The relationship between EEG and fMRI connectomes is reproducible across simultaneous EEG-fMRI studies from 1.5T to 7T

Both electroencephalography (EEG) and functional Magnetic Resonance Imaging (fMRI) are non-invasive methods that show complementary aspects of human brain activity. Despite their differences in probing brain activity, both electrophysiology and BOLD signal can map the underlying functional connectivity structure at the whole brain scale at different timescales. Previous work demonstrated a moderate but significant correlation between resting-state functional connectivity of both modalities, however there is a wide range of technical setups to measure simultaneous EEG-fMRI and the reliability of those measures between different setups remains unknown. This is true notably with respect to different magnetic field strengths (low and high field) and different spatial sampling of EEG (medium to high-density electrode coverage). Here, we investigated the reliability of the bimodal EEG-fMRI functional connectome in the most comprehensive resting-state simultaneous EEG-fMRI dataset compiled to date including a total of 72 subjects from four different imaging centers. Data was acquired from 1.5T, 3T and 7T scanners with simultaneously recorded EEG using 64 or 256 electrodes. We demonstrate that the whole-brain monomodal connectivity reliably correlates across different datasets and that the crossmodal correlation between EEG and fMRI connectivity of r{approx}0.3 can be reliably extracted in low and high-field scanners. The crossmodal correlation was strongest in the EEG-{beta} frequency band but exists across all frequency bands. Both homotopic and withing intrinsic connectivity network (ICN) connections contributed the most to the crossmodal relationship. This study confirms, using a considerably diverse range of recording setups, that simultaneous EEG-fMRI offers a consistent estimate of multimodal functional connectomes in healthy subjects being organized into reliable ICNs across different timescales. This opens new avenues for estimating the dynamics of brain function and provides a better understanding of interactions between EEG and fMRI measures. Alterations of this coupling could be explored as a potential clinical marker of pathological brain function.

[1]  Markus Siegel,et al.  Dissociated neuronal phase- and amplitude-coupling patterns in the human brain , 2020, NeuroImage.

[2]  Guang-Zhong Yang,et al.  Comparison of Brain Networks Based on Predictive Models of Connectivity , 2018, 2019 IEEE 19th International Conference on Bioinformatics and Bioengineering (BIBE).

[3]  Olivier D. Faugeras,et al.  A common formalism for the Integral formulations of the forward EEG problem , 2005, IEEE Transactions on Medical Imaging.

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

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

[6]  Christoph M. Michel,et al.  Investigating the variability of cardiac pulse artifacts across heartbeats in simultaneous EEG-fMRI recordings: A 7T study , 2019, NeuroImage.

[7]  Stefan Haufe,et al.  Consistency of EEG source localization and connectivity estimates , 2016, NeuroImage.

[8]  Alberto Leal,et al.  Characterisation and Reduction of the EEG Artefact Caused by the Helium Cooling Pump in the MR Environment: Validation in Epilepsy Patient Data , 2014, Brain Topography.

[9]  Brian B. Avants,et al.  An Open Source Multivariate Framework for n-Tissue Segmentation with Evaluation on Public Data , 2011, Neuroinformatics.

[10]  Joaquín Goñi,et al.  Mapping the functional connectome traits of levels of consciousness , 2016, NeuroImage.

[11]  Rami K. Niazy,et al.  Removal of FMRI environment artifacts from EEG data using optimal basis sets , 2005, NeuroImage.

[12]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[13]  Jonas Richiardi,et al.  Graph analysis of functional brain networks: practical issues in translational neuroscience , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  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.

[15]  R. Gruetter,et al.  Mapping and characterization of positive and negative BOLD responses to visual stimulation in multiple brain regions at 7T , 2018, Human brain mapping.

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

[17]  C. Clark,et al.  NODDI and Tensor-Based Microstructural Indices as Predictors of Functional Connectivity , 2016, PloS one.

[18]  João Jorge,et al.  Towards high-quality simultaneous EEG-fMRI at 7T: Detection and reduction of EEG artifacts due to head motion , 2015, NeuroImage.

[19]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[20]  Joaquín Goñi,et al.  The quest for identifiability in human functional connectomes , 2017, Scientific Reports.

[21]  Dariusz M Plewczynski,et al.  Three-dimensional Epigenome Statistical Model: Genome-wide Chromatin Looping Prediction , 2018, Scientific Reports.

[22]  Rodolfo Abreu,et al.  Pushing the Limits of EEG: Estimation of Large-Scale Functional Brain Networks and Their Dynamics Validated by Simultaneous fMRI , 2020, Frontiers in Neuroscience.

[23]  B T Thomas Yeo,et al.  Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[25]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[26]  Christoph M. Michel,et al.  Epileptic source localization with high density EEG: how many electrodes are needed? , 2003, Clinical Neurophysiology.

[27]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

[28]  Stephen D. Mayhew,et al.  Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans , 2018, Human brain mapping.

[29]  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.

[30]  A. Kleinschmidt,et al.  Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[31]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[32]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[33]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Corbetta,et al.  A Cortical Core for Dynamic Integration of Functional Networks in the Resting Human Brain , 2012, Neuron.

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

[36]  Stefan Everling,et al.  Stable long-range interhemispheric coordination is supported by direct anatomical projections , 2015, Proceedings of the National Academy of Sciences.

[37]  J. C. de Munck,et al.  Artifact removal in co-registered EEG/fMRI by selective average subtraction , 2007, Clinical Neurophysiology.

[38]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[39]  Patric Hagmann,et al.  Using structural connectivity to augment community structure in EEG functional connectivity , 2019, bioRxiv.

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

[41]  V. Calhoun,et al.  Resting state connectivity differences in eyes open versus eyes closed conditions , 2019, Human brain mapping.

[42]  René Scheeringa,et al.  Adapted cabling of an EEG cap improves simultaneous measurement of EEG and fMRI at 7T , 2019, Journal of Neuroscience Methods.

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

[44]  Enrico Amico,et al.  Multi-timescale hybrid components of the functional brain connectome: A bimodal EEG-fMRI decomposition , 2019, bioRxiv.

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

[46]  Bradley C. Love,et al.  Variability in the analysis of a single neuroimaging dataset by many teams , 2020, Nature.

[47]  Rodolfo Abreu,et al.  EEG-Informed fMRI: A Review of Data Analysis Methods , 2018, Front. Hum. Neurosci..

[48]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Mingzhou Ding,et al.  Coupling between visual alpha oscillations and default mode activity , 2013, NeuroImage.

[50]  Dustin Scheinost,et al.  A decade of test-retest reliability of functional connectivity: A systematic review and meta-analysis , 2019, NeuroImage.

[51]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[52]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

[53]  S. Debener,et al.  Effects of simultaneous EEG recording on MRI data quality at 1.5, 3 and 7 tesla. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[54]  Richard Bowtell,et al.  Exploring the feasibility of simultaneous electroencephalography/functional magnetic resonance imaging at 7 T. , 2008, Magnetic resonance imaging.

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

[56]  Piet Van Mieghem,et al.  Predicting haemodynamic networks using electrophysiology: The role of non-linear and cross-frequency interactions , 2016, NeuroImage.

[57]  Sepideh Sadaghiani,et al.  Intrinsic connectome organization across temporal scales: New insights from cross-modal approaches , 2020, Network Neuroscience.

[58]  Sepideh Sadaghiani,et al.  Phase- and amplitude-coupling are tied by an intrinsic spatial organization but show divergent stimulus-related changes , 2020, NeuroImage.

[59]  Joerg F. Hipp,et al.  BOLD fMRI Correlation Reflects Frequency-Specific Neuronal Correlation , 2015, Current Biology.

[60]  Mathieu Bourguignon,et al.  Comparing MEG and high-density EEG for intrinsic functional connectivity mapping , 2020, NeuroImage.

[61]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[62]  René Scheeringa,et al.  The relationship between oscillatory EEG activity and the laminar-specific BOLD signal , 2016, Proceedings of the National Academy of Sciences.

[63]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[64]  Théodore Papadopoulo,et al.  OpenMEEG: opensource software for quasistatic bioelectromagnetics , 2010, Biomedical engineering online.

[65]  S. Debener,et al.  Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[67]  Arno Villringer,et al.  Internal ventilation system of MR scanners induces specific EEG artifact during simultaneous EEG-fMRI , 2013, NeuroImage.

[68]  AmanPreet Badhwar,et al.  Multivariate consistency of resting-state fMRI connectivity maps acquired on a single individual over 2.5 years, 13 sites and 3 vendors , 2018, NeuroImage.

[69]  M. Corbetta,et al.  Temporal dynamics of spontaneous MEG activity in brain networks , 2010, Proceedings of the National Academy of Sciences.

[70]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[71]  Adeel Razi,et al.  Bayesian fusion and multimodal DCM for EEG and fMRI , 2019, NeuroImage.

[72]  Nadim Joni Shah,et al.  EEG acquisition in ultra-high static magnetic fields up to 9.4T , 2013, NeuroImage.

[73]  F. Deligianni,et al.  Relating resting-state fMRI and EEG whole-brain connectomes across frequency bands , 2014, Front. Neurosci..

[74]  H. Laufs,et al.  Decoding Wakefulness Levels from Typical fMRI Resting-State Data Reveals Reliable Drifts between Wakefulness and Sleep , 2014, Neuron.

[75]  Daniel Brandeis,et al.  Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth , 2006, NeuroImage.

[76]  Christoph M. Michel,et al.  Simultaneous EEG–fMRI at ultra-high field: Artifact prevention and safety assessment , 2015, NeuroImage.

[77]  Rodolfo Abreu,et al.  Ballistocardiogram artifact correction taking into account physiological signal preservation in simultaneous EEG-fMRI , 2016, NeuroImage.

[78]  Sepideh Sadaghiani,et al.  Concurrent EEG- and fMRI-derived functional connectomes exhibit linked dynamics , 2018, NeuroImage.

[79]  Robert Oostenveld,et al.  EEG-BIDS, an extension to the brain imaging data structure for electroencephalography , 2019, Scientific Data.

[80]  Claus Svarer,et al.  Safety and EEG data quality of concurrent high-density EEG and high-speed fMRI at 3 Tesla , 2017, PloS one.

[81]  Matthew J. Brookes,et al.  Ghost interactions in MEG/EEG source space: A note of caution on inter-areal coupling measures , 2017, NeuroImage.

[82]  C. Waelbroeck,et al.  Consistently dated Atlantic sediment cores over the last 40 thousand years , 2019, Scientific Data.

[83]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[84]  Luca Turella,et al.  Variability in the analysis of a single neuroimaging dataset by many teams , 2019, Nature.

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

[86]  Graeme D. Jackson,et al.  Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings , 2007, NeuroImage.

[87]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[88]  Laura Astolfi,et al.  Electrophysiological Brain Connectivity: Theory and Implementation , 2019, IEEE Transactions on Biomedical Engineering.

[89]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[90]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[91]  Leonardo L. Gollo,et al.  Time-resolved resting-state brain networks , 2014, Proceedings of the National Academy of Sciences.

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

[93]  Joshua Carp,et al.  On the Plurality of (Methodological) Worlds: Estimating the Analytic Flexibility of fMRI Experiments , 2012, Front. Neurosci..

[94]  Christoph M. Michel,et al.  Pulse Artifact Detection in Simultaneous EEG–fMRI Recording Based on EEG Map Topography , 2014, Brain Topography.

[95]  Mark W. Woolrich,et al.  How reliable are MEG resting-state connectivity metrics? , 2016, NeuroImage.

[96]  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.

[97]  Richard S. J. Frackowiak,et al.  Neurophysiological origin of human brain asymmetry for speech and language , 2010, Proceedings of the National Academy of Sciences.

[98]  Pascal Fries,et al.  Cortical layers, rhythms and BOLD signals , 2017, NeuroImage.

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

[100]  Justus Marquetand,et al.  Reliability of Magnetoencephalography and High-Density Electroencephalography Resting-State Functional Connectivity Metrics , 2019, Brain Connect..

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

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