Yet another artefact rejection study: an exploration of cleaning methods for biological and neuromodulatory noise

Objective. Electroencephalography (EEG) cleaning has been a longstanding issue in the research community. In recent times, huge leaps have been made in the field, resulting in very promising techniques to address the issue. The most widespread ones rely on a family of mathematical methods known as blind source separation (BSS), ideally capable of separating artefactual signals from the brain originated ones. However, corruption of EEG data still remains a problem, especially in real life scenario where a mixture of artefact components affects the signal and thus correctly choosing the correct cleaning procedure can be non trivial. Our aim is here to evaluate and score the plethora of available BSS-based cleaning methods, providing an overview of their advantages and downsides and of their best field of application. Approach. To address this, we here first characterized and modeled different types of artefact, i.e. arising from muscular or blinking activity as well as from transcranial alternate current stimulation. We then tested and scored several BSS-based cleaning procedures on semi-synthetic datasets corrupted by the previously modeled noise sources. Finally, we built a lifelike dataset affected by many artefactual components. We tested an iterative multistep approach combining different BSS steps, aimed at sequentially removing each specific artefactual component. Main results. We did not find an overall best method, as different scenarios require different approaches. We therefore provided an overview of the performance in terms of both reconstruction accuracy and computational burden of each method in different use cases. Significance. Our work provides insightful guidelines for signal cleaning procedures in the EEG related field.

[1]  Marianna Semprini,et al.  Removal of tACS artefact: a simulation study for algorithm comparison , 2019, 2019 9th International IEEE/EMBS Conference on Neural Engineering (NER).

[2]  Keinosuke Fukunaga,et al.  A Graph-Theoretic Approach to Nonparametric Cluster Analysis , 1976, IEEE Transactions on Computers.

[3]  G. Pfurtscheller,et al.  A fully automated correction method of EOG artifacts in EEG recordings , 2007, Clinical Neurophysiology.

[4]  J. Contreras-Vidal,et al.  Real-time EEG-based brain-computer interface to a virtual avatar enhances cortical involvement in human treadmill walking , 2017, Scientific Reports.

[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]  Laura Frølich,et al.  Removal of muscular artifacts in EEG signals: a comparison of linear decomposition methods , 2018, Brain Informatics.

[7]  EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities , 2019, Brain Stimulation.

[8]  Bashir I. Morshed,et al.  Unsupervised Eye Blink Artifact Denoising of EEG Data with Modified Multiscale Sample Entropy, Kurtosis, and Wavelet-ICA , 2015, IEEE Journal of Biomedical and Health Informatics.

[9]  Alfredo Brancucci,et al.  A computationally efficient method for the attenuation of alternating current stimulation artifacts in electroencephalographic recordings , 2020, Journal of neural engineering.

[10]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[11]  Markus Siegel,et al.  Phase properties of transcranial electrical stimulation artifacts in electrophysiological recordings , 2017, NeuroImage.

[12]  Xueyuan Xu,et al.  Removal of muscle artefacts from few-channel EEG recordings based on multivariate empirical mode decomposition and independent vector analysis , 2018 .

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

[14]  Kenneth Kreutz-Delgado,et al.  ICLabel: An automated electroencephalographic independent component classifier, dataset, and website , 2019, NeuroImage.

[15]  Alexander J. Casson,et al.  Removal of Gross Artifacts of Transcranial Alternating Current Stimulation in Simultaneous EEG Monitoring † , 2019, Sensors.

[16]  W. R. Adey,et al.  Contamination of scalp EEG spectrum during contraction of cranio-facial muscles. , 1974, Electroencephalography and clinical neurophysiology.

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

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

[19]  M. Nitsche,et al.  Induction of self awareness in dreams through frontal low current stimulation of gamma activity , 2014, Nature Neuroscience.

[20]  Dorothy V. M. Bishop,et al.  Journal of Neuroscience Methods , 2015 .

[21]  Karl J. Friston,et al.  Academic Software Applications for Electromagnetic Brain Mapping Using MEG and EEG , 2011, Comput. Intell. Neurosci..

[22]  P. König,et al.  Combining EEG and eye tracking: identification, characterization, and correction of eye movement artifacts in electroencephalographic data , 2012, Front. Hum. Neurosci..

[23]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[24]  Kai Wang,et al.  Independent Vector Analysis Applied to Remove Muscle Artifacts in EEG Data , 2017, IEEE Transactions on Instrumentation and Measurement.

[25]  Alexander J. Casson,et al.  Removal of Transcranial a.c. Current Stimulation artifact from simultaneous EEG recordings by superposition of moving averages , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[26]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[27]  Gary E. Birch,et al.  Online Removal of Eye Movement and Blink EEG Artifacts Using a High-Speed Eye Tracker , 2012, IEEE Transactions on Biomedical Engineering.

[28]  Pekcan Ungan,et al.  Facial muscle activity contaminates EEG signal at rest: evidence from frontalis and temporalis motor units , 2019, Journal of neural engineering.

[29]  Paul B. Fitzgerald,et al.  The effect of γ-tACS on working memory performance in healthy controls , 2015, Brain and Cognition.

[30]  C. Herrmann,et al.  Recovering Brain Dynamics During Concurrent tACS-M/EEG: An Overview of Analysis Approaches and Their Methodological and Interpretational Pitfalls , 2019, Brain Topography.

[31]  Toralf Neuling,et al.  Faith and oscillations recovered: On analyzing EEG/MEG signals during tACS , 2017, NeuroImage.

[32]  Joydeep Bhattacharya,et al.  Correction of blink artifacts using independent component analysis and empirical mode decomposition. , 2010, Psychophysiology.

[33]  Siddharth Kohli,et al.  Machine learning validation of EEG+tACS artefact removal , 2019, Journal of neural engineering.

[34]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

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

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

[37]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[38]  Martin J. McKeown,et al.  Removal of High-Voltage Brain Stimulation Artifacts From Simultaneous EEG Recordings , 2019, IEEE Transactions on Biomedical Engineering.

[39]  Christian Jutten,et al.  Joint blind source separation of multidimensional components: Model and algorithm , 2014, 2014 22nd European Signal Processing Conference (EUSIPCO).

[40]  Muhammad Ahmad Kamran,et al.  Hybrid EEG—Eye Tracker: Automatic Identification and Removal of Eye Movement and Blink Artifacts from Electroencephalographic Signal , 2016, Sensors.

[41]  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.

[42]  Tülay Adali,et al.  Joint Blind Source Separation With Multivariate Gaussian Model: Algorithms and Performance Analysis , 2012, IEEE Transactions on Signal Processing.

[43]  Peter König,et al.  Combining EEG and eye tracking: Identification, characterization and correction of eye movement artifacts in electroencephalographic data , 2012 .

[44]  Joerg F. Hipp,et al.  Physiological processes non-linearly affect electrophysiological recordings during transcranial electric stimulation , 2016, NeuroImage.

[45]  Sven Hoffmann,et al.  The Correction of Eye Blink Artefacts in the EEG: A Comparison of Two Prominent Methods , 2008, PloS one.

[46]  Lucas C. Parra,et al.  Inherent physiological artifacts in EEG during tDCS , 2019, NeuroImage.

[47]  M. M. Samani,et al.  Basic and functional effects of transcranial Electrical Stimulation (tES)—An introduction , 2018, Neuroscience and Biobehavioral Reviews.

[48]  K. Schellhorn,et al.  P 215. A method for online correction of artifacts in EEG signals during transcranial electrical stimulation , 2013, Clinical Neurophysiology.

[49]  Myung Yung Jeong,et al.  Identification and Removal of Physiological Artifacts From Electroencephalogram Signals: A Review , 2018, IEEE Access.

[50]  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..

[51]  Lucas C. Parra,et al.  Optimal use of EEG recordings to target active brain areas with transcranial electrical stimulation , 2016, NeuroImage.

[52]  Gui-Bin Bian,et al.  Removal of Artifacts from EEG Signals: A Review , 2019, Sensors.

[53]  C. Neuper,et al.  Combining Brain–Computer Interfaces and Assistive Technologies: State-of-the-Art and Challenges , 2010, Front. Neurosci..

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

[55]  Hiroaki Wagatsuma,et al.  A Removal of Eye Movement and Blink Artifacts from EEG Data Using Morphological Component Analysis , 2017, Comput. Math. Methods Medicine.

[56]  K. Jellinger Toward Brain-Computer Interfacing , 2009 .