EEG Source Connectivity Analysis: From Dense Array Recordings to Brain Networks

The recent past years have seen a noticeable increase of interest for electroencephalography (EEG) to analyze functional connectivity through brain sources reconstructed from scalp signals. Although considerable advances have been done both on the recording and analysis of EEG signals, a number of methodological questions are still open regarding the optimal way to process the data in order to identify brain networks. In this paper, we analyze the impact of three factors that intervene in this processing: i) the number of scalp electrodes, ii) the combination between the algorithm used to solve the EEG inverse problem and the algorithm used to measure the functional connectivity and iii) the frequency bands retained to estimate the functional connectivity among neocortical sources. Using High-Resolution (hr) EEG recordings in healthy volunteers, we evaluated these factors on evoked responses during picture recognition and naming task. The main reason for selection this task is that a solid literature background is available about involved brain networks (ground truth). From this a priori information, we propose a performance criterion based on the number of connections identified in the regions of interest (ROI) that belong to potentially activated networks. Our results show that the three studied factors have a dramatic impact on the final result (the identified network in the source space) as strong discrepancies were evidenced depending on the methods used. They also suggest that the combination of weighted Minimum Norm Estimator (wMNE) and the Phase Synchronization (PS) methods applied on High-Resolution EEG in beta/gamma bands provides the best performance in term of topological distance between the identified network and the expected network in the above-mentioned cognitive task.

[1]  A. Nakamura,et al.  Different neural systems for recognizing plants, animals, and artifacts , 2001, Brain Research Bulletin.

[2]  M. Rosenblum,et al.  Chapter 9 Phase synchronization: From theory to data analysis , 2001 .

[3]  Rodrigo Quian Quiroga,et al.  Nonlinear multivariate analysis of neurophysiological signals , 2005, Progress in Neurobiology.

[4]  M Erb,et al.  Activation of right fronto-temporal cortex characterizes the 'living' category in semantic processing. , 2001, Brain research. Cognitive brain research.

[5]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[6]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[7]  James J. DiCarlo,et al.  How Does the Brain Solve Visual Object Recognition? , 2012, Neuron.

[8]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[9]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Laura Astolfi,et al.  Estimation of the effective and functional human cortical connectivity with structural equation modeling and directed transfer function applied to high-resolution EEG. , 2004, Magnetic resonance imaging.

[11]  Emmanuel Mellet,et al.  Picture naming without Broca's and Wernicke's area , 2000, Neuroreport.

[12]  Anders M. Dale,et al.  Spectral spatiotemporal imaging of cortical oscillations and interactions in the human brain , 2004, NeuroImage.

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

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

[15]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  Jean Gotman,et al.  Evaluation of EEG localization methods using realistic simulations of interictal spikes , 2006, NeuroImage.

[17]  T W Picton,et al.  Comparative electrophysiological and hemodynamic measures of neural activation during memory‐retrieval , 2001, Human brain mapping.

[18]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

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

[20]  Marianna D. Eddy,et al.  Masked repetition priming and event-related brain potentials: a new approach for tracking the time-course of object perception. , 2006, Psychophysiology.

[21]  J. Bellanger,et al.  Interpretation of interdependencies in epileptic signals using a macroscopic physiological model of the EEG , 2001, Clinical Neurophysiology.

[22]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[23]  Hoi-Chung Leung,et al.  Frontal activations associated with accessing and evaluating information in working memory: an fMRI study , 2003, NeuroImage.

[24]  M. Roulston Estimating the errors on measured entropy and mutual information , 1999 .

[25]  A. Hillis,et al.  Neural regions essential for distinct cognitive processes underlying picture naming. , 2007, Brain : a journal of neurology.

[26]  F. Babiloni,et al.  Assessing cortical functional connectivity by linear inverse estimation and directed transfer function: simulations and application to real data , 2005, Clinical Neurophysiology.

[27]  J. Rodd,et al.  Processing Objects at Different Levels of Specificity , 2004, Journal of Cognitive Neuroscience.

[28]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[29]  Michael J Brammer,et al.  Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses , 2003, Human brain mapping.

[30]  R Quian Quiroga,et al.  Performance of different synchronization measures in real data: a case study on electroencephalographic signals. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  Mia Liljeström,et al.  Perceiving and naming actions and objects , 2008, NeuroImage.

[32]  G. Orban,et al.  Comparative mapping of higher visual areas in monkeys and humans , 2004, Trends in Cognitive Sciences.

[33]  Riitta Salmelin,et al.  Naming actions and objects: cortical dynamics in healthy adults and in an anomic patient with a dissociation in action/object naming , 2003, NeuroImage.

[34]  Karl J. Friston,et al.  Evaluation of different measures of functional connectivity using a neural mass model , 2004, NeuroImage.

[35]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[36]  Alex Martin,et al.  A wavelet-based method for measuring the oscillatory dynamics of resting-state functional connectivity in MEG , 2011, NeuroImage.

[37]  G. A. Miller,et al.  Comparison of different cortical connectivity estimators for high‐resolution EEG recordings , 2007, Human brain mapping.

[38]  Febo Cincotti,et al.  Multimodal integration of high-resolution EEG and functional magnetic resonance imaging data: a simulation study , 2003, NeuroImage.

[39]  Alan C. Evans,et al.  The Neural Substrate of Picture Naming , 1999, Journal of Cognitive Neuroscience.

[40]  R. Hari,et al.  Dynamics of brain activation during picture naming , 1994, Nature.

[41]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[42]  M A B BRAZIER,et al.  Cross-correlation and autocorrelation studies of electroencephalographic potentials. , 1952, Electroencephalography and clinical neurophysiology.

[43]  Peter A Tass,et al.  swLORETA: a novel approach to robust source localization and synchronization tomography , 2007, Physics in medicine and biology.

[44]  Matthew J. Brookes,et al.  Measuring functional connectivity using MEG: Methodology and comparison with fcMRI , 2011, NeuroImage.

[45]  Eric Achten,et al.  Multilingualism: an fMRI study , 2003, NeuroImage.

[46]  Fernando H. Lopes da Silva,et al.  Propagation of Electrical Activity: Nonlinear Associations and Time Delays between EEG Signals , 1993 .

[47]  Martin Klein,et al.  How do brain tumors alter functional connectivity? A magnetoencephalography study , 2006, Annals of neurology.

[48]  John C Gore,et al.  Assessing functional connectivity in the human brain by fMRI. , 2007, Magnetic resonance imaging.

[49]  F. D. Silva,et al.  Propagation of seizure activity in kindled dogs. , 1983 .

[50]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[51]  F X Alario,et al.  A set of 400 pictures standardized for French: Norms for name agreement, image agreement, familiarity, visual complexity, image variability, and age of acquisition , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[52]  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.

[53]  W. El-Deredy,et al.  Reconstructing Coherent Networks from Electroencephalography and Magnetoencephalography with Reduced Contamination from Volume Conduction or Magnetic Field Spread , 2013, PloS one.

[54]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[55]  I. Toni,et al.  Oscillations , 2018, Physics to a Degree.

[56]  Emmanuel Mandonnet,et al.  Evidence for an occipito-temporal tract underlying visual recognition in picture naming , 2009, Clinical Neurology and Neurosurgery.

[57]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  Ruth A. Carper,et al.  Autism and Abnormal Development of Brain Connectivity , 2004, The Journal of Neuroscience.

[59]  Mia Liljeström,et al.  Comparing MEG and fMRI views to naming actions and objects , 2009, NeuroImage.

[60]  Riitta Salmelin,et al.  Accessing newly learned names and meanings in the native language , 2009, Human brain mapping.

[61]  Riitta Salmelin,et al.  Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation , 2006, NeuroImage.

[62]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[63]  Katarzyna J. Blinowska,et al.  Review of the methods of determination of directed connectivity from multichannel data , 2011, Medical & Biological Engineering & Computing.

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

[65]  J. Kurths,et al.  Phase synchronization: from theory to data analysis , 2003 .

[66]  C. E. SHANNON,et al.  A mathematical theory of communication , 1948, MOCO.

[67]  Olivier David,et al.  Estimation of neural dynamics from MEG/EEG cortical current density maps: application to the reconstruction of large-scale cortical synchrony , 2002, IEEE Transactions on Biomedical Engineering.

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

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

[70]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[71]  Dominique Hasboun,et al.  A multitrial analysis for revealing significant corticocortical networks in magnetoencephalography and electroencephalography , 2003, NeuroImage.

[72]  Charles D. Smith,et al.  Differences in Functional Magnetic Resonance Imaging Activation by Category in a Visual Confrontation Naming Task , 2001, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[73]  I Law,et al.  Categorization and category effects in normal object recognition A PET Study , 2000, Neuropsychologia.

[74]  M. Brazier Studies of the EEG activity of limbic structures in man. , 1968, Electroencephalography and clinical neurophysiology.

[75]  L. Senhadji,et al.  From EEG signals to brain connectivity: A model-based evaluation of interdependence measures , 2009, Journal of Neuroscience Methods.

[76]  C. Stam,et al.  Nonlinear synchronization in EEG and whole‐head MEG recordings of healthy subjects , 2003, Human brain mapping.

[77]  Robert T. Knight,et al.  Spatiotemporal imaging of cortical activation during verb generation and picture naming , 2010, NeuroImage.

[78]  Angela R Laird,et al.  Meta‐analyses of object naming: Effect of baseline , 2005, Human brain mapping.

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

[80]  Bin He,et al.  Evaluation of cortical current density imaging methods using intracranial electrocorticograms and functional MRI , 2007, NeuroImage.

[81]  Antje S. Meyer,et al.  An MEG Study of Picture Naming , 1998, Journal of Cognitive Neuroscience.

[82]  F Cincotti,et al.  Linear inverse source estimate of combined EEG and MEG data related to voluntary movements , 2001, Human brain mapping.

[83]  Michael C. Stevens,et al.  The developmental cognitive neuroscience of functional connectivity , 2009, Brain and Cognition.

[84]  Lotfi Senhadji,et al.  Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[85]  Matthias M. Müller,et al.  Directed Cortical Information Flow during Human Object Recognition: Analyzing Induced EEG Gamma-Band Responses in Brain's Source Space , 2007, PloS one.

[86]  John W Belliveau,et al.  Monte Carlo simulation studies of EEG and MEG localization accuracy , 2002, Human brain mapping.

[87]  F. H. Lopes da Silva,et al.  Propagation of seizure activity in kindled dogs. , 1983, Electroencephalography and clinical neurophysiology.

[88]  Cheryl Garn,et al.  An fMRI study of sex differences in brain activation during object naming , 2009, Cortex.

[89]  C. Price,et al.  Three Distinct Ventral Occipitotemporal Regions for Reading and Object Naming , 1999, NeuroImage.

[90]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[91]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[92]  Karl J. Friston,et al.  The neural regions sustaining object recognition and naming , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[94]  O. Sporns Structure and function of complex brain networks , 2013, Dialogues in clinical neuroscience.

[95]  Eugenio Rodriguez,et al.  Studying Single-Trials of phase Synchronous Activity in the Brain , 2000, Int. J. Bifurc. Chaos.

[96]  Alex Martin,et al.  Modulation of neural activity during object naming: effects of time and practice. , 2003, Cerebral cortex.