Electromyogram (EMG) Removal by Adding Sources of EMG (ERASE)—A Novel ICA-Based Algorithm for Removing Myoelectric Artifacts From EEG

Electroencephalographic (EEG) recordings are often contaminated by electromyographic (EMG) artifacts, especially when recording during movement. Existing methods to remove EMG artifacts include independent component analysis (ICA), and other high-order statistical methods. However, these methods can not effectively remove most of EMG artifacts. Here, we proposed a modified ICA model for EMG artifacts removal in the EEG, which is called EMG Removal by Adding Sources of EMG (ERASE). In this new approach, additional channels of real EMG from neck and head muscles (reference artifacts) were added as inputs to ICA in order to “force” the most power from EMG artifacts into a few independent components (ICs). The ICs containing EMG artifacts (the “artifact ICs”) were identified and rejected using an automated procedure. ERASE was validated first using both simulated and experimentally-recorded EEG and EMG. Simulation results showed ERASE removed EMG artifacts from EEG significantly more effectively than conventional ICA. Also, it had a low false positive rate and high sensitivity. Subsequently, EEG was collected from 8 healthy participants while they moved their hands to test the realistic efficacy of this approach. Results showed that ERASE successfully removed EMG artifacts (on average, about 75% of EMG artifacts were removed when using real EMGs as reference artifacts) while preserving the expected EEG features related to movement. We also tested the ERASE procedure using simulated EMGs as reference artifacts (about 63% of EMG artifacts removed). Compared to conventional ICA, ERASE removed on average 26% more EMG artifacts from EEG. These findings suggest that ERASE can achieve significant separation of EEG signal and EMG artifacts without a loss of the underlying EEG features. These results indicate that using additional real or simulated EMG sources can increase the effectiveness of ICA in removing EMG artifacts from EEG. Combined with automated artifact IC rejection, ERASE also minimizes potential user bias. Future work will focus on improving ERASE so that it can also be used in real-time applications.

[1]  Rabab Kreidieh Ward,et al.  A Preliminary Study of Muscular Artifact Cancellation in Single-Channel EEG , 2014, Sensors.

[2]  Francisco J. Pelayo,et al.  Trends in EEG-BCI for daily-life: Requirements for artifact removal , 2017, Biomed. Signal Process. Control..

[3]  U. Rajendra Acharya,et al.  EEG Signal Analysis: A Survey , 2010, Journal of Medical Systems.

[4]  Y. Tran,et al.  Using independent component analysis to remove artifact from electroencephalographic measured during stuttered speech , 2004, Medical and Biological Engineering and Computing.

[5]  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.

[6]  Pierre Comon Independent component analysis - a new concept? signal processing , 1994 .

[7]  S. Romero,et al.  Ocular Reduction in EEG Signals Based on Adaptive Filtering, Regression and Blind Source Separation , 2008, Annals of Biomedical Engineering.

[8]  An H. Do,et al.  Hemicraniectomy in Traumatic Brain Injury: A Noninvasive Platform to Investigate High Gamma Activity for Brain Machine Interfaces , 2019, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[9]  Andreas Schulze-Bonhage,et al.  Decoding natural grasp types from human ECoG , 2012, NeuroImage.

[10]  Q. Yang,et al.  Linear correlation between fractal dimension of EEG signal and handgrip force , 2005, Biological Cybernetics.

[11]  Rami K. Niazy,et al.  Automatic correction of eye blink artifact in single channel EEG recording using EMD and OMP , 2013, 21st European Signal Processing Conference (EUSIPCO 2013).

[12]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[13]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[14]  An H. Do,et al.  Refinement of High-Gamma EEG Features From TBI Patients With Hemicraniectomy Using an ICA Informed by Simulated Myoelectric Artifacts , 2020, Frontiers in Neuroscience.

[15]  Xun Chen,et al.  Removal of Muscle Artifacts from Single-Channel EEG Based on Ensemble Empirical Mode Decomposition and Multiset Canonical Correlation Analysis , 2014, J. Appl. Math..

[16]  M. Huzmezan,et al.  A wavelet based de-noising technique for ocular artifact correction of the electroencephalogram , 2002, Proceedings of the Second Joint 24th Annual Conference and the Annual Fall Meeting of the Biomedical Engineering Society] [Engineering in Medicine and Biology.

[17]  Björn Eskofier,et al.  ICA-based reduction of electromyogenic artifacts in EEG data: Comparison with and without EMG data , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[18]  K. Jellinger,et al.  Practical Guide for Clinical Neurophysiologic Testing: EEG , 2009 .

[19]  L. Miller,et al.  Accurate decoding of reaching movements from field potentials in the absence of spikes , 2012, Journal of neural engineering.

[20]  Christopher J. James,et al.  On Semi-Blind Source Separation Using Spatial Constraints With Applications in EEG Analysis , 2006, IEEE Transactions on Biomedical Engineering.

[21]  S. Edward Rajan,et al.  A novel approach for the elimination of artefacts from EEG signals employing an improved Artificial Immune System algorithm , 2016, J. Exp. Theor. Artif. Intell..

[22]  Robert T. Knight,et al.  Hemicraniectomy: A New Model for Human Electrophysiology with High Spatio-temporal Resolution , 2010, Journal of Cognitive Neuroscience.

[23]  Domenico Prattichizzo,et al.  Off-line removal of TMS-induced artifacts on human electroencephalography by Kalman filter , 2007, Journal of Neuroscience Methods.

[24]  Christopher J. James,et al.  Employing spatially constrained ICA and wavelet denoising, for automatic removal of artifacts from multichannel EEG data , 2012, Signal Process..

[25]  Karl Pearson,et al.  On the Distribution of the Correlation Coefficient in Small Samples. Appendix II to the Papers of "Student" and R. A. Fisher , 1917 .

[26]  Norden E. Huang,et al.  Ensemble Empirical Mode Decomposition: a Noise-Assisted Data Analysis Method , 2009, Adv. Data Sci. Adapt. Anal..

[27]  P Berg,et al.  Dipole modelling of eye activity and its application to the removal of eye artefacts from the EEG and MEG. , 1991, Clinical physics and physiological measurement : an official journal of the Hospital Physicists' Association, Deutsche Gesellschaft fur Medizinische Physik and the European Federation of Organisations for Medical Physics.

[28]  Akaysha Tang,et al.  Applications of Second Order Blind Identification to High-Density EEG-Based Brain Imaging: A Review , 2010, ISNN.

[29]  Xueyuan Xu,et al.  The Use of Multivariate EMD and CCA for Denoising Muscle Artifacts From Few-Channel EEG Recordings , 2018, IEEE Transactions on Instrumentation and Measurement.

[30]  Lotfi Senhadji,et al.  ICA-based EEG denoising: a comparative analysis of fifteen methods , 2012 .

[31]  Zoran Nenadic,et al.  Extracting kinetic information from human motor cortical signals , 2014, NeuroImage.

[32]  Peter Gruber,et al.  Automatic removal of high-amplitude artefacts from single-channel electroencephalograms , 2006, Comput. Methods Programs Biomed..

[33]  V. Krishnaveni,et al.  Removal of ocular artifacts from EEG using adaptive thresholding of wavelet coefficients , 2006, Journal of neural engineering.

[34]  Jiang Li,et al.  EOG artifact removal using a wavelet neural network , 2012, Neurocomputing.

[35]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[36]  R. Oostenveld,et al.  Independent EEG Sources Are Dipolar , 2012, PloS one.

[37]  L. Euginia,et al.  A wavelet based de-noising technique for ocular artifact correction of the electroencephalogram , 2004, Proceedings. The 8th Russian-Korean International Symposium on Science and Technology, 2004. KORUS 2004..

[38]  Rabab K. Ward,et al.  Removing Muscle Artifacts From EEG Data: Multichannel or Single-Channel Techniques? , 2016, IEEE Sensors Journal.

[39]  Christian Sander,et al.  ICA-based muscle artefact correction of EEG data: What is muscle and what is brain? Comment on McMenamin et al. , 2011, NeuroImage.

[40]  Miguel Angel Mañanas,et al.  A comparative study of automatic techniques for ocular artifact reduction in spontaneous EEG signals based on clinical target variables: A simulation case , 2008, Comput. Biol. Medicine.

[41]  Juan R. Vidal,et al.  Spanning the rich spectrum of the human brain: slow waves to gamma and beyond , 2011, Brain Structure and Function.

[42]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[43]  Raveendran Paramesran,et al.  Artifacts-matched blind source separation and wavelet transform for multichannel EEG denoising , 2015, Biomed. Signal Process. Control..

[44]  Michael Unser,et al.  A review of wavelets in biomedical applications , 1996, Proc. IEEE.

[45]  Seán F. McLoone,et al.  The Use of Ensemble Empirical Mode Decomposition With Canonical Correlation Analysis as a Novel Artifact Removal Technique , 2013, IEEE Transactions on Biomedical Engineering.

[46]  Vince D. Calhoun,et al.  A fast algorithm for one-unit ICA-R , 2007, Inf. Sci..

[47]  Kevin Warwick,et al.  Automated Artifact Removal From the Electroencephalogram , 2013, Clinical EEG and neuroscience.

[48]  Wim Van Paesschen,et al.  Canonical Correlation Analysis Applied to Remove Muscle Artifacts From the Electroencephalogram , 2006, IEEE Transactions on Biomedical Engineering.

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

[50]  F. La Foresta,et al.  Automatic Artifact Rejection From Multichannel Scalp EEG by Wavelet ICA , 2012, IEEE Sensors Journal.

[51]  Erkki Oja,et al.  Independent component approach to the analysis of EEG and MEG recordings , 2000, IEEE Transactions on Biomedical Engineering.

[52]  Moritz Dannhauer,et al.  Modeling of the human skull in EEG source analysis , 2011, Human brain mapping.

[53]  Brian Litt,et al.  A comparison of waveform fractal dimension algorithms , 2001 .

[54]  Joachim Gross,et al.  Good practice for conducting and reporting MEG research , 2013, NeuroImage.

[55]  Vera Kaiser,et al.  What does clean EEG look like? , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[56]  I. Johnstone,et al.  Adapting to Unknown Smoothness via Wavelet Shrinkage , 1995 .

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

[58]  Zoran Nenadic,et al.  Characterization of electrocorticogram high-gamma signal in response to varying upper extremity movement velocity , 2017, Brain Structure and Function.

[59]  D F Stegeman,et al.  Muscle fiber action potential changes and surface EMG: A simulation study. , 1992, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[60]  Zoran Nenadic,et al.  Electrocorticographic Encoding of Human Gait in the Leg Primary Motor Cortex , 2018, Cerebral cortex.

[61]  Rajesh P. N. Rao,et al.  Cortical electrode localization from X-rays and simple mapping for electrocorticographic research: The “Location on Cortex” (LOC) package for MATLAB , 2007, Journal of Neuroscience Methods.

[62]  Pierre Comon,et al.  Independent component analysis, A new concept? , 1994, Signal Process..

[63]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[64]  Slawomir J. Nasuto,et al.  Automatic Artefact Removal from Event-related Potentials via Clustering , 2007, J. VLSI Signal Process..

[65]  Terrence J. Sejnowski,et al.  Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis , 2007, NeuroImage.

[66]  M. Scherg,et al.  Spatially constrained independent component analysis for artifact correction in EEG and MEG , 2001, NeuroImage.

[67]  Tomás Ward,et al.  Artifact Removal in Physiological Signals—Practices and Possibilities , 2012, IEEE Transactions on Information Technology in Biomedicine.

[68]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[69]  Mark A. Girolami,et al.  An Alternative Perspective on Adaptive Independent Component Analysis Algorithms , 1998, Neural Computation.

[70]  Jacques Duchêne,et al.  A model of EMG generation , 2000, IEEE Transactions on Biomedical Engineering.

[71]  Bin Gao,et al.  Single channel blind source separation , 2011 .

[72]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[73]  S. Muthukumaraswamy High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations , 2013, Front. Hum. Neurosci..

[74]  Marc W. Slutzky,et al.  Continuous decoding of human grasp kinematics using epidural and subdural signals , 2017, Journal of neural engineering.

[75]  Frédéric Grouiller,et al.  A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI , 2007, NeuroImage.

[76]  Jing Hu,et al.  Removal of EOG and EMG artifacts from EEG using combination of functional link neural network and adaptive neural fuzzy inference system , 2015, Neurocomputing.

[77]  Wei Wu,et al.  ARTIST: A fully automated artifact rejection algorithm for single‐pulse TMS‐EEG data , 2018, Human brain mapping.

[78]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[79]  Sabine Van Huffel,et al.  Source Separation From Single-Channel Recordings by Combining Empirical-Mode Decomposition and Independent Component Analysis , 2010, IEEE Transactions on Biomedical Engineering.

[80]  A. J. Bell,et al.  INDEPENDENT COMPONENT ANALYSIS OF BIOMEDICAL SIGNALS , 2000 .

[81]  Christiaan Burger,et al.  Removal of EOG artefacts by combining wavelet neural network and independent component analysis , 2015, Biomed. Signal Process. Control..

[82]  Richard J. Davidson,et al.  Validation of ICA-based myogenic artifact correction for scalp and source-localized EEG , 2010, NeuroImage.

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

[84]  S. Debener,et al.  Towards a truly mobile auditory brain-computer interface: exploring the P300 to take away. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[85]  Wei Lu,et al.  Approach and applications of constrained ICA , 2005, IEEE Transactions on Neural Networks.

[86]  Fang Xu,et al.  A cautionary tale of entropic criteria in assessing the validity of the maximum entropy principle , 2019, EPL (Europhysics Letters).

[87]  M. J. Katz,et al.  Fractals and the analysis of waveforms. , 1988, Computers in biology and medicine.

[88]  Yongcheng Li,et al.  A novel algorithm for removing artifacts from EEG data , 2018, 2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[89]  Matías Zañartu,et al.  Improving EEG Muscle Artifact Removal With an EMG Array , 2020, IEEE Transactions on Instrumentation and Measurement.

[90]  Roberto Hornero,et al.  Quantitative Evaluation of Artifact Removal in Real Magnetoencephalogram Signals with Blind Source Separation , 2011, Annals of Biomedical Engineering.

[91]  Begoña Garcia-Zapirain,et al.  EEG artifact removal—state-of-the-art and guidelines , 2015, Journal of neural engineering.

[92]  Guoping Gao,et al.  Removal of Ocular Artifacts in EEG—An Improved Approach Combining DWT and ANC for Portable Applications , 2013, IEEE Journal of Biomedical and Health Informatics.

[93]  Aiguo Song,et al.  EOG Artifact Correction from EEG Recording Using Stationary Subspace Analysis and Empirical Mode Decomposition , 2013, Sensors.

[94]  Carlos Guerrero-Mosquera,et al.  Automatic removal of ocular artifacts from EEG data using adaptive filtering and Independent Component Analysis , 2009, 2009 17th European Signal Processing Conference.

[95]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[96]  Jeffrey S. Maxwell,et al.  Validation of regression-based myogenic correction techniques for scalp and source-localized EEG. , 2009, Psychophysiology.

[97]  Richard J. Davidson,et al.  Electromyogenic Artifacts and Electroencephalographic Inferences , 2009, Brain Topography.

[98]  Lotfi Senhadji,et al.  Removal of muscle artifact from EEG data: comparison between stochastic (ICA and CCA) and deterministic (EMD and wavelet-based) approaches , 2012, EURASIP J. Adv. Signal Process..

[99]  Thomas R. Knösche,et al.  Influences of skull segmentation inaccuracies on EEG source analysis , 2012, NeuroImage.

[100]  Trieu H. Pham,et al.  A test of four EOG correction methods using an improved validation technique. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[101]  Terrence J. Sejnowski,et al.  AUTOMATIC ARTIFACT REJECTION FOR EEG DATA USING HIGH-ORDER STATISTICS AND INDEPENDENT COMPONENT ANALYSIS , 2001 .

[102]  W. David Hairston,et al.  Adding neck muscle activity to a head phantom device to validate mobile EEG muscle and motion artifact removal * , 2019, 2019 9th International IEEE/EMBS Conference on Neural Engineering (NER).

[103]  Pham Trieu,et al.  Empirically Validating Fully Automated EOG Artifact Correction using Independent Components Analysis , 2012 .

[104]  Mercedes Atienza,et al.  Muscle Artifact Removal from Human Sleep EEG by Using Independent Component Analysis , 2008, Annals of Biomedical Engineering.

[105]  R. Kass,et al.  Automatic correction of ocular artifacts in the EEG: a comparison of regression-based and component-based methods. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[106]  Christopher J. James,et al.  Temporally constrained ICA: an application to artifact rejection in electromagnetic brain signal analysis , 2003, IEEE Transactions on Biomedical Engineering.

[107]  Rémi Gribonval,et al.  A survey of Sparse Component Analysis for blind source separation: principles, perspectives, and new challenges , 2006, ESANN.

[108]  John P. Donoghue,et al.  Reconstructing grasping motions from high-frequency local field potentials in primary motor cortex , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[109]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

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

[111]  R. Ward,et al.  EMG and EOG artifacts in brain computer interface systems: A survey , 2007, Clinical Neurophysiology.

[112]  Patrick Berg,et al.  Artifact Correction of the Ongoing EEG Using Spatial Filters Based on Artifact and Brain Signal Topographies , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[113]  Robert D Flint,et al.  Local field potentials allow accurate decoding of muscle activity. , 2012, Journal of neurophysiology.

[114]  G. Pellizzer,et al.  Power Modulations of ECoG Alpha/Beta and Gamma Bands Correlate With Time-Derivative of Force During Hand Grasp , 2020, Frontiers in Neuroscience.

[115]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

[116]  Sabine Van Huffel,et al.  Removal of Muscle Artifacts from EEG Recordings of Spoken Language Production , 2010, Neuroinformatics.

[117]  S. P. Levine,et al.  Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement , 2003, Clinical Neurophysiology.