

[45]  Dimitri Van De Ville,et al.  BOLD correlates of EEG topography reveal rapid resting-state network dynamics , 2010, NeuroImage.

[46]  Amy L. Daitch,et al.  Electrophysiological dynamics of antagonistic brain networks reflect attentional fluctuations , 2020, Nature Communications.

[47]  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.

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

[49]  Cornelis J. Stam,et al.  Activity Dependent Degeneration Explains Hub Vulnerability in Alzheimer's Disease , 2012, PLoS Comput. Biol..

[50]  Simon K. Warfield,et al.  Cortical Graph Smoothing: A Novel Method for Exploiting DWI-Derived Anatomical Brain Connectivity to Improve EEG Source Estimation , 2013, IEEE Transactions on Medical Imaging.

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

[52]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[53]  Mathieu Bourguignon,et al.  A geometric correction scheme for spatial leakage effects in MEG/EEG seed‐based functional connectivity mapping , 2015, Human brain mapping.

[54]  Maria Giulia Preti,et al.  Decoupling of brain function from structure reveals regional behavioral specialization in humans , 2019, Nature Communications.

[55]  Benjamin A. E. Hunt,et al.  Measuring electrophysiological connectivity by power envelope correlation: a technical review on MEG methods , 2015, Physics in medicine and biology.

[56]  Mark W. Woolrich,et al.  A symmetric multivariate leakage correction for MEG connectomes , 2015, NeuroImage.

[57]  N. Wenderoth,et al.  Detecting large-scale networks in the human brain using high-density electroencephalography , 2016, bioRxiv.

[58]  J. Polimeni,et al.  Blipped‐controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g‐factor penalty , 2012, Magnetic resonance in medicine.

[59]  Damien Coyle,et al.  Alpha and theta rhythm abnormality in Alzheimer's Disease: a study using a computational model. , 2011, Advances in experimental medicine and biology.

[60]  Matthieu Gilson,et al.  Resting state networks in empirical and simulated dynamic functional connectivity , 2016, NeuroImage.

[61]  Matthew J. Brookes,et al.  How do spatially distinct frequency specific MEG networks emerge from one underlying structural connectome? The role of the structural eigenmodes , 2019, NeuroImage.

[62]  Alan Connelly,et al.  Anatomically-constrained tractography: Improved diffusion MRI streamlines tractography through effective use of anatomical information , 2012, NeuroImage.

[63]  L. Cammoun,et al.  The Connectome Mapper: An Open-Source Processing Pipeline to Map Connectomes with MRI , 2012, PloS one.

[64]  Linda Douw,et al.  Local polymorphic delta activity in cortical lesions causes global decreases in functional connectivity , 2013, NeuroImage.

[65]  Pascal Frossard,et al.  The emerging field of signal processing on graphs: Extending high-dimensional data analysis to networks and other irregular domains , 2012, IEEE Signal Processing Magazine.

[66]  Jeremy D. Schmahmann,et al.  Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers , 2008, NeuroImage.

[67]  Gijs Plomp,et al.  Directed functional connections underlying spontaneous brain activity , 2018, Human brain mapping.

[68]  N. Volkow,et al.  Energetic cost of brain functional connectivity , 2013, Proceedings of the National Academy of Sciences.

[69]  Tracy Warbrick,et al.  Spontaneous brain activity and EEG microstates. A novel EEG/fMRI analysis approach to explore resting-state networks , 2010, NeuroImage.

[70]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[71]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[72]  Selen Atasoy,et al.  Human brain networks function in connectome-specific harmonic waves , 2016, Nature Communications.

[73]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

[74]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[75]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[76]  P. Nunez,et al.  EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics , 2007, Journal of Neuroscience Methods.

[77]  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.

[78]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[79]  Michael Breakspear,et al.  Intrinsic Coupling Modes in Source-Reconstructed Electroencephalography , 2014, Brain Connect..

[80]  Andreas Daffertshofer,et al.  The relationship between structural and functional connectivity: Graph theoretical analysis of an EEG neural mass model , 2010, NeuroImage.