Statistical feature extraction for artifact removal from concurrent fMRI-EEG recordings
Open accessAbstract
We propose a set of algorithms for sequentially removing artifacts related to MRI gradient switching and cardiac pulsations from electroencephalography (EEG) data recorded during functional magnetic resonance imaging (fMRI). Special emphasis is directed upon the use of statistical metrics and methods for the extraction and selection of features that characterize gradient and pulse artifacts. To remove gradient artifacts, we use channel-wise filtering based on singular value decomposition (SVD). To remove pulse artifacts, we first decompose data into temporally independent components and then select a compact cluster of components that possess sustained high mutual information with the electrocardiogram (ECG). After the removal of these components, the time courses of remaining components are filtered by SVD to remove the temporal patterns phase-locked to the cardiac timing markers derived from the ECG. The filtered component time courses are then inversely transformed into multi-channel EEG time series free of pulse artifacts. Evaluation based on a large set of simultaneous EEG-fMRI data obtained during a variety of behavioral tasks, sensory stimulations and resting conditions showed excellent data quality and robust performance attainable with the proposed methods. These algorithms have been implemented as a Matlab-based toolbox made freely available for public access and research use.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Existing methods for removing recording artifacts are mostly post-processing algorithms.
“Existing ways of removing such recording artifacts are mostly in post-processing algorithms (180).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [180]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Delorme, A., & Makeig, S. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.10.009 · Cited by 24,371 · see citing works
Peng, H., Long, F., & Ding, C. (2005) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/tpami.2005.159 · Cited by 10,614 · see citing works
An Information-Maximization Approach to Blind Separation and Blind Deconvolution
Bell, A. J., & Sejnowski, T. J. (1995) · Neural Computation · doi:10.1162/neco.1995.7.6.1129 · Cited by 8,986 · see citing works
Statistical pattern recognition: a review
Jain, A. K., Duin, P., & Mao, J. (2000) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/34.824819 · Cited by 6,795 · see citing works
A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI
Allen, P. J., Josephs, O., & Turner, R. (2000) · NeuroImage · doi:10.1006/nimg.2000.0599 · Cited by 1,301 · see citing works
Allen, P. J., Polizzi, G., Krakow, K., Fish, D. R., & Lemieux, L. (1998) · NeuroImage · doi:10.1006/nimg.1998.0361 · Cited by 914 · see citing works
Removal of FMRI environment artifacts from EEG data using optimal basis sets
Niazy, R. K., Beckmann, C. F., Iannetti, G. D., Brady, J. M., & Smith, S. M. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.067 · Cited by 569 · see citing works
On amplitude and frequency demodulation using energy operators
Maragos, P. A., Kaiser, J. F., & Quatieri, T. F. (1993) · IEEE Transactions on Signal Processing · doi:10.1109/78.212729 · Cited by 541 · see citing works
Real time electrocardiogram QRS detection using combined adaptive threshold
Christov, I. (2004) · BioMedical Engineering OnLine · doi:10.1186/1475-925x-3-28 · Cited by 468 · see citing works
A new interpretation of nonlinear energy operator and its efficacy in spike detection
Mukhopadhyay, S., & Ray, G. C. (1998) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.661266 · Cited by 387 · see citing works
Ritter, P., & Villringer, A. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.06.008 · Cited by 294 · see citing works
Acquiring simultaneous EEG and functional MRI
Goldman, R. I., Stern, J. M., Engel, J., & Cohen, M. S. (2000) · Clinical Neurophysiology · doi:10.1016/s1388-2457(00)00456-9 · Cited by 284 · see citing works
Identification of the neural sources of the pattern-reversal VEP
Russo, F. D., Pitzalis, S., Spitoni, G. F., Aprile, T., Patria, F., Donatella Spinelli, A., & Hillyard, S. A. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.029 · Cited by 269 · see citing works
Srivastava, G., Crottaz‐Herbette, S., Lau, K. M., Glover, G. H., & Menon, V. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.041 · Cited by 264 · see citing works
Quality of EEG in simultaneous EEG-fMRI for epilepsy
Bénar, C., Aghakhani, Y., Wang, Y., Izenberg, A., Al-Asmi, A. R., Dubeau, F., & Gotman, J. (2003) · Clinical Neurophysiology · doi:10.1016/s1388-2457(02)00383-8 · Cited by 259 · see citing works
Mantini, D., Perrucci, M. G., Cugini, S., Ferretti, A., Romani, G. L., & Gratta, C. D. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.037 · Cited by 236 · see citing works
Debener, S., Mullinger, K. J., Niazy, R. K., & Bowtell, R. W. (2007) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2007.05.015 · Cited by 206 · see citing works
Debener, S., Strobel, A., Sorger, B., Peters, J. C., Kranczioch, C., Engel, A. K., & Goebel, R. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.031 · Cited by 201 · see citing works
Laufs, H., Jean Daunizeau, A., Carmichael, D. W., & Kleinschmidt, A. K. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.11.039 · Cited by 193 · see citing works
Multimodal Functional Neuroimaging: Integrating Functional MRI and EEG/MEG
He, B., & Liu, Z. (2008) · IEEE Reviews in Biomedical Engineering · doi:10.1109/rbme.2008.2008233 · Cited by 171 · see citing works
Self-citationMandelkow, H., Halder, P., Boesiger, P., & Brandeis, D. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.04.231 · Cited by 154 · see citing works
Grouiller, F., Vercueil, L., Krainik, A., Segebarth, C. M., Kahane, P., & Olivier David, A. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.025 · Cited by 119 · see citing works
Simultaneous functional magnetic resonance imaging and electrophysiological recording
Huang‐Hellinger, F. R., Breiter, H. C., Mccormack, G. L., Cohen, M. S., Kwong, K. K., Sutton, J. P., Savoy, R. L., Weisskoff, R. M., Davis, T. L., Baker, J. R., et al. (1995) · Human Brain Mapping · doi:10.1002/hbm.460030103 · Cited by 117 · see citing works
Anami, K., Mori, T., Tanaka, F., Kawagoe, Y., Okamoto, J., Yarita, M., Ohnishi, T., Yumoto, M., Matsuda, H., & Saitoh, O. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00048-x · Cited by 117 · see citing works
Realignment parameter-informed artefact correction for simultaneous EEG–fMRI recordings
Moosmann, M., Schönfelder, V. H., Specht, K., Scheeringa, R., Nordby, H., & Hugdahl, K. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.01.024 · Cited by 100 · see citing works
Removal of time-varying gradient artifacts from EEG data acquired during continuous fMRI
Negishi, M., Abildgaard, M., Nixon, T., & Constable, R. T. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.04.005 · Cited by 93 · see citing works
Vanderperren, K., Vos, M. D., Ramautar, J. R., Novitskiy, N., Mennes, M., Assecondi, S., Vanrumste, B., Stiers, P. L. J., den Bergh, B. R. H. V., Wagemans, J. P., et al. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.010 · Cited by 93 · see citing works
Tong, S., Bezerianos, A., Paul, J. S., Zhu, Y., & Thakor, N. V. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00366-1 · Cited by 89 · see citing works
Nakamura, W., Anami, K., Mori, T., Saitoh, O., Cichocki, A. S., & Амари, Ш.-И. (2006) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2006.875718 · Cited by 85 · see citing works
Improved ballistocardiac artifact removal from the electroencephalogram recorded in fMRI
Kim, K. H., Yoon, H. W., & Park, H. W. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.12.016 · Cited by 84 · see citing works
Restoration of MR-induced artifacts in simultaneously recorded MR/EEG data
Sijbers, J., Michiels, I., Verhoye, M., Audekerke, J. V., der Linden, A. V., & Dyck, D. V. (1999) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(99)00096-x · Cited by 80 · see citing works
Evaluating gradient artifact correction of EEG data acquired simultaneously with fMRI
Ritter, P., Becker, R., Graefe, C., & Villringer, A. (2007) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2007.03.005 · Cited by 79 · see citing works
Reduction of ECG and gradient related artifacts in simultaneously recorded human EEG/MRI data
Sijbers, J., Audekerke, J. V., Verhoye, M., et al. (2000) · Magnetic Resonance Imaging · doi:10.1016/s0730-725x(00)00178-8 · Cited by 78 · see citing works
Ballistocardiogram artifact reduction in the simultaneous acquisition of auditory ERPS and fMRI
Ellingson, M., Liebenthal, E., Spanaki, M. V., Prieto, T. E., Binder, J. R., & ROPELLA, K. M. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.033 · Cited by 73 · see citing works
Physical modeling of pulse artefact sources in simultaneous EEG/fMRI
Yan, W. X., Mullinger, K. J., Geirsdóttir, G. B., & Bowtell, R. W. (2009) · Human Brain Mapping · doi:10.1002/hbm.20891 · Cited by 70 · see citing works
Ultrahigh-frequency EEG during fMRI: Pushing the limits of imaging-artifact correction
Freyer, F., Becker, R., Anami, K., Curio, G., Villringer, A., & Ritter, P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.06.022 · Cited by 69 · see citing works
Minimizing interference from magnetic resonance imagers during electrocardiography
Laudon, M. K., Webster, J. G., Frayne, R., et al. (1998) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.661264 · Cited by 67 · see citing works
Artifact removal in co-registered EEG/fMRI by selective average subtraction
Goncalves, S. I., Pouwels, P. J. W., Kuijer, J. P. A., Heethaar, R. M., & de Munck, J. C. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.08.017 · Cited by 64 · see citing works
An independent component analysis-based approach on ballistocardiogram artifact removing
Briselli, E., Garreffa, G., Bianchi, L., Bianciardi, M., Macaluso, E., Abbafati, M., Marciani, M. G., & Maraviglia, B. (2006) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2006.01.008 · Cited by 48 · see citing works
Leclercq, Y., Balteau, E., Dang‐Vu, T. T., Schabus, M., Luxen, A., Maquet, P., & Phillips, C. L. M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.017 · Cited by 38 · see citing works
Artifact reduction for simultaneous EEG/fMRI recording: Adaptive FIR reduction of imaging artifacts
Wan, X., Iwata, K., Riera, J. J., Kitamura, M., & Kawashima, R. (2006) · Clinical Neurophysiology · doi:10.1016/j.clinph.2005.07.025 · Cited by 34 · see citing works
Moving GLM ballistocardiogram artifact reduction for EEG acquired simultaneously with fMRI
Vincent, J. L., Larson‐Prior, L. J., Zempel, J. M., & Snyder, A. Z. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2006.12.017 · Cited by 31 · see citing works
Ryali, S., Glover, G. H., Chang, C. E., & Menon, V. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.06.072 · Cited by 28 · see citing works
Functional cortical source imaging from simultaneously recorded ERP and fMRI
Im, C., Liu, Z., Zhang, N., Chen, W., & He, B. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.03.015 · Cited by 25 · see citing works
Self-citationMandelkow, H., Brandeis, D., & Boesiger, P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.050 · Cited by 18 · see citing works
Rasheed, T., Lee, Y.-K., Lee, S. Y., et al. (2009) · Physiological Measurement · doi:10.1088/0967-3334/30/4/004 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Electrophysiological source imaging: A noninvasive window to brain dynamics
He, B., Sohrabpour, A., Brown, E., & Liu, Z. (2018) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-062117-120853 · Cited by 297 · see citing works
Self-citationBroadband Electrophysiological Dynamics Contribute to Global Resting-State fMRI Signal
Wen, H., & Liu, Z. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0187-16.2016 · Cited by 100 · see citing works
Self-citationFinding thalamic BOLD correlates to posterior alpha EEG
Liu, Z., de Zwart, J. A., Yao, B., van Gelderen, P., Kuo, L.-W., & Duyn, J. H. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.08.025 · Cited by 104 · see citing works
Self-citationMcMillan, R., Forsyth, A., Campbell, D., Malpas, G., Maxwell, E., Dukart, J., Hipp, J. F., & Muthukumaraswamy, S. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881118822263 · Cited by 21 · see citing works
Wang, S., Duan, F., & Zhang, M. (2020) · Applied Sciences · doi:10.3390/app10217465 · Cited by 10 · see citing works
- Authors
- Liu, Z., de Zwart, J. A., van Gelderen, P., Kuo, L.-W., & Duyn, J. H.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Liu, Zhongming
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2012-02
- Volume
- 59
- Issue
- 3
- Pages
- 2073-2087
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC3254729
- OpenAlex
- W2115261698
- Cited by
- 97
- References
- 46
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 5 · 2020: 8 · 2019: 6 · 2018: 11 · 2017: 5 · 2016: 11 · 2015: 10 · 2014: 7 · 2013: 3 · 2012: 2
- FWCI
- 1.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Intramural Research Program of the National Institute of Neurological Disorders and Stroke, National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Physical Sciences › Computer Science › Signal Processing › Blind Source Separation Techniques
- Keywords
- artifact removal, EEG-fMRI, singular value decomposition, independent component analysis, mutual information, electrocardiogram, feature extraction
- MeSH terms
- Adult, Algorithms, Alpha Rhythm, Data Interpretation, Statistical, Electrocardiography, Electroencephalography, Evoked Potentials, Visual, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Oxygen, Pattern Recognition, Automated, Photic Stimulation, Artifacts, Phantoms, Imaging, Principal Component Analysis, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
