Abstract
Muscle artifacts are typically associated with sleep arousals and awakenings in normal and pathological sleep, contaminating EEG recordings and distorting quantitative EEG results. Most EEG correction techniques focus on ocular artifacts but little research has been done on removing muscle activity from sleep EEG recordings. The present study was aimed at assessing the performance of four independent component analysis (ICA) algorithms (AMUSE, SOBI, Infomax, and JADE) to separate myogenic activity from EEG during sleep, in order to determine the optimal method. AMUSE, Infomax, and SOBI performed significantly better than JADE at eliminating muscle artifacts over temporal regions, but AMUSE was independent of the signal-to-noise ratio over non-temporal regions and markedly faster than the remaining algorithms. AMUSE was further successful at separating muscle artifacts from spontaneous EEG arousals when applied on a real case during different sleep stages. The low computational cost of AMUSE, and its excellent performance with EEG arousals from different sleep stages supports this ICA algorithm as a valid choice to minimize the influence of muscle artifacts on human sleep EEG recordings.
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References
American Sleep Disorders Association (ASDA). EEG arousals: scoring rules and examples. Sleep 15:173–184, 1992
Barlow, J. S. Artifact processing (rejection and minimization) in EEG data processing, In: Handbook of Electroencephalography and Clinical Neurophysiology. Revised series, vol. 2, edited by F. H. Lopes da Silva, W. Storm van Leeuwen, A. Remond. Amsterdam: Elsevier, 1986, pp. 15–62
Bell A. J., T. J. Sejnowski. An information-maximization approach to blind separation and blind deconvolution. Neural. Comput. 7:1129–1159, 1995
Belouchrani A., K. Abed-Meraim, J. F. Cardoso, E. Moulines. A blind source separation technique using second order statistics. IEEE Trans. Signal Process. 45:434–444, 1997
Belouchrani A., A. Cichocki. Robust whitening procedure in blind source separation context. Electron. Lett. 36:2050–2051, 2000
Berg P., M. Scherg. Dipole models of eye activity and its application to the removal of eye artifacts from the EEG ad MEG. Clin. Physiol. Meas. 12:49–54, 2000
Bonnet M. H., D.L. Arand. EEG arousal norms by age. J. Clin. Sleep Med. 3:271–274, 2007
Boselli M., L. Parrino, A. Smerieri, M. G. Terzano. Effect of age on EEG arousals in normal sleep. Sleep 21:351–357, 1998
Boudet S., L. Peyrodie, P. Gallois, C. Vasseur. A global approach for automatic artifact removal for standard EEG record. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1:5719–5722, 2006
Brunner D. P., R. C. Vasko, C. S. Detka, J. P. Monahan, C. F. Reynolds, D. J. Kupfer. Muscle artifacts in the sleep EEG: automated detection and effect on all-night EEG power spectra. J. Sleep Res. 5:155–164, 1996
Cardoso J. F., A. Souloumiac. Blind beam-forming for non gaussian signals. IEEE Proc. Radar Signal Process. 140:362–370, 1993
Cichocki C., S. Amari. Adaptive Blind Signal and Image Processing: Learning Algorithms and Applications. Chichester: John Wiley and Sons, Ltd., 2002
Cichocki, C., S. Amari, K. Siwek, and T. Tanaka. ICALAB Toolboxes for Signal and Image Processing. http://www.bsp.brain.riken.go.jp, 2002
Cohrs S., T. Rasch, S. Altmeyer, J. Kinkelbur, T. Kostanecka, A. Rothenberger, E. Rüther, G. Hajak. Decreased sleep quality and increased sleep related movements in patients with Tourette’s syndrome. J. Neurol. Neurosurg. Psychiatry 70:192–197, 2001
Comon P. Independent component analysis, a new concept? Signal Process. 36:287–314, 1994
Croft R. J., J. S. Chandler, R. J. Barry, N. R. Cooper, A. R. Clarke. EOG correction: a comparison of four methods, Psychophysiology 42:16–24, 2005
Delorme A., S. Makeig. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134:9–21, 2004
Delorme A., T. Sejnowski, S. Makeig, Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. NeuroImage 34:1443–1449, 2007
Fantini M. L., L. Ferini-Strambi. Idiopathic rapid eye movement sleep behaviour disorder. Neurol. Sci. 1:15–20, 2007
Fatourechi M., A. Bashashati, R. K. Ward, G. E. Birch. EMG and EOG artifacts in brain computer interface systems: a survey. Clin. Neurophysiol. 118:480–494, 2007
Ferri R., O. Bruni, S. Miano, M. G. Terzano. Topographic mapping of the spectral components of the cyclic alternating pattern (CAP). Sleep Med. 6:29–36, 2005
Frank R. M., G. A. Frishkoff. Automated protocol for evaluation of electromagnetic component separation (APECS): application of a framework for evaluating statistical methods of blink extraction from multichannel EEG. Clin. Neurophysiol. 118(1):80–97, 2007
Gasser T., J. C. Schuller, U. S. Gasser. Correction of muscle artifacts in the EEG power spectrum, Clin. Neurophysiol. 116:2044–2050, 2005
Goncharova I. I., D. J. McFarland, T. M. Vaughan, J. R. Wolpaw. EMG contamination of EEG: spectral and topographical characteristics. Clin. Neurophysiol. 114:1580–1593, 2003
Gotman J., D. R. Skuce, C. J. Thompson, P. Gloor, J. R. Ives, W. F. Ray. Clinical applications of spectral analysis and extraction of features from electroencephalograms with slow waves in adult patients. Electroencephalogr. Clin. Neurophysiol. 35:225–235, 1973
Hallez H., A. Vergult, R. Phlypo, P. Van Hese, W. De Clercq, Y. D’Asseler, R. Van de Walle, B. Vanrumste, W. Van Paesschen, S. Van Huffel, I. Lemahieu. Muscle and eye movement artifact removal prior to EEG source localization. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1:1002–1005, 2006
Hening W. The clinical neurophysiology of the restless legs syndrome and periodic limb movements. Part I: diagnosis, assessment, and characterization. Clin. Neurophysiol. 115:1965–1974, 2004
Hornyak M., B. Feige, U. Voderholzer, D. Riemann. Spectral analysis of sleep EEG in patients with restless legs syndrome. Clin. Neurophysiol. 116:1265–1272, 2005
Ikeda T., K. Nishigawa, K. Kondo, H. Takeuchi, G.T. Clark. Criteria for the detection of sleep-associated bruxism in humans. J. Orofac. Pain 10:270–282, 1996
Iriarte J., E. Urrestarazu, M. Valencia, M. Alegre, A. Malanda, C. Viteri, J. Artieda. Independent component analysis as a tool to eliminate artefacts in EEG: a quantitative study. J. Clin. Neurophysiol. 20:249–257, 2003
Jasper H. H. The 10–20 electrode system of the international federation. EEG Clin. Neurophysiol. 10: 371–375, 1958
Joyce C. A., I. F. Gorodnitsky, M. Kutas. Automatic removal of eye movement and blink artifacts from EEG data using blind component separation. Psychophysiology 41:313–325, 2004
Jung T. P., C. Humphries, T. W. Lee, S. Makeig, M. J. McKeown, V. Iragui, T. J. Sejnowski. Extended ICA removes artifacts from electroencephalographic recordings. Adv. Neural Inf. Process. Syst. 10:894–900, 1998
Jung T. P., C. Humphries, T.-W. Lee, M. McKeown, V. Iragui, S. Makeig, T. J. Sejnowski. Removing electroencephalographic artifacts: comparison between ICA and PCA, IEEE Int. Workshop Neural Netw. Signal Process. 8:63–72, 1998
Jung T. P., S. Makeig, C. Humphries, T. W. Lee, M. J. Mckeown, V. Iragui, T. J. Sejnowski. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37:163–178, 2000
Karadeniz D., B. Ondze, A. Besset, M. Billiard. EEG arousals and awakenings in relation with periodic leg movements during sleep. J. Sleep Res. 9:273–277, 2000
Klass D. W. The continuing challenge of artifacts in the EEG. Am. J. EEG Technol. 35:239–269, 1995
Lee T. W., M. Girolami, T. J. Sejnowski. Independent component analysis using an extended Infomax algorithm for mixed subgaussian and supergaussian sources. Neural. Comput. 11:417–441, 1999
Mathur R., N. J. Douglas. Frequency of EEG arousals from nocturnal sleep in normal subjects. Sleep 18:330–333, 1995
Rechtschaffen A, A. Kales. A Manual for Standardized Terminology, Technique and Scoring for Sleep Stages of Human Subjects. Los Angeles: Brain Information Service/Brain Research Institute, 1968
Schwartz D. J., P. Moxley. On the potential clinical relevance of the length of arousals from sleep in patients with obstructive sleep apnea. J. Clin. Sleep Med. 2:175–180, 2006
Smurra M. V., M. Dury, G. Aubert, D. O. Rodenstein, G. Liistro. Sleep fragmentation: comparison of two definitions of short arousals during sleep in OSAS patients. Eur. Respir. J. 17:723–727, 2001
Stepanski E., J. Lamphere, P. Badia, F. Zorick, T. Roth. Sleep fragmentation and daytime sleepiness. Sleep 7:18–26, 1984
Steriade M. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb. Cortex 7:583–604, 1997
Steriade M., D. A. McCormick, T. J. Sejnowski. Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685, 1993
Stiasny K., W. H. Oertel, C. Trenkwalder. Clinical symptomatology and treatment of restless legs syndrome and periodic limb movement disorder. Sleep Med. Rev. 6:253–265, 2002
Swarnkar V., U. R. Abeyratne, C. Hukins. Inter-hemispheric asynchrony of the brain during events of apnoea and EEG arousals. Physiol. Meas. 28(8):869–880, 2007
Tang A. C., J.-Y. Liu, M. T. Sutherland. Recovery of correlated neuronal sources from EEG: the good and bad ways of using SOBI. NeuroImage 28:507–519, 2005
Tang A.C., M. T. Sutherland, C. J. McKinney. Validation of SOBI components from high density EEG. NeuroImage 25:539–553, 2005
Terzaghi, M., I. Sartori, R. Mai, L. Tassi, S. Francione, F. Cardinale, L. Castana, M. Cossu, G. Lorusso, R. Manni, and L. Nobili. Coupling of minor motor events and epileptiform discharges with arousal fluctuations in NFLE. Epilepsia 2007 (in press).
Terzano M. G., L. Parrino, M. C. Spaggiari, V. Palomba, M. Rossi, A. Smerieri. CAP variables and arousals as sleep electroencephalogram markers for primary insomnia. Clin. Neurophysiol. 114:1715–1723, 2003
Ting K. H., P. C. W. Fung, C. Q. Chang, F. H. Y. Chan. Automatic correction of artifact from single-trial event-related potentials by blind source separation using second order statistics only. Med. Eng. Phys. 28:780–794, 2006
Tong L., Y. Inouye, R. Liu. Waveform-preserving blind estimation of multiple independent sources. IEEE Trans. Signal Process. 41:2461–2470, 1993
Tong L., V. Soon, Y. F. Huang, R. Liu. Indeterminacy and identifiability of blind identification. IEEE Trans. Circuits Syst. 38:499–509, 1991
Tran Y., A. Craig, P. Boord, D. Craig. Using independent component analysis to remove artifact from electroencephalographic measured during stuttered speech. Med. Biol. Eng. Comput. 42:627–633, 2004
Urrestarazu E., J. Iriarte, M. Alegre, M. Valencia, C. Viteri, J. Artieda. Independent component analisis removing artifacts in ictal recordings. Epilepsia 45:1071–1078, 2004
Xavier P., K. Behbehani, D. Watenpaugh, J. R. Burk. Detecting electroencephalography variations due to sleep disordered breathing events. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1:6097–6100, 2007
Zhou W., J. Gotman. Removing eye-movements artifacts from the EEG during the intracarotid amobarbital procedure. Epilepsia 46:409–414, 2005
Zimmermann R., E. Scharein. MEG and EEG show different sensitivity to myogenic artifacts. Neurol. Clin. Neurophysiol. 2004:78, 2004
Acknowledgments
This research was supported by grants from European Union (FP6-2005-NEST-Path 043309), Spanish Ministry of Education and Science (SAF2005-00398), and Regional Ministry of Innovation, Science and Enterprise, Junta de Andalucia (CTS-229).
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Crespo-Garcia, M., Atienza, M. & Cantero, J.L. Muscle Artifact Removal from Human Sleep EEG by Using Independent Component Analysis. Ann Biomed Eng 36, 467–475 (2008). https://doi.org/10.1007/s10439-008-9442-y
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DOI: https://doi.org/10.1007/s10439-008-9442-y