Automatic and robust noise suppression in EEG and MEG: The SOUND algorithm

&NA; Electroencephalography (EEG) and magnetoencephalography (MEG) often suffer from noise‐ and artifact‐contaminated channels and trials. Conventionally, EEG and MEG data are inspected visually and cleaned accordingly, e.g., by identifying and rejecting the so‐called “bad” channels. This approach has several shortcomings: data inspection is laborious, the rejection criteria are subjective, and the process does not fully utilize all the information in the collected data. Here, we present noise‐cleaning methods based on modeling the multi‐sensor and multi‐trial data. These approaches offer objective, automatic, and robust removal of noise and disturbances by taking into account the sensor‐ or trial‐specific signal‐to‐noise ratios. We introduce a method called the source‐estimate‐utilizing noise‐discarding algorithm (the SOUND algorithm). SOUND employs anatomical information of the head to cross‐validate the data between the sensors. As a result, we are able to identify and suppress noise and artifacts in EEG and MEG. Furthermore, we discuss the theoretical background of SOUND and show that it is a special case of the well‐known Wiener estimators. We explain how a completely data‐driven Wiener estimator (DDWiener) can be used when no anatomical information is available. DDWiener is easily applicable to any linear multivariate problem; as a demonstrative example, we show how DDWiener can be utilized when estimating event‐related EEG/MEG responses. We validated the performance of SOUND with simulations and by applying SOUND to multiple EEG and MEG datasets. SOUND considerably improved the data quality, exceeding the performance of the widely used channel‐rejection and interpolation scheme. SOUND also helped in localizing the underlying neural activity by preventing noise from contaminating the source estimates. SOUND can be used to detect and reject noise in functional brain data, enabling improved identification of active brain areas. HighlightsWe present the SOUND algorithm that is based on the optimal Wiener‐filtering.SOUND automatically identifies and suppresses noise in multichannel MEG/EEG data.SOUND surpasses the common channel‐rejection and interpolation scheme.Running SOUND takes significantly less time compared to visual data inspection.The MATLAB implementation of SOUND is provided in a freely downloadable demo package.

[1]  S. Makeig,et al.  Imaging human EEG dynamics using independent component analysis , 2006, Neuroscience & Biobehavioral Reviews.

[2]  Jafar A. Khan,et al.  Robust Linear Model Selection Based on Least Angle Regression , 2007 .

[3]  Richard M. Leahy,et al.  BrainSuite: An Automated Cortical Surface Identification Tool , 2000, MICCAI.

[4]  Matti Stenroos,et al.  Recovering TMS-evoked EEG responses masked by muscle artifacts , 2016, NeuroImage.

[5]  R. Ilmoniemi,et al.  Signal-space projection method for separating MEG or EEG into components , 1997, Medical and Biological Engineering and Computing.

[6]  Cornelis J. Stam,et al.  Functional brain network analysis using minimum spanning trees in Multiple Sclerosis: An MEG source-space study , 2014, NeuroImage.

[7]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[8]  Faranak Farzan,et al.  Characterizing Long Interval Cortical Inhibition over the Time-Frequency Domain , 2014, PloS one.

[9]  K. Uutela,et al.  Detecting and Correcting for Head Movements in Neuromagnetic Measurements , 2001, NeuroImage.

[10]  B. Yvert,et al.  An evaluation of dipole reconstruction accuracy with spherical and realistic head models in MEG , 1999, Clinical Neurophysiology.

[11]  Richard M. Leahy,et al.  Generalized sidelobe canceller for magnetoencephalography arrays , 2009, 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[12]  L. Elliot Hong,et al.  Evoked gamma band synchronization and the liability for schizophrenia , 2004, Schizophrenia Research.

[13]  Andrea Pigorini,et al.  Assessing the Effects of Electroconvulsive Therapy on Cortical Excitability by Means of Transcranial Magnetic Stimulation and Electroencephalography , 2012, Brain Topography.

[14]  M. S. Mobin,et al.  Weighted averaging of evoked potentials , 1992, IEEE Transactions on Biomedical Engineering.

[15]  Petro Julkunen,et al.  Combining Transcranial Magnetic Stimulation and Electroencephalography May Contribute to Assess the Severity of Alzheimer's Disease , 2011, International journal of Alzheimer's disease.

[16]  Andreas Keil,et al.  Cortical activation during Pavlovian fear conditioning depends on heart rate response patterns: an MEG study. , 2005, Brain research. Cognitive brain research.

[17]  Matti Stenroos,et al.  Dealing with artifacts in TMS-evoked EEG , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[18]  Panagiotis D Bamidis,et al.  Amygdala responses to Valence and its interaction by arousal revealed by MEG. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  Faming Liang,et al.  Statistical and Computational Inverse Problems , 2006, Technometrics.

[20]  A. Dale,et al.  Distributed current estimates using cortical orientation constraints , 2006, Human brain mapping.

[21]  J. Sarvas,et al.  Mixed and sensory nerve stimulations activate different cytoarchitectonic areas in the human primary somatosensory cortex SI , 1986, Experimental Brain Research.

[22]  M. Bertero,et al.  Linear inverse problems with discrete data: II. Stability and regularisation , 1988 .

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

[24]  Peter Bajorski,et al.  Wiley Series in Probability and Statistics , 2010 .

[25]  Alan C. Evans,et al.  OMEGA: The Open MEG Archive , 2016, NeuroImage.

[26]  Tri-Dung Nguyen,et al.  Outlier detection and robust covariance estimation using mathematical programming , 2010, Adv. Data Anal. Classif..

[27]  Robert J Barry,et al.  Specificity of quantitative EEG analysis in adults with attention deficit hyperactivity disorder , 2002, Psychiatry Research.

[28]  Jukka Sarvas,et al.  Removal of large muscle artifacts from transcranial magnetic stimulation-evoked EEG by independent component analysis , 2011, Medical & Biological Engineering & Computing.

[29]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[30]  J. Sarvas,et al.  Bioelectromagnetic forward problem: isolated source approach revis(it)ed , 2012, Physics in medicine and biology.

[31]  P Berg,et al.  A multiple source approach to the correction of eye artifacts. , 1994, Electroencephalography and clinical neurophysiology.

[32]  Olaf Hauk,et al.  Keep it simple: a case for using classical minimum norm estimation in the analysis of EEG and MEG data , 2004, NeuroImage.

[33]  M. Foster An Application of the Wiener-Kolmogorov Smoothing Theory to Matrix Inversion , 1961 .

[34]  S. Taulu,et al.  Presentation of electromagnetic multichannel data: The signal space separation method , 2005 .

[35]  R. B. Reilly,et al.  FASTER: Fully Automated Statistical Thresholding for EEG artifact Rejection , 2010, Journal of Neuroscience Methods.

[36]  B. Ripley,et al.  Robust Statistics , 2018, Encyclopedia of Mathematical Geosciences.

[37]  Lucas C. Parra,et al.  Recipes for the linear analysis of EEG , 2005, NeuroImage.

[38]  T. Demiralp,et al.  Human EEG gamma oscillations in neuropsychiatric disorders , 2005, Clinical Neurophysiology.

[39]  P. Rousseeuw Least Median of Squares Regression , 1984 .

[40]  R N Vigário,et al.  Extraction of ocular artefacts from EEG using independent component analysis. , 1997, Electroencephalography and clinical neurophysiology.

[41]  Monson H. Hayes,et al.  Statistical Digital Signal Processing and Modeling , 1996 .

[42]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[43]  Arnaud Delorme,et al.  EEGLAB, SIFT, NFT, BCILAB, and ERICA: New Tools for Advanced EEG Processing , 2011, Comput. Intell. Neurosci..

[44]  J. Wolpaw,et al.  EMG contamination of EEG: spectral and topographical characteristics , 2003, Clinical Neurophysiology.

[45]  Vladimir Litvak,et al.  Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex , 2007, NeuroImage.

[46]  R. Hari,et al.  Stronger occipital cortical activation to lower than upper visual field stimuli Neuromagnetic recordings , 1999, Experimental Brain Research.

[47]  Alexandre Gramfort,et al.  Automated model selection in covariance estimation and spatial whitening of MEG and EEG signals , 2015, NeuroImage.

[48]  R. Ilmoniemi,et al.  Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity , 1997, Neuroreport.

[49]  Sauli Savolainen,et al.  Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation , 2002, Clinical Neurophysiology.

[50]  Alain de Cheveigné,et al.  Sensor noise suppression , 2008, Journal of Neuroscience Methods.

[51]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

[52]  Giulio Tononi,et al.  Human brain connectivity during single and paired pulse transcranial magnetic stimulation , 2011, NeuroImage.

[53]  Shiro Ikeda,et al.  Independent component analysis for noisy data -- MEG data analysis , 2000, Neural Networks.

[54]  Marcello Massimini,et al.  Consciousness and cortical responsiveness: a within-state study during non-rapid eye movement sleep , 2016, Scientific Reports.

[55]  Willy Wong,et al.  TMSEEG: A MATLAB-Based Graphical User Interface for Processing Electrophysiological Signals during Transcranial Magnetic Stimulation , 2016, Front. Neural Circuits.

[56]  Terence W Picton,et al.  Weighted averaging of steady-state responses , 2001, Clinical Neurophysiology.

[57]  Thomas Hinze,et al.  Biochemical Frequency Control by Synchronisation of Coupled Repressilators: An In Silico Study of Modules for Circadian Clock Systems , 2011, Comput. Intell. Neurosci..

[58]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[59]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

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

[61]  Anthony T. Herdman,et al.  Application of multi-source minimum variance beamformers for reconstruction of correlated neural activity , 2009, NeuroImage.

[62]  Risto J. Ilmoniemi,et al.  Projecting out muscle artifacts from TMS-evoked EEG , 2011, NeuroImage.

[63]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[64]  Alexandre Gramfort,et al.  Autoreject: Automated artifact rejection for MEG and EEG data , 2016, NeuroImage.

[65]  N. Campbell Robust Procedures in Multivariate Analysis I: Robust Covariance Estimation , 1980 .

[66]  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.

[67]  R. Ilmoniemi,et al.  EEG minimum-norm estimation compared with MEG dipole fitting in the localization of somatosensory sources at S1 , 2004, Clinical Neurophysiology.

[68]  Kyungmin Su,et al.  The PREP pipeline: standardized preprocessing for large-scale EEG analysis , 2015, Front. Neuroinform..

[69]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[70]  Risto J. Ilmoniemi,et al.  Methodology for Combined TMS and EEG , 2009, Brain Topography.

[71]  C. Stam,et al.  Cognition in MS correlates with resting-state oscillatory brain activity: An explorative MEG source-space study☆ , 2013, NeuroImage: Clinical.

[72]  A Bezerianos,et al.  Data dependent weighted averages for recording of evoked potential signals. , 1995, Electroencephalography and clinical neurophysiology.

[73]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[74]  O. Hauk,et al.  Neurophysiological distinction of action words in the fronto‐central cortex , 2004, Human brain mapping.

[75]  J. Nenonen,et al.  Transformation of multichannel magnetocardiographic signals to standard grid form , 1995, IEEE Transactions on Biomedical Engineering.

[76]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[77]  Olivier Ledoit,et al.  A well-conditioned estimator for large-dimensional covariance matrices , 2004 .

[78]  D. Tucker,et al.  Scalp electrode impedance, infection risk, and EEG data quality , 2001, Clinical Neurophysiology.

[79]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.