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Removing artefacts from TMS-EEG recordings using independent component analysis: Importance for assessing prefrontal and motor cortex network properties
Abstract
Introduction The combination of transcranial magnetic stimulation and electroencephalography (TMS-EEG) is emerging as a powerful tool for causally investigating cortical mechanisms and networks. However, various artefacts contaminate TMS-EEG recordings, particularly over regions such as the dorsolateral prefrontal cortex (DLPFC). The aim of this study was to substantiate removal of artefacts from TMS-EEG recordings following stimulation of the DLPFC and motor cortex using independent component analysis (ICA). Methods 36 healthy volunteers (30.8 ± 9 years, 9 female) received 75 single TMS pulses to the left DLPFC or left motor cortex while EEG was recorded from 57 electrodes. A subset of 9 volunteers also received 50 sham pulses. The large TMS artefact and early muscle activity (-2 to ~15 ms) were removed using interpolation and the remaining EEG signal was processed in two separate ICA runs using the FastICA algorithm. Five sub-types of TMS-related artefacts were manually identified: remaining muscle artefacts, decay artefacts, blink artefacts, auditory-evoked potentials and other noise-related artefacts. The cause of proposed blink and auditory-evoked potentials was assessed by concatenating known artefacts (i.e. voluntary blinks or auditory-evoked potentials resulting from sham TMS) to the TMS trials before ICA and evaluating grouping of resultant independent components (ICs). Finally, we assessed the effect of removing specific artefact types on TMS-evoked potentials (TEPs) and TMS-evoked oscillations. Results Over DLPFC, ICs from proposed muscle and decay artefacts correlated with TMS-evoked muscle activity size, whereas proposed TMS-evoked blink ICs combined with voluntary blinks and auditory ICs with auditory-evoked potentials from sham TMS. Individual artefact sub-types characteristically distorted each measure of DLPFC function across the scalp. When free of artefact, TEPs and TMS-evoked oscillations could be measured following DLPFC stimulation. Importantly, characteristic TEPs following motor cortex stimulation (N15, P30, N45, P60, N100) could be recovered from artefactual data, corroborating the reliability of ICA-based artefact correction. Conclusions Various different artefacts contaminate TMS-EEG recordings over the DLPFC and motor cortex. However, these artefacts can be removed with apparent minimal impact on neural activity using ICA, allowing the study of TMS-evoked cortical network properties.
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“During TMS-EEG, participants listened to white noise through intra-auricular earphones (Etymotic Research, ER3-14A, USA) to reduce the influence of auditory processing of the TMS click (Rogasch et al., 2014).”
From Investigation of neurobiological responses to theta burst stimulation during recovery from mild traumatic brain injury (mTBI) (2023) · cites this paper as Rogasch et al., 2014
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“Both rounds of component rejection following FastICA utilised a semiautomated artefact detection algorithm, based on previous research (Rogasch et al., 2014) and using TESA toolbox (Rogasch et al., 2017).”
From Investigation of neurobiological responses to theta burst stimulation during recovery from mild traumatic brain injury (mTBI) (2023) · cites this paper as Rogasch et al., 2014
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Valero‐Cabré, A., Amengual, J. L., Stengel, C., Pascual‐Leone, Á., & Coubard, O. A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.10.006 · Cited by 483
“…induce electrical artifacts on the recorded EEG signal hence several TMS artifact cancelation approaches have been proposed (Litvak et al., 2007; Rogasch et al., 2014; Thut et al., 2017; Thut et al., 2005) to clean as much as possible stimulation artifacts from post-pulse EEG evoked and…”
BackgroundRogasch, N. C., Sullivan, C., Thomson, R. H., Rose, N. S., Bailey, N. W., Fitzgerald, P. B., Farzan, F., & Hernandez-Pavon, J. C. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.10.031 · Cited by 411
Self-citationThe non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies
Conde, V., Tomasevic, L., Akopian, I., Stanek, K., Saturnino, G. B., Thielscher, A., Bergmann, T. O., & Siebner, H. R. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.10.052 · Cited by 343
“…the amplitudes of the TEPs were well within the range of previous TMS-EEG studies on healthy conscious individuals, ranging from 2 to 6 μV (Herring et al., 2015; Kahkonen et al., 2005; Kerwin et al., 2018; Komssi et al., 2004; Noda et al., 2016; Premoli et al., 2014a; Rogasch et al., 2014).”
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“Following the interference approach, the coil position and orientation producing themaximally disruptive effects is considered optimal, e.g. when functionally localizing Broca's area by inducing speech arrest (Rogic et al., 2014) or to localize the FEF by saccade delay (Ro et al., 2002).”
TMS combined with EEG: Recommendations and open issues for data collection and analysis
Hernandez-Pavon, J. C., Veniero, D., Bergmann, T. O., Belardinelli, P., Bortoletto, M., Casarotto, S., Casula, E. P., Farzan, F., Fecchio, M., Julkunen, P., et al. (2023) · Brain Stimulation · doi:10.1016/j.brs.2023.02.009 · Cited by 238
“Figure created with BioRender.com. and 180 (P180) milliseconds [28,32,35,36].”
InfluentialSelf-citationThut, G., Bergmann, T. O., Frӧhlich, F., Soekadar, S. R., Brittain, J., Valero‐Cabré, A., Sack, A. T., Miniussi, C., Antal, A., Siebner, H. R., et al. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2017.01.003 · Cited by 280
“For TMS, these consist of auditory and tactile sensations (and associated cranial muscle potentials) (Nikouline et al., 1999; Mutanen et al., 2013; Rogasch et al., 2014).”
BackgroundDisentangling EEG responses to TMS due to cortical and peripheral activations
Rocchi, L., Santo, A. D., Brown, K. E., Ibáñez, J., Casula, E. P., Rawji, V., Lazzaro, V. D., Koch, G., & Rothwell, J. C. (2020) · Brain stimulation · doi:10.1016/j.brs.2020.10.011 · Cited by 202
“The early ones reflect brainstem activation; they last for a few ms after the 436 stimulation (25) and are not considered here, since pre-processing of TMS-EEG data usually 437 removed data in that time window (21, 26).”
BackgroundMethodInfluentialFarzan, F., Vernet, M., Shafi, M. M. D., Rotenberg, A., Daskalakis, Z. J., & Pascual-Leone, A. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00073 · Cited by 173
Self-citationCash, R. F. H., Noda, Y., Zomorrodi, R., Radhu, N., Farzan, F., Rajji, T. K., Fitzgerald, P. B., Chen, R. E., Daskalakis, Z. J., & Blumberger, D. M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.133 · Cited by 178
“The absence of P30 in DLPFC is consistent with previous findings that P30 is expressed to a lesser extent in DLPFC compared with M1 (c.f. Figure 6A,B and 10A,B Rogasch et al, 2014; Van Der Werf and Paus, 2006).”
BackgroundMethodResultInfluentialSelf-citationMethods for analysis of brain connectivity: An IFCN-sponsored review
Rossini, P. M., Iorio, R. D., Bentivoglio, M., Bertini, G., Ferreri, F., Gerloff, C. P., Ilmoniemi, R. J., Miraglia, F., Nitsche, M. A., Pestilli, F., et al. (2019) · Clinical Neurophysiology · doi:10.1016/j.clinph.2019.06.006 · Cited by 169
“, 2015) and state-of-the-art methodologies are applied to minimize confounding factors (Casarotto et al., 2010; Rogasch et al., 2014).”
BackgroundCharacterizing and minimizing the contribution of sensory inputs to TMS-evoked potentials
Biabani, M., Fornito, A., Mutanen, T. P., Morrow, J., & Rogasch, N. C. (2019) · Brain Stimulation · doi:10.1016/j.brs.2019.07.009 · Cited by 158
Self-citationRogasch, N. C., Daskalakis, Z. J., & Fitzgerald, P. B. (2014) · Cortex · doi:10.1016/j.cortex.2014.10.003 · Cited by 158
Self-citationChung, S. W., Rogasch, N. C., Hoy, K. E., Sullivan, C. M., Cash, R. F. H., & Fitzgerald, P. B. (2017) · Human Brain Mapping · doi:10.1002/hbm.23882 · Cited by 155
“(2) Original data were bandpass filtered at 1–80 Hz, and FastICA with artefact component removal was conducted as described above (only one round of ICA).”
BackgroundMethodResultInfluentialSelf-citationTMS-EEG signatures of glutamatergic neurotransmission in human cortex
Belardinelli, P., König, F., Liang, C., Premoli, I., Desideri, D., Müller‐Dahlhaus, F., Gordon, P. C., Zipser, C. M., Zrenner, C., & Ziemann, U. (2021) · Scientific Reports · doi:10.1038/s41598-021-87533-z · Cited by 151
Sun, Y., Farzan, F., Mulsant, B. H., Rajji, T. K., Fitzgerald, P. B., Barr, M. S., Downar, J. H., Wong, W., Blumberger, D. M., & Daskalakis, Z. J. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.3097 · Cited by 141
Self-citationVoineskos, D., Blumberger, D. M., Zomorrodi, R., Rogasch, N. C., Farzan, F., Foussias, G., Rajji, T. K., & Daskalakis, Z. J. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.09.032 · Cited by 141
Self-citationChung, S. W., Lewis, B. P., Rogasch, N. C., Saeki, T., Thomson, R. H., Hoy, K. E., Bailey, N. W., & Fitzgerald, P. B. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2017.04.005 · Cited by 133
Self-citationRemoval of Muscle Artifacts From the EEG: A Review and Recommendations
Chen, X., Xu, X., Liu, A., Lee, S., Chen, X. '., Zhang, X., McKeown, M. J., & Wang, Z. J. (2019) · IEEE Sensors Journal · doi:10.1109/jsen.2019.2906572 · Cited by 133
“[31], [51], [70]–[72], canonical correlation analysis (CCA)”
Measuring Brain Stimulation Induced Changes in Cortical Properties Using TMS-EEG
Chung, S. W., Rogasch, N. C., Hoy, K. E., & Fitzgerald, P. B. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.07.029 · Cited by 129
“Electrophysiological responses induced by a single pulse TMS can be illustrated with waveforms and topographic representation of TMS-evoked potentials (TEPs), providing a direct measure of brain activity [51].”
BackgroundSelf-citationHill, A. T., Rogasch, N. C., Fitzgerald, P. B., & Hoy, K. E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.006 · Cited by 131
Self-citationTAAC - TMS Adaptable Auditory Control: A universal tool to mask TMS clicks
Russo, S., Sarasso, S., Puglisi, G. E., Palù, D. D., Pigorini, A., Casarotto, S., D’Ambrosio, S., Astolfi, A., Massimini, M., Rosanova, M., et al. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109491 · Cited by 126
Darmani, G., Zipser, C. M., Böhmer, G. M., Deschet, K., Müller‐Dahlhaus, F., Belardinelli, P., Schwab, M. G., & Ziemann, U. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1689-16.2016 · Cited by 124
“Independent component analysis was then used to remove components reflecting TMS-induced muscle activity and TMS artifacts (within the first 50 ms after the TMS pulse) from TEPs based on each participant’s data (Rogasch and Fitzgerald, 2013; Rogasch et al., 2014).”
MethodBrain responsivity provides an individual readout for motor recovery after stroke
Tscherpel, C., Dern, S., Hensel, L., Ziemann, U., Fink, G. R., & Grefkes, C. (2020) · Brain · doi:10.1093/brain/awaa127 · Cited by 129
“By using the EEGLAB function runica, independent component analysis was applied to remove residual TMS-related artefacts as well as ocular or muscle artefacts (Rogasch et al., 2014).”
MethodChung, S. W., Sullivan, C. M., Rogasch, N. C., Hoy, K. E., Bailey, N. W., Cash, R. F. H., & Fitzgerald, P. B. (2018) · Human Brain Mapping · doi:10.1002/hbm.24398 · Cited by 123
“The first ICA was used to remove the remaining tail of TMS-evoked muscle artefacts (Rogasch et al., 2014) which was identified if the component time course was eight times larger than the mean absolute amplitude across the entire time course.”
BackgroundMethodResultSelf-citationSpampinato, D. A., Ibáñez, J., Rocchi, L., & Rothwell, J. C. (2023) · The Journal of Physiology · doi:10.1113/jp281885 · Cited by 147
“For instance, if TMS is applied over lateral areas, including M1, EMG activity caused by direct scalp muscle activation can contaminate the EEG signal, requiring special cleaning techniques (Hernandez-Pavon et al., 2012; Rogasch et al., 2014; Salo et al., 2020).”
BackgroundRecovering TMS-evoked EEG responses masked by muscle artifacts
Mutanen, T. P., Kukkonen, M., Nieminen, J. O., Stenroos, M., Sarvas, J., & Ilmoniemi, R. J. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.05.028 · Cited by 111
“Therefore, effective artifact-removal methods are needed to improve the usability of TMS–EEG. Independent component analysis (ICA) has been suggested to separate TMS–EEG data to brain and muscle-artifact signal components (Korhonen et al., 2011; Hernandez-Pavon et al., 2012; Rogasch et al., 2014).”
Hill, A. T., Rogasch, N. C., Fitzgerald, P. B., & Hoy, K. E. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.03.001 · Cited by 105
“The TEP waveform elicited following a single TMS pulse consists of a number of positive and negative deflections occurring over a period of up to 300 ms (Farzan et al., 2016; Rogasch et al., 2014).”
Self-citationEffects of antiepileptic drugs on cortical excitability in humans: A TMS‐EMG and TMS‐EEG study
Darmani, G., Bergmann, T. O., Zipser, C. M., Baur, D., Müller‐Dahlhaus, F., & Ziemann, U. (2018) · Human Brain Mapping · doi:10.1002/hbm.24448 · Cited by 104
“Part of the P180 component is likely caused by auditory evoked activity induced by the click of the stimulating coil (Conde et al., 2018; Rogasch et al., 2014).”
BackgroundBenwell, C., Davila-Pérez, P., Fried, P. J., Jones, R. N., Travison, T. G., Santarnecchi, E., Pascual‐Leone, Á., & Shafi, M. M. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.10.004 · Cited by 108
Effects of pulse width, waveform and current direction in the cortex: A combined cTMS-EEG study
Casula, E. P., Rocchi, L., Hannah, R., & Rothwell, J. C. (2018) · Brain stimulation · doi:10.1016/j.brs.2018.04.015 · Cited by 97
“Alternatively, it is possible that the reverse phase of biphasic pulses could have partially impeded the activation of neurons involved in the origin of late TEPs.”
InfluentialChung, S. W., Rogasch, N. C., Hoy, K. E., & Fitzgerald, P. B. (2018) · Brain Stimulation · doi:10.1016/j.brs.2018.01.002 · Cited by 98
Self-citationARTIST: A fully automated artifact rejection algorithm for single‐pulse TMS‐EEG data
Wu, W., Keller, C. J., Rogasch, N. C., Longwell, P., Shpigel, E., Rolle, C. E., & Etkin, A. (2018) · Human Brain Mapping · doi:10.1002/hbm.23938 · Cited by 90
“One limitation of this study is that the masking white noise was not used during the acquisition of the spTMS-EEG data and the resulting auditory-evoked potential artifacts were not considered in ARTIST (Rogasch et al., 2014).”
MethodSelf-citationVariability and Predictors of Response to Continuous Theta Burst Stimulation: A TMS-EEG Study
Rocchi, L., Ibáñez, J., Benussi, A., Hannah, R., Rawji, V., Casula, E., & Rothwell, J. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00400 · Cited by 77
Martínek, R., Ládrová, M., Šidiková, M., Jaroš, R., Behbehani, K., Kahankova, R. V., & Kawala‐Sterniuk, A. (2021) · Sensors · doi:10.3390/s21155186 · Cited by 102
The impact of artifact removal approaches on TMS–EEG signal
Bertazzoli, G., Esposito, R., Mutanen, T. P., Ferrari, C., Ilmoniemi, R. J., Miniussi, C., & Bortoletto, M. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118272 · Cited by 82
Short-interval and long-interval intracortical inhibition of TMS-evoked EEG potentials
Premoli, I., Király, J., Müller‐Dahlhaus, F., Zipser, C. M., Rossini, P. G., Zrenner, C., Ziemann, U., & Belardinelli, P. (2018) · Brain stimulation · doi:10.1016/j.brs.2018.03.008 · Cited by 82
“Components were visually inspected considering time course, topographical distribution and amplitude allowing removal of residual muscle activity [31] appearing mostly in the fronto-temporal region ipsilateral to the stimulation site, TMS-related artifacts showing exponential decays, and recharge artifacts around 200…”
MethodSurvey on Brain-Computer Interface
Bablani, A., Edla, D. R., Tripathi, D., & Cheruku, R. (2019) · ACM Computing Surveys · doi:10.1145/3297713 · Cited by 82
“…have been performed for artifact removal by applying ICA, such as voluntary and involuntary eye blink detection [84], ICA on time series fMRI data [31], removal of muscles, decay, blink, and auditory data using Transcranial Magnetic Stimulation and Electroencephalography (TMS-EEG) [129].”
MethodGordon, P. C., Jovellar, D. B., Song, Y., Zrenner, C., Belardinelli, P., Siebner, H. R., & Ziemann, U. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118708 · Cited by 84
Identification and verification of a 'true' TMS evoked potential in TMS-EEG
Farzan, F., & Bortoletto, M. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109651 · Cited by 78
Self-citationVoineskos, D., Blumberger, D. M., Rogasch, N. C., Zomorrodi, R., Farzan, F., Foussias, G., Rajji, T. K., & Daskalakis, Z. J. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.05.008 · Cited by 72
Self-citationAtluri, S., Frehlich, M., Mei, Y., García-Domínguez, L., Rogasch, N., Wong, W., Daskalakis, Z., & Farzan, F. (2016) · Front. Neural Circuits · doi:10.3389/fncir.2016.00078 · Cited by 60
“The efficacy of blind source separation in removing TMS-related artifacts has been documented previously and will not be discussed here (e.g., Litvak et al., 2007; Mäki and Ilmoniemi, 2011; Rogasch et al., 2014; Lyzhko et al., 2015).”
BackgroundResultInfluentialSelf-citationDesideri, D., Zrenner, C., Ziemann, U., & Belardinelli, P. (2019) · The Journal of Physiology · doi:10.1113/jp278638 · Cited by 76
“4A, B) were comparable to the typical M1 TEP topographies reported in the literature (Bonato et al. 2006; Farzan et al. 2013; Rogasch et al. 2014; Premoli et al. 2014a; Petrichella et al. 2017).”
ResultGordon, P. C., Zrenner, C., Desideri, D., Belardinelli, P., Zrenner, B., Brunoni, A. R., & Ziemann, U. (2018) · Brain stimulation · doi:10.1016/j.brs.2018.06.004 · Cited by 66
The role of neuronavigation in TMS–EEG studies: Current applications and future perspectives
Lioumis, P., & Rosanova, M. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109677 · Cited by 61
Lamotrigine and levetiracetam exert a similar modulation of TMS‐evoked EEG potentials
Premoli, I., Biondi, A., Carlesso, S., Rivolta, D., & Richardson, M. P. (2016) · Epilepsia · doi:10.1111/epi.13599 · Cited by 63
“independent component analysis (FastICA).(25) Components were removed on the basis of the spatiotemporal profile indicating the activation of temporal muscles, and by an activation of opposed polarity mainly recorded over frontocentral electrodes.”
MethodRagazzoni, A., Cincotta, M., Giovannelli, F., Cruse, D., Young, G. B., Miniussi, C., & Rossi, S. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2017.06.037 · Cited by 65
“…have allowed the successful co-registration of brain activity during and immediately following TMS without saturation (for revisions see Komssi and Kahkonen, 2006; Miniussi and Thut, 2010; Rogasch and Fitzgerald, 2013; but see also Rogasch et al., 2014; Atluri et al., 2016; Mutanen et al., 2016).”
BackgroundNoda, Y., Zomorrodi, R., Cash, R. F. H., Barr, M. S., Farzan, F., Rajji, T. K., Chen, R. E., Daskalakis, Z. J., & Blumberger, D. M. (2017) · Aging · doi:10.18632/aging.101178 · Cited by 58
Self-citationAlyagon, U., Shahar, H., Hadar, A. A., Barnea‐Ygael, N., Lazarovits, A., Shalev, H., & Zangen, A. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102206 · Cited by 62
“The probability of a TMS pulse to produce either a motor or a visual response is reduced with greater Alpha power under the stimulation area (Romei et al., 2008; Samaha et al., 2017; Sauseng et al., 2009).”
BackgroundHarquel, S., Bacle, T., Beynel, L., Marendaz, C., Chauvin, A., & Olivier David, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.05.009 · Cited by 59
“The first ICA suppressed the muscle artifacts, while the second aimed at removing the decay artifact, ocular activity, auditory-evoked potentials and other noise-related artifacts (Rogasch et al., 2014).”
BackgroundMethodInfluentialRogasch, N. C., Zipser, C. M., Darmani, G., Mutanen, T. P., Biabani, M., Zrenner, C., Desideri, D., Belardinelli, P., Müller‐Dahlhaus, F., & Ziemann, U. (2020) · Scientific Reports · doi:10.1038/s41598-020-59911-6 · Cited by 57
Self-citationNoreika, V., Kamke, M. R., Canales‐Johnson, A., Chennu, S., Bekinschtein, T. A., & Mattingley, J. B. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117305 · Cited by 65
Che, X., Cash, R. F. H., Chung, S. W., Bailey, N. W., Fitzgerald, P. B., & Fitzgibbon, B. M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116053 · Cited by 60
Self-citationTranscranial Evoked Potentials Can Be Reliably Recorded with Active Electrodes
Mancuso, M., Sveva, V., Cruciani, A., Brown, K. E., Ibáñez, J., Rawji, V., Casula, E. P., Premoli, I., D’Ambrosio, S., Rothwell, J. C., et al. (2021) · Brain Sciences · doi:10.3390/brainsci11020145 · Cited by 58
“After epoching, the early, TMS-locked artefacts [20] were removed by means of a fastICA algorithm; only the 15 components explaining the largest variance were plotted, in a time window ranging from −200 to 500 ms, and only those reflecting residual scalp muscle or decay were eliminated after visual inspection, based o…”
MethodTMS-evoked long-lasting artefacts: A new adaptive algorithm for EEG signal correction
Casula, E. P., Bertoldo, A., Tarantino, V., Maiella, M., Koch, G., Rothwell, J. C., TOFFOLO, G. M., & Bisiacchi, P. S. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2017.06.003 · Cited by 58
“…through a phantom (Bender et al., 2005) or a TMS control condition (Thut et al., 2003) is subtracted from the data; (2) independent component analysis (ICA) or principal component analysis (PCA) (e.g. Korhonen et al., 2011; Ter Braack et al., 2013; Metsomaa et al., 2014; Rogasch et al., 2014).”
InfluentialMartínek, R., Ládrová, M., Šidiková, M., Jaroš, R., Behbehani, K., Kahankova, R. V., & Kawala‐Sterniuk, A. (2021) · Sensors · doi:10.3390/s21196343 · Cited by 58
Du, X. M., Choa, F., Summerfelt, A. T., Rowland, L. M., Chiappelli, J., Kochunov, P. V., & Hong, L. E. (2016) · Experimental Brain Research · doi:10.1007/s00221-016-4773-7 · Cited by 54
“However, to fully exclude the explanation of muscle activity, methods thoroughly removing TMS artifacts, such as independent component analysis, are needed (Rogasch et al. 2014).”
Ye, Y., Wang, J., & Che, X. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab493 · Cited by 52
Opie, G. M., Rogasch, N. C., Goldsworthy, M. R., Ridding, M. C., & Semmler, J. G. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.08.004 · Cited by 53
“However, this confounding influence is significantly reduced bywhite noise masking during stimulation [52], in addition to the use of independent component analysis [27], both of which were utilised within the current study.”
Self-citationHill, A. T., Rogasch, N. C., Fitzgerald, P. B., & Hoy, K. E. (2018) · Cortex · doi:10.1016/j.cortex.2018.11.022 · Cited by 51
Self-citationRogasch, N. C., Biabani, M., & Mutanen, T. P. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109494 · Cited by 56
Self-citationRemoving artifacts from TMS-evoked EEG: A methods review and a unifying theoretical framework
Hernandez-Pavon, J. C., Kugiumtzis, D., Zrenner, C., Kimiskidis, V. Κ., & Metsomaa, J. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109591 · Cited by 55
Self-citationGordon, P. C., Belardinelli, P., Stenroos, M., Ziemann, U., & Zrenner, C. (2022) · Brain stimulation · doi:10.1016/j.brs.2022.02.006 · Cited by 55
“Trials were inspected visually, epochs and channels with excessive noise were excluded, and further artifacts were removed with a 2-step independent component analysis procedure [44,45].”
MethodResultDealing with artifacts in TMS-evoked EEG
Ilmoniemi, R. J., Hernandez-Pavon, J. C., Mäkelä, N., Metsomaa, J., Mutanen, T. P., Stenroos, M., & Sarvas, J. (2015) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/embc.2015.7318342 · Cited by 48
“ICA can usually explain artifactual parts of the data with just a few components [18, 31].”
BackgroundSelf-citationNoda, Y., Barr, M. S., Zomorrodi, R., Cash, R. F. H., Rajji, T. K., Farzan, F., Chen, R. E., George, T. P., Daskalakis, Z. J., & Blumberger, D. M. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx041 · Cited by 49
Self-citationCortical inhibition assessed using paired-pulse TMS-EEG is increased in older adults
Opie, G. M., Sidhu, S. K., Rogasch, N. C., Ridding, M. C., & Semmler, J. G. (2017) · Brain stimulation · doi:10.1016/j.brs.2017.12.013 · Cited by 48
Self-citationMotor Cortical Network Excitability in Parkinson's Disease
Leodori, G., Bartolo, M. I. D., Guerra, A., Fabbrini, A., Rocchi, L., Latorre, A., Paparella, G., Belvisi, D., Conte, A., Bhatia, K. P., et al. (2022) · Movement Disorders · doi:10.1002/mds.28914 · Cited by 47
Strafella, R., Momi, D., Zomorrodi, R., Lissemore, J. I., Noda, Y., Chen, R. E., Rajji, T. K., Griffiths, J. D., Vila‐Rodriguez, F., Downar, J. H., et al. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.04.011 · Cited by 48
Self-citationVarone, G., Hussain, Z. U., Sheikh, Z., Howard, A., Boulila, W., Mahmud, M., Howard, N., Morabito, F., & Hussain, A. (2021) · Italian National Conference on Sensors · doi:10.3390/s21020637 · Cited by 43
Identifying novel biomarkers with TMS-EEG – Methodological possibilities and challenges
Kallioniemi, E., & Daskalakis, Z. J. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109631 · Cited by 49
Self-citationTranscranial Magnetic Stimulation–Electroencephalography for Biomarker Discovery in Psychiatry
Farzan, F. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.12.018 · Cited by 45
Self-citationOscillatory TMS-EEG-Responses as a Measure of the Cortical Excitability Threshold
Saari, J., Kallioniemi, E., Tarvainen, M. P., & Julkunen, P. (2017) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2017.2779135 · Cited by 45
“2) display commonly reported peaks in motor cortex stimulation [20], [24], [25], [43], [49], [50].”
BackgroundMethodInfluentialPharmacological mechanisms of interhemispheric signal propagation: a TMS-EEG study
Hui, J., Zomorrodi, R., Lioumis, P., Salavati, B., Rajji, T. K., Chen, R. E., Blumberger, D. M., & Daskalakis, Z. J. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0468-7 · Cited by 45
Self-citationTMS-EEG perturbation biomarkers for Alzheimer’s disease patients classification
Tăuţan, A.-M., Casula, E. P., Pellicciari, M. C., Borghi, I., Maiella, M., Bonnı̀, S., Minei, M., Assogna, M., Palmisano, A., Smeralda, C. L., et al. (2023) · Scientific Reports · doi:10.1038/s41598-022-22978-4 · Cited by 44
Intracortical Inhibition and Surround Inhibition in the Motor Cortex: A TMS-EEG Study
Leodori, G., Thirugnanasambandam, N., Conn, H., Popa, T., Berardelli, A., & Hallett, M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00612 · Cited by 44
Freedberg, M., Reeves, J. A., Hussain, S. J., Zaghloul, K. A., & Wassermann, E. M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0216185 · Cited by 44
“The first round of ICA included an automated artifact detection algorithm (tesa_compselect) [8] to remove large pulse-related artifacts.”
MethodInfluentialDose-response of intermittent theta burst stimulation of the prefrontal cortex: A TMS-EEG study
Desforges, M., Hadas, I., Mihov, B., Morin, Y., Braün, M. R., Lioumis, P., Zomorrodi, R., Théoret, H., Lepage, M., Daskalakis, Z. J., et al. (2022) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.12.018 · Cited by 45
Self-citationResting Motor Threshold, MEP and TEP Variability During Daytime
ter Braack, E. M., de Goede, A. A., & van Putten, M. J. A. M. (2018) · Brain Topography · doi:10.1007/s10548-018-0662-7 · Cited by 43
Noda, Y., Cash, R. F. H., Zomorrodi, R., Dominguez, L. G., Farzan, F., Rajji, T. K., Barr, M. S., Chen, R. E., Daskalakis, Z. J., & Blumberger, D. M. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00260.2016 · Cited by 43
“EEG signal processing was performed in line with previous methodology outlined in Rogasch et al. (2014).”
BackgroundMethodSelf-citationRaffin, E., Harquel, S., Passera, B., Chauvin, A., Bougerol, T., & Olivier David, A. (2020) · Human Brain Mapping · doi:10.1002/hbm.24975 · Cited by 41
“The first ICA suppressed the muscle artifacts, while the second ICA aimed at removing the decay artifact, ocular activity, auditoryevoked potentials, and other noise-related artifacts (Rogasch et al., 2014).”
MethodThe influence of endogenous estrogen on transcranial direct current stimulation: A preliminary study
Lee, S., Chung, S. W., Rogasch, N. C., Thomson, C. J., Worsley, R., Kulkarni, J., Thomson, R. H., Fitzgerald, P. B., & Segrave, R. A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14085 · Cited by 41
“The N120 and P200 were selected as the focus for analysis as they are reliably induced components of the cortical response to DLPFC stimulation, and both peaks were reliably elicited in all participants the current sample (Rogasch, Daskalakis, & Fitzgerald, 2015; Rogasch et al., 2014).”
BackgroundMethodInfluentialSelf-citationTMS as a pharmacodynamic indicator of cortical activity of a novel anti‐epileptic drug, XEN1101
Premoli, I., Rossini, P. G., Goldberg, P., Posadas, K., Green, L., Yogo, N., Pimstone, S. N., Abela, E., Beatch, G. N., & Richardson, M. P. (2019) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.50896 · Cited by 41
“On average, 17 components (range 4–24) were deleted following the procedures described in a previous report.(19) Finally, remaining data were baseline-corrected (from 600 to 50 msec), band-pass filtered (2–80 Hz) and rereferenced to the average channel signal.”
MethodBiabani, M., Fornito, A., Coxon, J. P., Fulcher, B. D., & Rogasch, N. C. (2021) · The Journal of Physiology · doi:10.1113/jp280966 · Cited by 41
“based on the method described in [40, 41], performed by custom scripts written in MATLAB (R2016b, The Mathworks, USA) using the functions provided by EEGLAB [42] and TESA [40] toolboxes.”
MethodSelf-citationLuo, X., Che, X., & Li, H. (2022) · International Journal of Clinical and Health Psychology · doi:10.1016/j.ijchp.2022.100343 · Cited by 41
Wong, W., Noreika, V., Móró, L., Revonsuo, A., Windt, J., Valli, K., & Tsuchiya, N. (2020) · Neuroscience of Consciousness · doi:10.1093/nc/niaa006 · Cited by 40
Kallioniemi, E., Saari, J., Ferreri, F., & Määttä, S. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109430 · Cited by 40
A structured ICA-based process for removing auditory evoked potentials
Ross, J. M., Ozdemir, R. A., Lian, S. J., Fried, P. J., Schmitt, E. M., Inouye, S. K., Pascual‐Leone, Á., & Shafi, M. M. (2022) · Scientific Reports · doi:10.1038/s41598-022-05397-3 · Cited by 40
“An initial round of fast independent component analysis (fICA) 60 was performed to identify and remove exclusively components with early TMS evoked high amplitude electrode and EMG artifacts 52,61 .”
MethodResultSingle and paired pulse transcranial magnetic stimulation in drug naïve epilepsy
de Goede, A. A., ter Braack, E. M., & van Putten, M. J. A. M. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2016.06.025 · Cited by 43
Assessing cerebellar-cortical connectivity using concurrent TMS-EEG: a feasibility study
Fernández, L., Biabani, M., Do, M., Opie, G. M., Hill, A. T., Barham, M. P., Teo, W., Byrne, L. K., Rogasch, N. C., & Enticott, P. G. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00617.2020 · Cited by 39
Self-citationTia, B., Takemi, M., Kosugi, A., Castagnola, E., Ansaldo, A., Nakamura, T., Ricci, D., Ushiba, J., Fadiga, L., & Iriki, A. (2017) · The Journal of Physiology · doi:10.1113/jp274629 · Cited by 37
“The segments including large amplitude artifacts, which are problematic for accurate independent component analysis (ICA) decomposition, as well as saturated channels, were removed (Rogasch et al. 2014).”
BackgroundGedankien, T., Fried, P. J., Pascual‐Leone, Á., & Shafi, M. M. (2017) · Clinical Neurophysiology · doi:10.1016/j.clinph.2017.08.034 · Cited by 38
“Following iTBS, MEPs and TEPs ation. residual TMS pulse artifact, single-electrode noise and other electrical artifacts (Rogasch et al., 2014).”
MethodNoda, Y. (2019) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12936 · Cited by 38
The influence of endogenous estrogen on high-frequency prefrontal transcranial magnetic stimulation
Chung, S. W., Thomson, C. J., Lee, S., Worsley, R., Rogasch, N. C., Kulkarni, J., Thomson, R. H., Fitzgerald, P. B., & Segrave, R. A. (2019) · Brain stimulation · doi:10.1016/j.brs.2019.05.007 · Cited by 38
Self-citationBridging the gap: TMS-EEG from lab to clinic
Julkunen, P., Kimiskidis, V. Κ., & Belardinelli, P. (2022) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2022.109482 · Cited by 40
“In TMS-EEG responses, the signal processing is also crucial in removing other than meaningful TEP-signal (Rogasch et al., 2014), and openly available tools (Atluri et al., 2016; Bertazzoli et al., 2021; Mutanen et al., 2018; Wu et al., 2018) have been provided for quite effective removal of…”
BackgroundMethodInfluentialAssessing effective connectivity of the cerebellum with cerebral cortex using TMS-EEG
Gaßmann, L., Gordon, P. C., & Ziemann, U. (2022) · Brain stimulation · doi:10.1016/j.brs.2022.09.013 · Cited by 36
“A two-step independent component analysis (ICA) was then performed on the resulting data [36].”
MethodDeprez, H., Gransier, R., Hofmann, M., Wieringen, A. V., Wouters, J. M., & Moonen, M. (2016) · Biomedical Signal Processing and Control · doi:10.1016/j.bspc.2016.07.013 · Cited by 35
Ross, J. M., Sarkar, M., & Keller, C. J. (2022) · Human Brain Mapping · doi:10.1002/hbm.25990 · Cited by 34
“Although it is difficult to match the sensory experience of active TMS with sham TMS, the topography and time course of evoked sensory potentials may be similar (Biabani et al., 2019) enough to employ an ICA-based technique for removal (Rogasch, Thomson, et al., 2014; Ross et al., 2021).”
Beck, M. M., Heyl, M., Mejer, L., Vinding, M. C., Christiansen, L., Tomasevic, L., & Siebner, H. R. (2024) · Human Brain Mapping · doi:10.1002/hbm.70048 · Cited by 33
Li, S., Jin, J., Wang, X., Qi, H., Liu, Z., & Yin, T. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00170 · Cited by 33
“TMS-evoked electrical artifacts were reported as the main source of interference in previous rTMS studies (Veniero et al., 2009; Rogasch et al., 2014).”
Premoli, I., Costantini, A. A., Rivolta, D., Biondi, A., & Richardson, M. P. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00585 · Cited by 33
“org/tutorial/ tms-eeg), was applied to remove TMS-related artifacts (i.e., cranial muscle response, recharging of capacitors, and related exponential decay artifacts; Korhonen et al., 2011; Rogasch et al., 2014; Herring et al., 2015) as well as further muscle and ocular activity.”
BackgroundMethodInfluentialGray, W. A., Palmer, J. A., Wolf, S. L., & Borich, M. R. (2017) · Neurorehabilitation and neural repair · doi:10.1177/1545968317712470 · Cited by 32
“During TMS, the coil click generates an auditory-evoked potential (AEP) that is present predominately over central electrodes (including Cz) and can influence TEP components at N100 and P180.(38,53) Participants wore ear plugs to minimize the AEP, however, earplugs are insufficient to fully mask the AEP.”
Background
Metadata
- Authors
- Rogasch, N. C., Thomson, R. H., Farzan, F., Fitzgibbon, B. M., Bailey, N. W., Hernandez-Pavon, J. C., Daskalakis, Z. J., & Fitzgerald, P. B.
- Affiliations
- The Alfred Hospital (AU)
- Centre for Addiction and Mental Health (CA)
- Aalto University (FI)
- Corresponding author
- Rogasch, Nigel C.
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2014-11
- Volume
- 101
- Pages
- 425-439
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1969040087
- Cited by
- 309
- References
- 77
- Citations by year
- 2026: 34 · 2025: 28 · 2024: 25 · 2023: 33 · 2022: 36 · 2021: 34 · 2020: 18 · 2019: 26 · 2018: 26 · 2017: 22 · 2016: 19 · 2015: 7 · 2014: 1
- FWCI
- 7.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- Pfizer
- BrainsWay
- National Health and Medical Research Council
- National Medical Research Council
- Topics
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
- Physical Sciences › Computer Science › Signal Processing › Blind Source Separation Techniques
- Keywords
- TMS-EEG, artifact removal, independent component analysis, TMS-evoked potentials, dorsolateral prefrontal cortex, motor cortex, auditory evoked potentials, FastICA, EEG signal processing
- MeSH terms
- Adult, Data Interpretation, Statistical, Electroencephalography, Evoked Potentials, Female, Humans, Male, Motor Cortex, Artifacts, Prefrontal Cortex, Transcranial Magnetic Stimulation, Young Adult
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