Multi-timescale hybrid components of the functional brain connectome: A bimodal EEG-fMRI decomposition

Concurrent electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) bridge brain connectivity across timescales. During concurrent EEG-fMRI resting-state recordings, whole-brain functional connectivity (FC) strength is spatially correlated across modalities. However, cross-modal investigations have commonly remained correlational, and joint analysis of EEG-fMRI connectivity is largely unexplored. Here we investigated if there exist (spatially) independent FC networks linked between modalities. We applied the recently proposed hybrid connectivity independent component analysis (connICA) framework to two concurrent EEG-fMRI resting state datasets (total 40 subjects). Two robust components were found across both datasets. The first component has a uniformly distributed EEG-frequency fingerprint linked mainly to intrinsic connectivity networks (ICNs) in both modalities. Conversely, the second component is sensitive to different EEG-frequencies and is primarily linked to intra-ICN connectivity in fMRI but to inter-ICN connectivity in EEG. The first hybrid component suggests that connectivity dynamics within well-known ICNs span timescales, from millisecond-range in all canonical frequencies of FCEEG to second-range of FCfMRI. Conversely, the second component additionally exposes linked but spatially divergent neuronal processing at the two timescales. This work reveals the existence of joint spatially independent components, suggesting that parts of resting-state connectivity are co-expressed in a linked manner across EEG and fMRI over individuals.

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

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

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

[4]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[5]  Joaquín Goñi,et al.  Cognitive complaints in older adults at risk for Alzheimer's disease are associated with altered resting-state networks , 2016, Alzheimer's & dementia.

[6]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

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

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

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

[10]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[11]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[12]  Gustavo Deco,et al.  Inferring multi-scale neural mechanisms with brain network modelling , 2017, bioRxiv.

[13]  Gustavo Deco,et al.  Functional connectivity dynamics: Modeling the switching behavior of the resting state , 2015, NeuroImage.

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

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

[16]  S. Debener,et al.  Mining EEG-fMRI using independent component analysis. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

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

[19]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

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

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

[22]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

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

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

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

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

[27]  J. Haxby,et al.  Dissociation of face-selective cortical responses by attention. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[29]  Christian Bénar,et al.  Single-trial EEG-informed fMRI reveals spatial dependency of BOLD signal on early and late IC-ERP amplitudes during face recognition , 2014, NeuroImage.

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

[31]  R. Tsien,et al.  Specificity and Stability in Topology of Protein Networks , 2022 .

[32]  Olaf Sporns,et al.  Network-Level Structure-Function Relationships in Human Neocortex , 2016, Cerebral cortex.

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

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

[35]  K. McGraw,et al.  Forming inferences about some intraclass correlation coefficients. , 1996 .

[36]  Patrice Y. Simard,et al.  Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. , 1994, Cerebral cortex.

[37]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[38]  Enrico Amico,et al.  Mapping hybrid functional-structural connectivity traits in the human connectome , 2017, Network Neuroscience.

[39]  M E J Newman,et al.  Fast algorithm for detecting community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[40]  D Lehmann,et al.  EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. , 1987, Electroencephalography and clinical neurophysiology.

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

[42]  P. Sajda,et al.  Simultaneous EEG-fMRI Reveals Temporal Evolution of Coupling between Supramodal Cortical Attention Networks and the Brainstem , 2013, The Journal of Neuroscience.

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

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

[45]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

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

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

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

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

[50]  Lauri Parkkonen,et al.  The brain timewise: how timing shapes and supports brain function , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  Juliane Britz,et al.  EEG microstate sequences in healthy humans at rest reveal scale-free dynamics , 2010, Proceedings of the National Academy of Sciences.

[52]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[53]  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.

[54]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[55]  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.

[56]  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.

[57]  J. Bartko The Intraclass Correlation Coefficient as a Measure of Reliability , 1966, Psychological reports.

[58]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[59]  Olaf Sporns,et al.  Weight-conserving characterization of complex functional brain networks , 2011, NeuroImage.

[60]  Dietrich Lehmann,et al.  Functional states of the brain : their determinants , 1980 .

[61]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

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

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

[64]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[65]  Enrico Amico,et al.  Multi-timescale hybrid components of the functional brain connectome: A bimodal EEG-fMRI decomposition , 2020, Network Neuroscience.

[66]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

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

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