Abstract
The artifact induced on the EEG recorded inside an MRI scanner as a result of the cardiac function—the pulse artifact (PA)—remains one of the most challenging problems in simultaneous EEG-fMRI studies. Although the biophysical mechanisms underlying the PA are not yet completely understood, an increasing body of evidence indicates three possible cardiac-related sources: bulk head motion induced by the arrival of blood to the head, pulsatile dilation of the scalp, and Hall effects in the moving blood inside the head. Based on these hypothesized mechanisms, some efforts have been made to minimize the occurrence of the PA by accordingly optimizing the recording setup or the experimental protocol. Regardless of the data acquisition procedure, however, post-processing artifact reduction is always required to some extent. Various methods have been proposed for PA reduction, which may be classified into three main categories: temporal waveform-based methods, spatiotemporal pattern-based methods, and sensor-based methods. Approaches based on independent component analysis (ICA) in combination with average artifact subtraction (AAS) have often proved to be the most effective. The use of motion sensors to estimate the PA may further improve its reduction, at the cost of modifications to the acquisition setup, including additional equipment in some cases. In general, the effects of applying PA reduction methods on the EEG data should be evaluated in each case, according to the specific experiment and research question.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abreu R, Leite M, Jorge J, Grouiller F, van der Zwaag W, Leal A, Figueiredo P (2016a) Ballistocardiogram artifact correction taking into account physiological signal preservation in simultaneous EEG-fMRI. NeuroImage 135:45–63. https://doi.org/10.1016/j.neuroimage.2016.03.034
Abreu R, Leite M, Leal A, Figueiredo P (2016b) Objective selection of epilepsy-related independent components from EEG data. J Neurosci Methods 258:67–78. https://doi.org/10.1016/j.jneumeth.2015.10.003
Abreu R, Leal A, Figueiredo P (2018) EEG-informed fMRI: a review of data analysis methods. Front Hum Neurosci 12:29. https://doi.org/10.3389/fnhum.2018.00029
Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L (1998) Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. NeuroImage 8:229–239. https://doi.org/10.1006/nimg.1998.0361
Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. NeuroImage 12:230–239. https://doi.org/10.1006/nimg.2000.0599
Anami K, Saitoh O, Yumoto M, Tanaka F, Kawagoe Y, Ohnishi T, Matsuda H (2002) Reduction of ballistocardiogram with a vacuum head-fixating system during simultaneous fMRI and multi-channel monopolar EEG recording. Int Congr Ser 1232:427–431. https://doi.org/10.1016/S0531-5131(01)00624-0
Assecondi S, Lavallee C, Ferrari P, Jovicich J (2016) Length matters: improved high field EEG-fMRI recordings using shorter EEG cables. J Neurosci Methods 269:74–87. https://doi.org/10.1016/j.jneumeth.2016.05.014
Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129–1159. https://doi.org/10.1162/neco.1995.7.6.1129
Bonmassar G, Purdon PL, Jääskeläinen IP, Chiappa K, Solo V, Brown EN, Belliveau JW (2002) Motion and ballistocardiogram artifact removal for interleaved recording of EEG and EPs during MRI. NeuroImage 16:1127–1141. https://doi.org/10.1006/nimg.2002.1125
Chowdhury MEH, Mullinger KJ, Glover P, Bowtell R (2014) Reference layer artefact subtraction (RLAS): a novel method of minimizing EEG artefacts during simultaneous fMRI. NeuroImage 84:307–319. https://doi.org/10.1016/j.neuroimage.2013.08.039
Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel AK (2005) Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25:11730–11737. https://doi.org/10.1523/JNEUROSCI.3286-05.2005
Debener S, Strobel A, Sorger B, Peters J, Kranczioch C, Engel AK, Goebel R (2007) Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: removal of the ballistocardiogram artefact. NeuroImage 34:587–597. https://doi.org/10.1016/j.neuroimage.2006.09.031
Debener S, Mullinger KJ, Niazy RK, Bowtell RW (2008) Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. Int J Psychophysiol 67:189–199. https://doi.org/10.1016/j.ijpsycho.2007.05.015
Deburchgraeve W, Cherian PJ, De Vos M, Swarte RM, Blok JH, Visser GH, Govaert P, Van Huffel S (2008) Automated neonatal seizure detection mimicking a human observer reading EEG. Clin Neurophysiol 119:2447–2454. https://doi.org/10.1016/j.clinph.2008.07.281
Ertl M, Kirsch V, Leicht G, Karch S, Olbrich S, Reiser M, Hegerl U, Pogarell O, Mulert C (2010) Avoiding the ballistocardiogram (BCG) artifact of EEG data acquired simultaneously with fMRI by pulse-triggered presentation of stimuli. J Neurosci Methods 186:231–241. https://doi.org/10.1016/J.JNEUMETH.2009.11.009
Grouiller F, Vercueil L, Krainik A, Segebarth C, Kahane P, David O (2007) A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI. NeuroImage 38:124–137. https://doi.org/10.1016/j.neuroimage.2007.07.025
Hall JE, Guyton AC (2015) Textbook of medical physiology, 11th edn. Elsevier Health Sciences, Philadelphia, PA
Hawsawi H, Carmichael DW, Lemieux L (2017) Safety of simultaneous scalp or intracranial EEG during MRI: a review. Front Phys 5:42. https://doi.org/10.3389/fphy.2017.00042
Hermans K, de Munck JC, Verdaasdonk R, Boon P, Krausz G, Prueckl R, Ossenblok P (2016) Effectiveness of reference signal-based methods for removal of EEG artifacts due to subtle movements during fMRI scanning. IEEE Trans Biomed Eng 63:2638–2646. https://doi.org/10.1109/TBME.2016.2602038
Hill RA, Chiappa KH, Huang-Hellinger F, Jenkins BG (1995) EEG during MR imaging: differentiation of movement artifact from paroxysmal cortical activity. Neurology 45:1942–1943. https://doi.org/10.1212/WNL.45.10.1942-A
Iannotti GR, Pittau F, Michel CM, Vulliemoz S, Grouiller F (2015) Pulse artifact detection in simultaneous EEG-fMRI recording based on EEG map topography. Brain Topogr 28:21–32. https://doi.org/10.1007/s10548-014-0409-z
Javed E, Faye I, Malik AS, Abdullah JM (2014) Reference-free reduction of ballistocardiogram artifact from EEG data using EMD-PCA. 2014. In: 5th International Conference Intelligent Advanced System Technological Convergence Sustainable Future ICIAS 2014—Proc, pp 14–19. https://doi.org/10.1109/ICIAS.2014.6869512
Jorge J, Van der Zwaag W, Figueiredo P (2014) EEG-fMRI integration for the study of human brain function. NeuroImage 102:24–34. https://doi.org/10.1016/j.neuroimage.2013.05.114
Jorge J, Grouiller F, Gruetter R, van der Zwaag W, Figueiredo P (2015a) Towards high-quality simultaneous EEG-fMRI at 7T: detection and reduction of EEG artifacts due to head motion. NeuroImage 120:143–153. https://doi.org/10.1016/j.neuroimage.2015.07.020
Jorge J, Grouiller F, Ipek Ö, Stoermer R, Michel CM, Figueiredo P, van der Zwaag W, Gruetter R (2015b) Simultaneous EEG-fMRI at ultra-high field: artifact prevention and safety assessment. NeuroImage 105:132–144. https://doi.org/10.1016/j.neuroimage.2014.10.055
Jorge J, Bouloc C, Bréchet L, Michel CM, Gruetter R (2019) Investigating the variability of cardiac pulse artifacts across heartbeats in simultaneous EEG-fMRI recordings: a 7T study. NeuroImage 191:21–35. https://doi.org/10.1016/J.NEUROIMAGE.2019.02.021
Krishnaswamy P, Bonmassar G, Poulsen C, Pierce ET, Purdon PL, Brown EN (2016) Reference-free removal of EEG-fMRI ballistocardiogram artifacts with harmonic regression. NeuroImage 128:398–412. https://doi.org/10.1016/j.neuroimage.2015.06.088
Laufs H (2012) A personalized history of EEG-fMRI integration. NeuroImage 62:1056–1067. https://doi.org/10.1016/j.neuroimage.2012.01.039
Leclercq Y, Balteau E, Dang-Vu T, Schabus M, Luxen A, Maquet P, Phillips C (2009) Rejection of pulse related artefact (PRA) from continuous electroencephalographic (EEG) time series recorded during functional magnetic resonance imaging (fMRI) using constraint independent component analysis (cICA). NeuroImage 44:679–691. https://doi.org/10.1016/j.neuroimage.2008.10.017
Lee T-W, Girolami M, Sejnowski TJ (1999) Independent component analysis using an extended Infomax algorithm for mixed Subgaussian and supergaussian sources. Neural Comput 11:417–441. https://doi.org/10.1162/089976699300016719
LeVan P, Maclaren J, Herbst M, Sostheim R, Zaitsev M, Hennig J (2013) Ballistocardiographic artifact removal from simultaneous EEG-fMRI using an optical motion-tracking system. NeuroImage 75:1–11. https://doi.org/10.1016/j.neuroimage.2013.02.039
Liu Z, de Zwart JA, van Gelderen P, Kuo LW, Duyn JH (2012) Statistical feature extraction for artifact removal from concurrent fMRI-EEG recordings. NeuroImage 59:2073–2087. https://doi.org/10.1016/j.neuroimage.2011.10.042
Luo Q, Huang X, Glover GH (2014) Ballistocardiogram artifact removal with a reference layer and standard EEG cap. J Neurosci Methods 233:137–149. https://doi.org/10.1016/J.JNEUMETH.2014.06.021
Maclaren J, Armstrong BSR, Barrows RT, Danishad KA, Ernst T (2012) Measurement and correction of microscopic head motion during magnetic resonance imaging of the brain. PLoS One 7:48088. https://doi.org/10.1371/journal.pone.0048088
Mantini D, Perrucci MG, Cugini S, Ferretti A, Romani GL, Del Gratta C (2007) Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis. NeuroImage 34:598–607. https://doi.org/10.1016/j.neuroimage.2006.09.037
Marino M, Liu Q, Del Castello M, Corsi C, Wenderoth N, Mantini D (2018a) Heart–brain interactions in the MR environment: characterization of the ballistocardiogram in EEG signals collected during simultaneous fMRI. Brain Topogr 31:337–345. https://doi.org/10.1007/s10548-018-0631-1
Marino M, Liu Q, Koudelka V, Porcaro C, Hlinka J, Wenderoth N, Mantini D (2018b) Adaptive optimal basis set for BCG artifact removal in simultaneous EEG-fMRI. Sci Rep 8:8902. https://doi.org/10.1038/s41598-018-27187-6
Masterton RAJ, Abbott DF, Fleming SW, Jackson GD (2007) Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings. NeuroImage 37:202–211. https://doi.org/10.1016/j.neuroimage.2007.02.060
Mullinger KJ, Morgan PS, Bowtell RW (2008) Improved artifact correction for combined electroencephalography/functional MRI by means of synchronization and use of vectorcardiogram recordings. J Magn Reson Imaging 27:607–616. https://doi.org/10.1002/jmri.21277
Mullinger, Castellone P, Bowtell R (2013a) Best current practice for obtaining high quality EEG data during simultaneous FMRI. J Vis Exp 76:50283. https://doi.org/10.3791/50283
Mullinger, Havenhand J, Bowtell R (2013b) Identifying the sources of the pulse artefact in EEG recordings made inside an MR scanner. NeuroImage 71:75–83. https://doi.org/10.1016/j.neuroimage.2012.12.070
Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20:249–264. https://doi.org/10.1007/s10548-008-0054-5
Murta T, Leite M, Carmichael DW, Figueiredo P, Lemieux L (2015) Electrophysiological correlates of the BOLD signal for EEG-informed fMRI. Hum Brain Mapp 36:391–414. https://doi.org/10.1002/hbm.22623
Neuner I, Warbrick T, Arrubla J, Felder J, Celik A, Reske M, Boers F, Shah NJ (2013) EEG acquisition in ultra-high static magnetic fields up to 9.4T. NeuroImage 68:214–220. https://doi.org/10.1016/j.neuroimage.2012.11.064
Niazy RK, Beckmann CF, Iannetti GD, Brady JM, Smith SM (2005) Removal of FMRI environment artifacts from EEG data using optimal basis sets. NeuroImage 28:720–737. https://doi.org/10.1016/j.neuroimage.2005.06.067
Niendorf T, Winter L, Frauenrath T (2012) Electrocardiogram in an MRI environment: clinical needs, practical considerations, safety implications, technical solutions and future directions. In: Advances in electrocardiograms-methods and analysis. InTech, London. https://doi.org/10.5772/24340
Nunez PL, Srinivasan R (2006) Electric fields of the brain the Neurophysics of EEG, 2nd edn. Oxford University Press, Oxford
Srivastava G, Crottaz-Herbette S, Lau KM, Glover GH, Menon V (2005) ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner. NeuroImage 24:50–60. https://doi.org/10.1016/j.neuroimage.2004.09.041
Steyrl D, Krausz G, Koschutnig K, Edlinger G, Müller-Putz GR (2017) Reference layer adaptive filtering (RLAF) for EEG artifact reduction in simultaneous EEG-fMRI. J Neural Eng 14:026003. https://doi.org/10.1088/1741-2552/14/2/026003
Steyrl D, Krausz G, Koschutnig K, Edlinger G, Müller-Putz GR (2018) Online reduction of artifacts in EEG of simultaneous EEG-fMRI using reference layer adaptive filtering (RLAF). Brain Topogr 31:129–149. https://doi.org/10.1007/s10548-017-0606-7
Tenforde TS, Gaffey CT, Moyer BR, Budlnger TF (1983) Cardiovascular alterations in Macaca monkeys exposed to stationary magnetic fields: experimental observations and theoretical analysis. Bioelectromagnetics 4:1–9. https://doi.org/10.1002/bem.2250040102
Vanderperren K, Ramautar J, Novitski N, De Vos M (2007) Ballistocardiogram artifacts in simultaneous EEG- fMRI acquisitions. Int J Bioelectromagn 9:146–150
Vanderperren K, De Vos M, Ramautar JR, Novitskiy N, Mennes M, Assecondi S, Vanrumste B, Stiers P, Van den Bergh BRH, Wagemans J, Lagae L, Sunaert S, Van Huffel S (2010) Removal of BCG artifacts from EEG recordings inside the MR scanner: a comparison of methodological and validation-related aspects. NeuroImage 50:920–934. https://doi.org/10.1016/j.neuroimage.2010.01.010
Wong CK, Luo Q, Zotev V, Phillips R, Chan KWC, Bodurka J (2018) Automatic cardiac cycle determination directly from EEG-fMRI data by multi-scale peak detection method. J Neurosci Methods 304:168–184. https://doi.org/10.1016/j.jneumeth.2018.03.017
Xia H, Ruan D, Cohen MS (2014a) Removing ballistocardiogram (BCG) artifact from full-scalp EEG acquired inside the MR scanner with orthogonal matching pursuit (OMP). Front Neurosci 8:1–12. https://doi.org/10.3389/fnins.2014.00218
Xia H, Ruan D, Cohen MS (2014b) Separation and reconstruction of BCG and EEG signals during continuous EEG and fMRI recordings. Front Neurosci 8:1–12. https://doi.org/10.3389/fnins.2014.00163
Yan WX, Mullinger KJ, Geirsdottir GB, Bowtell R (2010) Physical modeling of pulse artefact sources in simultaneous EEG/fMRI. Hum Brain Mapp 31:604–620. https://doi.org/10.1002/hbm.20891
Acknowledgments
We acknowledge the financial support by the Portuguese Science Foundation (FCT) through grants LARSyS (UIDB/50009/2020), MIG_N2Treat (PTDC/EMDEMD/29675/2017) and NeurAugVR (PTDC/CCICOM/31485/2017), by the Swiss National Science Foundation (SNSF) through grant 185909, and by the CIBM Centre for Biomedical Imaging.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Abreu, R., Jorge, J., Figueiredo, P. (2022). EEG Quality: The Pulse Artifact. In: Mulert, C., Lemieux, L. (eds) EEG - fMRI. Springer, Cham. https://doi.org/10.1007/978-3-031-07121-8_8
Download citation
DOI: https://doi.org/10.1007/978-3-031-07121-8_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-07120-1
Online ISBN: 978-3-031-07121-8
eBook Packages: MedicineMedicine (R0)