Critical Comments on EEG Sensor Space Dynamical Connectivity Analysis

Many different analysis techniques have been developed and applied to EEG recordings that allow one to investigate how different brain areas interact. One particular class of methods, based on the linear parametric representation of multiple interacting time series, is widely used to study causal connectivity in the brain. However, the results obtained by these methods should be interpreted with great care. The goal of this paper is to show, both theoretically and using simulations, that results obtained by applying causal connectivity measures on the sensor (scalp) time series do not allow interpretation in terms of interacting brain sources. This is because (1) the channel locations cannot be seen as an approximation of a source’s anatomical location and (2) spurious connectivity can occur between sensors. Although many measures of causal connectivity derived from EEG sensor time series are affected by the latter, here we will focus on the well-known time domain index of Granger causality (GC) and on the frequency domain directed transfer function (DTF). Using the state-space framework and designing two simulation studies we show that mixing effects caused by volume conduction can lead to spurious connections, detected either by time domain GC or by DTF. Therefore, GC/DTF causal connectivity measures should be computed at the source level, or derived within analysis frameworks that model the effects of volume conduction. Since mixing effects can also occur in the source space, it is advised to combine source space analysis with connectivity measures that are robust to mixing.

[1]  J. Knoester,et al.  Scaling and universality in the optics of disordered exciton chains. , 2008, Physical review letters.

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

[3]  Qiang Xu,et al.  Small-world directed networks in the human brain: Multivariate Granger causality analysis of resting-state fMRI , 2011, NeuroImage.

[4]  Luca Faes,et al.  Assessing Connectivity in the Presence of Instantaneous Causality , 2014 .

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

[6]  Conrado A. Bosman,et al.  How to detect the Granger-causal flow direction in the presence of additive noise? , 2015, NeuroImage.

[7]  Giulio Tononi,et al.  State-Space Multivariate Autoregressive Models for Estimation of Cortical Connectivity from EEG , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[8]  Minfen Shen,et al.  Independent component analysis of electroencephalographic signals , 2002, 6th International Conference on Signal Processing, 2002..

[9]  A. Seth,et al.  Granger causality for state-space models. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[10]  Stefan Haufe,et al.  A Simulation Framework for Benchmarking EEG-Based Brain Connectivity Estimation Methodologies , 2016, Brain Topography.

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

[12]  Stefan Haufe,et al.  Validity of Time Reversal for Testing Granger Causality , 2015, IEEE Transactions on Signal Processing.

[13]  Roberto D. Pascual-Marqui,et al.  Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization , 2007, 0710.3341.

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

[15]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[16]  Karl J. Friston,et al.  Estimating Directed Connectivity from Cortical Recordings and Reconstructed Sources , 2015, Brain Topography.

[17]  Tohru Ozaki,et al.  A solution to the dynamical inverse problem of EEG generation using spatiotemporal Kalman filtering , 2004, NeuroImage.

[18]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[19]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[20]  Karl J. Friston,et al.  Analysing connectivity with Granger causality and dynamic causal modelling , 2013, Current Opinion in Neurobiology.

[21]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[22]  Clemens Brunner,et al.  Volume Conduction Influences Scalp-Based Connectivity Estimates , 2016, Front. Comput. Neurosci..

[23]  Luca Faes,et al.  Measuring Connectivity in Linear Multivariate Processes: Definitions, Interpretation, and Practical Analysis , 2012, Comput. Math. Methods Medicine.

[24]  Helmut Ltkepohl,et al.  New Introduction to Multiple Time Series Analysis , 2007 .

[25]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[26]  K. Müller,et al.  Robustly estimating the flow direction of information in complex physical systems. , 2007, Physical review letters.

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

[28]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[29]  K. Linkenkaer-Hansen,et al.  Consistency of EEG source localization and connectivity estimates , 2016, bioRxiv.

[30]  S. J. Grzybowski,et al.  Cortical functional connectivity is associated with the valence of affective states , 2014, Brain and Cognition.

[31]  Giulio Tononi,et al.  Estimation of Cortical Connectivity From EEG Using State-Space Models , 2010, IEEE Transactions on Biomedical Engineering.

[32]  Sue F. Phelps Evaluation of Information , 2018 .

[33]  Motoaki Kawanabe,et al.  Modeling Sparse Connectivity Between Underlying Brain Sources for EEG/MEG , 2009, IEEE Transactions on Biomedical Engineering.

[34]  Katarzyna J. Blinowska,et al.  Directed Transfer Function is not influenced by volume conduction—inexpedient pre-processing should be avoided , 2014, Front. Comput. Neurosci..

[35]  Tohru Ozaki,et al.  Recursive penalized least squares solution for dynamical inverse problems of EEG generation , 2004, Human brain mapping.

[36]  E. Vaucher,et al.  Activation of the mouse primary visual cortex by medial prefrontal subregion stimulation is not mediated by cholinergic basalo-cortical projections , 2015, Front. Syst. Neurosci..

[37]  Stefan Haufe,et al.  A critical assessment of connectivity measures for EEG data: A simulation study , 2013, NeuroImage.

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

[39]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[40]  Michael Eichler,et al.  On the Evaluation of Information Flow in Multivariate Systems by the Directed Transfer Function , 2006, Biological Cybernetics.

[41]  Maciej Kamiński,et al.  Interactions Between the Prefrontal Cortex and Attentional Systems During Volitional Affective Regulation: An Effective Connectivity Reappraisal Study , 2015, Brain Topography.

[42]  S. Bressler,et al.  Granger Causality: Basic Theory and Application to Neuroscience , 2006, q-bio/0608035.

[43]  Seungjin Choi,et al.  Independent Component Analysis , 2009, Handbook of Natural Computing.

[44]  Timoteo Carletti,et al.  The Stochastic Evolution of a Protocell: The Gillespie Algorithm in a Dynamically Varying Volume , 2011, Comput. Math. Methods Medicine.

[45]  S. J. Grzybowski,et al.  Effective connectivity during visual processing is affected by emotional state , 2014, Brain Imaging and Behavior.

[46]  Luca Faes,et al.  Wiener–Granger Causality in Network Physiology With Applications to Cardiovascular Control and Neuroscience , 2016, Proceedings of the IEEE.

[47]  Thomas R. Knösche,et al.  Influence of the head model on EEG and MEG source connectivity analyses , 2015, NeuroImage.

[48]  A. Seth,et al.  Granger Causality Analysis in Neuroscience and Neuroimaging , 2015, The Journal of Neuroscience.

[49]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[50]  Yu Huang,et al.  A highly detailed FEM volume conductor model based on the ICBM152 average head template for EEG source imaging and TCS targeting. , 2015, Conference proceedings : ... Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference.

[51]  Karen O. Egiazarian,et al.  Measuring directional coupling between EEG sources , 2008, NeuroImage.

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

[53]  Mingzhou Ding,et al.  Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance , 2001, Biological Cybernetics.

[54]  Karl J. Friston,et al.  Granger causality revisited , 2014, NeuroImage.

[55]  M. Eichler Causal inference in time series analysis , 2012 .

[56]  Jan-Mathijs Schoffelen,et al.  A Tutorial Review of Functional Connectivity Analysis Methods and Their Interpretational Pitfalls , 2016, Front. Syst. Neurosci..