What can be found in scalp EEG spectrum beyond common frequency bands. EEG–fMRI study

OBJECTIVE The scalp EEG spectrum is a frequently used marker of neural activity. Commonly, the preprocessing of EEG utilizes constraints, e.g. dealing with a predefined subset of electrodes or a predefined frequency band of interest. Such treatment of the EEG spectrum neglects the fact that particular neural processes may be reflected in several frequency bands and/or several electrodes concurrently, and can overlook the complexity of the structure of the EEG spectrum. APPROACH We showed that the EEG spectrum structure can be described by parallel factor analysis (PARAFAC), a method which blindly uncovers the spatial-temporal-spectral patterns of EEG. We used an algorithm based on variational Bayesian statistics to reveal nine patterns from the EEG of 38 healthy subjects, acquired during a semantic decision task. The patterns reflected neural activity synchronized across theta, alpha, beta and gamma bands and spread over many electrodes, as well as various EEG artifacts. MAIN RESULTS Specifically, one of the patterns showed significant correlation with the stimuli timing. The correlation was higher when compared to commonly used models of neural activity (power fluctuations in distinct frequency band averaged across a subset of electrodes) and we found significantly correlated hemodynamic fluctuations in simultaneously acquired fMRI data in regions known to be involved in speech processing. Further, we show that the pattern also occurs in EEG data which were acquired outside the MR machine. Two other patterns reflected brain rhythms linked to the attentional and basal ganglia large scale networks. The other patterns were related to various EEG artifacts. SIGNIFICANCE These results show that PARAFAC blindly identifies neural activity in the EEG spectrum and that it naturally handles the correlations among frequency bands and electrodes. We conclude that PARAFAC seems to be a powerful tool for analysis of the EEG spectrum and might bring novel insight to the relationships between EEG activity and brain hemodynamics.

[1]  Fumikazu Miwakeichi,et al.  Decomposing EEG data into space–time–frequency components using Parallel Factor Analysis , 2004, NeuroImage.

[2]  Wenxian Yu,et al.  Variational Bayesian PARAFAC decomposition for Multidimensional Harmonic Retrieval , 2011, Proceedings of 2011 IEEE CIE International Conference on Radar.

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

[4]  R. Bro PARAFAC. Tutorial and applications , 1997 .

[5]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[6]  Jean Gotman,et al.  Effects of fluctuating physiological rhythms during prolonged EEG-fMRI studies , 2008, Clinical Neurophysiology.

[7]  John S Ebersole,et al.  Advances in Spike Localization with EEG Dipole Modeling , 2009, Clinical EEG and neuroscience.

[8]  Elizabeth B. Liddle,et al.  Motion-related artefacts in EEG predict neuronally plausible patterns of activation in fMRI data , 2012, NeuroImage.

[9]  Rex E. Jung,et al.  A Baseline for the Multivariate Comparison of Resting-State Networks , 2011, Front. Syst. Neurosci..

[10]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.

[11]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Mircea Ariel Schoenfeld,et al.  Magneto- and electroencephalographic manifestations of reward anticipation and delivery , 2012, NeuroImage.

[13]  Thomas E. Nichols,et al.  Nonstationary cluster-size inference with random field and permutation methods , 2004, NeuroImage.

[14]  G Pfurtscheller,et al.  Computational model of thalamo-cortical networks: dynamical control of alpha rhythms in relation to focal attention. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[16]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

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

[18]  Helmut Laufs,et al.  Endogenous brain oscillations and related networks detected by surface EEG‐combined fMRI , 2008, Human brain mapping.

[19]  Wei Zhang,et al.  Concurrent TMS to the primary motor cortex augments slow motor learning , 2014, NeuroImage.

[20]  Wei Chu,et al.  Probabilistic Models for Incomplete Multi-dimensional Arrays , 2009, AISTATS.

[21]  R. Bro,et al.  A new efficient method for determining the number of components in PARAFAC models , 2003 .

[22]  N. Logothetis,et al.  Neurophysiology of the BOLD fMRI Signal in Awake Monkeys , 2008, Current Biology.

[23]  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.

[24]  Eduardo Martínez-Montes,et al.  Identifying Complex Brain Networks Using Penalized Regression Methods , 2008, Journal of biological physics.

[25]  Rasmus Bro,et al.  Improving the speed of multi-way algorithms:: Part I. Tucker3 , 1998 .

[26]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[27]  Fumikazu Miwakeichi,et al.  Concurrent EEG/fMRI analysis by multiway Partial Least Squares , 2004, NeuroImage.

[28]  N. Logothetis,et al.  The Amplitude and Timing of the BOLD Signal Reflects the Relationship between Local Field Potential Power at Different Frequencies , 2012, The Journal of Neuroscience.

[29]  Karl J. Friston,et al.  Variational Bayesian inference for fMRI time series , 2003, NeuroImage.

[30]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[31]  Zenglin Xu,et al.  Bayesian Nonparametric Models for Multiway Data Analysis , 2015, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[32]  Brian H. Bland,et al.  Basal ganglia–hippocampal interactions support the role of the hippocampal formation in sensorimotor integration , 2004, Experimental Neurology.

[33]  Manuel Rodriguez,et al.  Mu rhythm, visual processing and motor control , 2012, Clinical Neurophysiology.

[34]  Mark W. Woolrich,et al.  Variational Bayesian Inference for a Nonlinear Forward Model , 2020, IEEE Transactions on Signal Processing.

[35]  M. Barth,et al.  Electrophysiological Correlation Patterns of Resting State Networks in Single Subjects: A Combined EEG–fMRI Study , 2012, Brain Topography.

[36]  Tamara G. Kolda,et al.  Scalable Tensor Factorizations for Incomplete Data , 2010, ArXiv.

[37]  Evelyn C. Ferstl,et al.  The extended language network: A meta‐analysis of neuroimaging studies on text comprehension , 2008, Human brain mapping.

[38]  William D. Penny,et al.  Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI , 2010, NeuroImage.

[39]  Fernando Henrique Lopes da Silva,et al.  Interactions between different EEG frequency bands and their effect on alpha–fMRI correlations , 2009, NeuroImage.