Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of algorithms for correction of transcranial magnetic stimulation-induced artifacts in electroencephalograms

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Transcranial magnetic stimulation combined with electroencephalography (TMS-EEG) is widely used to study the reactivity and connectivity of brain regions for clinical or research purposes. The electromagnetic pulse of the TMS device generates at the instant of administration an artifact of large amplitude and a duration up to tens of milliseconds that overlaps with brain activity. Methods for TMS artifact correction have been developed to remove the artifact and recover the underlying, immediate response of the cerebral cortex to the magnetic stimulus. In this study, four such algorithms are evaluated. Since there is no ground truth for the masked brain activity, pilot data formed from the superposition of the isolated TMS artifact on EEG brain activity are used to evaluate the performance of the algorithms. Different scenarios of TMS-EEG experiments are considered for the evaluation: TMS at resting state, TMS inducing epileptiform discharges, and TMS administered during epileptiform discharges. We show that a proposed gap filling method is able to reproduce qualitative characteristics and, in many cases, closely resemble the hidden EEG signal. Finally, shortcomings of the TMS correction algorithms as well as the pilot data approach are discussed.

The transcranial magnetic stimulation (TMS) artifact on the electroencephalogram (EEG) and its correction

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  1. Atluri S, Frehlich M, Mei Y, et al (2016) TMSEEG: A MATLAB-based graphical user interface for processing electrophysiological signals during transcranial magnetic stimulation. Front Neural Circ 10. https://doi.org/10.3389/fncir.2016.00078

  2. Awiszus F (2003) TMS and threshold hunting. Suppl Clin Neurophysiol 56:13–23

    Article  Google Scholar 

  3. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107

    Article  CAS  Google Scholar 

  4. Bergmann TO, Molle M, Schmidt MA et al (2012) EEG-guided transcranial magnetic stimulation reveals rapid shifts in motor cortical excitability during the human sleep slow oscillation. J Neurosci 32:243–253. https://doi.org/10.1523/jneurosci.4792-11.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Casarotto S, Romero Lauro LJ, Bellina V, Casali AG, Rosanova M, Pigorini A et al (2010) EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 5(4):e10281. https://doi.org/10.1371/journal.pone.0010281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Daskalakis ZJ, Farzan F, Radhu N, Fitzgerald PB (2012) Combined transcranial magnetic stimulation and electroencephalography: Its past, present and future. Brain Res 1463:93–107. https://doi.org/10.1016/j.brainres.2012.04.045

    Article  CAS  PubMed  Google Scholar 

  7. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009

    Article  Google Scholar 

  8. Delorme A, Sejnowski T, Makeig S (2007) Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. NeuroImage 34:1443–1449. https://doi.org/10.1016/j.neuroimage.2006.11.004

    Article  PubMed  Google Scholar 

  9. Farzan F, Vernet M, Shafi MMD et al (2016) Characterizing and modulating brain circuitry through transcranial magnetic stimulation combined with electroencephalography. Front Neural Circ:10. https://doi.org/10.3389/fncir.2016.00073

  10. Friston K (2004) Introduction: experimental design and statistical parametric mapping. In: Frackowiak et al (eds) Human brain function, 2nd edn. Academic Press

  11. Hernandez-Pavon JC, Metsomaa J, Mutanen T, Stenroos M, Mäki H, Ilmoniemi RJ, Sarvas J (2012) Uncovering neural independent components from highly artifactual TMS-evoked EEG data. J Neurosci Methods 209:144–157. https://doi.org/10.1016/j.jneumeth.2012.05.029

    Article  PubMed  Google Scholar 

  12. Hyvärinen Α (1999) Fast and robust fixed-point algorithms for independent component analysis. IEEE Trans Neural Netw 10(3):626–634

    Article  Google Scholar 

  13. Hyvärinen A, Oja E (1997) A fast fixed-point algorithm for independent component analysis. Neural Comput 9(7):1483–1492

    Article  Google Scholar 

  14. Hyvärinen A, Oja E (2000) Independent component analysis: algorithms and applications. Neural Netw 13(4-5):411–430

    Article  Google Scholar 

  15. Ilmoniemi RJ, Kičić D (2010) Methodology for combined TMS and EEG. Brain Topogr 22:233–248. https://doi.org/10.1007/s10548-009-0123-4

    Article  PubMed  Google Scholar 

  16. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Näätänen R, Katila T (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8(16):3537–3540

    Article  CAS  Google Scholar 

  17. Iramina K, Maeno T, Nonaka Y, Ueno S (2003) Measurement of evoked electroencephalography induced by transcranial magnetic stimulation. J Appl Phys 93:6718–6720. https://doi.org/10.1063/1.1558635

    Article  CAS  Google Scholar 

  18. Islam MK, Rastegarnia A, Yang Z (2016) Methods for artifact detection and removal from scalp EEG: a review. Neurophysiol Clin/Clin Neurophysiol 46:287–305. https://doi.org/10.1016/j.neucli.2016.07.002

    Article  Google Scholar 

  19. Julkunen P, Pääkkönen A, Hukkanen T, Könönen M, Tiihonen P, Vanhatalo S, Karhu J (2008) Efficient reduction of stimulus artefact in TMS–EEG by epithelial short-circuiting by mini-punctures. Clin Neurophysiol 119:475–481. https://doi.org/10.1016/j.clinph.2007.09.139

    Article  CAS  PubMed  Google Scholar 

  20. Kammer T, Baumann LW (2010) Phosphene thresholds evoked with single and double TMS pulses. Clin Neurophysiol 121:376–379. https://doi.org/10.1016/j.clinph.2009.12.002

    Article  PubMed  Google Scholar 

  21. Kantz H, Schreiber T (2003) Nonlinear time series analysis. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511755798

    Book  Google Scholar 

  22. Kerwin LJ, Keller CJ, Wu W, Narayan M, Etkin A (2018) Test-retest reliability of transcranial magnetic stimulation EEG evoked potentials. Brain Stimul 11(3):536–544. https://doi.org/10.1016/j.brs.2017.12.010

    Article  PubMed  Google Scholar 

  23. Kimiskidis VK, Kugiumtzis D, Papagiannopoulos S, Vlaikidis N (2013) Transcranial magnetic stimulation (TMS) modulates epileptiform discharges in patients with frontal lobe epilepsy: a preliminary EEG-TMS study. Int J Neural Syst 23:1250035. https://doi.org/10.1142/s0129065712500359

    Article  PubMed  Google Scholar 

  24. Kimiskidis VK, Tsimpiris A, Ryvlin P, Kalviainen R, Koutroumanidis M, Valentin A, Laskaris N, Kugiumtzis D (2017) TMS combined with EEG in genetic generalized epilepsy: a phase II diagnostic accuracy study. Clin Neurophysiol 128:367–381. https://doi.org/10.1016/j.clinph.2016.11.013

    Article  PubMed  Google Scholar 

  25. Komssi S, Kähkönen S (2006) The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 52:183–192. https://doi.org/10.1016/j.brainresrev.2006.01.008

    Article  PubMed  Google Scholar 

  26. Komssi S, Kähkönen S, Ilmoniemi RJ (2004) The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 21:154–164. https://doi.org/10.1002/hbm.10159

    Article  PubMed  Google Scholar 

  27. Korhonen RJ, Hernandez-Pavon JC, Metsomaa J, Mäki H, Ilmoniemi RJ, Sarvas J (2011) Removal of large muscle artifacts from transcranial magnetic stimulation-evoked EEG by independent component analysis. Med Biol Eng Comput 49:397–407. https://doi.org/10.1007/s11517-011-0748-9

    Article  PubMed  Google Scholar 

  28. Kugiumtzis D, Kimiskidis VK (2015) Direct causal networks for the study of transcranial magnetic stimulation effects on focal epileptiform discharges. Int J Neural Syst 25:1550006. https://doi.org/10.1142/s0129065715500069

    Article  PubMed  Google Scholar 

  29. Kugiumtzis D, Koutlis C, Tsimpiris A, Kimiskidis VK (2017) Dynamics of epileptiform discharges induced by transcranial magnetic stimulation in genetic generalized epilepsy. Int J Neural Syst 27:1750037. https://doi.org/10.1142/s012906571750037x

    Article  PubMed  Google Scholar 

  30. Lefaucheur J-P, André-Obadia N, Antal A, Ayache SS, Baeken C, Benninger DH, Cantello RM, Cincotta M, de Carvalho M, de Ridder D, Devanne H, di Lazzaro V, Filipović SR, Hummel FC, Jääskeläinen SK, Kimiskidis VK, Koch G, Langguth B, Nyffeler T, Oliviero A, Padberg F, Poulet E, Rossi S, Rossini PM, Rothwell JC, Schönfeldt-Lecuona C, Siebner HR, Slotema CW, Stagg CJ, Valls-Sole J, Ziemann U, Paulus W, Garcia-Larrea L (2014) Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS). Clin Neurophysiol 125:2150–2206. https://doi.org/10.1016/j.clinph.2014.05.021

    Article  PubMed  Google Scholar 

  31. Lioumis P, Kičić D, Savolainen P, Mäkelä J, Kähkönen S (2008) Reproducibility of TMS-evoked EEG responses. Hum Brain Mapp 30:1387–1396. https://doi.org/10.1002/hbm.20608

    Article  Google Scholar 

  32. Litvak V, Komssi S, Scherg M, Hoechstetter K, Classen J, Zaaroor M, Pratt H, Kahkonen S (2007) Artifact correction and source analysis of early electroencephalographic responses evoked by transcranial magnetic stimulation over primary motor cortex. NeuroImage 37:56–70. https://doi.org/10.1016/j.neuroimage.2007.05.015

    Article  PubMed  Google Scholar 

  33. Lu M, Ueno S (2017) Comparison of the induced fields using different coil configurations during deep transcranial magnetic stimulation. PLoS One 12:e0178422. https://doi.org/10.1371/journal.pone.0178422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mäki H, Ilmoniemi RJ (2011) Projecting out muscle artifacts from TMS-evoked EEG. NeuroImage 54:2706–2710. https://doi.org/10.1016/j.neuroimage.2010.11.041

    Article  PubMed  Google Scholar 

  35. Mutanen T, Mäki H, Ilmoniemi RJ (2013) The Effect of Stimulus Parameters on TMS–EEG Muscle Artifacts. Brain Stimul 6:371–376. https://doi.org/10.1016/j.brs.2012.07.005

    Article  PubMed  Google Scholar 

  36. Napolitani M, Bodart O, Canali P, Seregni F, Casali A, Laureys S, Rosanova M, Massimini M, Gosseries O (2014) Transcranial magnetic stimulation combined with high-density EEG in altered states of consciousness. Brain Inj 28(9):1180–1189. https://doi.org/10.3109/02699052.2014.920524

    Article  PubMed  Google Scholar 

  37. Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:1–9. https://doi.org/10.1155/2011/156869

    Article  Google Scholar 

  38. Paparella F (2005) Filling gaps in chaotic time series. Phys Lett A 346:47–53. https://doi.org/10.1016/j.physleta.2005.07.076

    Article  CAS  Google Scholar 

  39. Premoli I, Rivolta D, Espenhahn S, Castellanos N, Belardinelli P, Ziemann U, Müller-Dahlhaus F (2014) Characterization of GABAB-receptor mediated neurotransmission in the human cortex by paired-pulse TMS–EEG. NeuroImage 103:152–162. https://doi.org/10.1016/j.neuroimage.2014.09.028

    Article  CAS  PubMed  Google Scholar 

  40. Rogasch NC, Thomson RH, Daskalakis ZJ, Fitzgerald PB (2013) Short-latency artifacts associated with concurrent TMS–EEG. Brain Stimul 6:868–876. https://doi.org/10.1016/j.brs.2013.04.004

    Article  PubMed  Google Scholar 

  41. Rogasch NC, Thomson RH, Farzan F et al (2014) Removing artefacts from TMS-EEG recordings using independent component analysis: importance for assessing prefrontal and motor cortex network properties. NeuroImage 101:425–439. https://doi.org/10.1016/j.neuroimage.2014.07.037

    Article  PubMed  Google Scholar 

  42. Rogasch NC, Sullivan C, Thomson RH, Rose NS, Bailey NW, Fitzgerald PB, Farzan F, Hernandez-Pavon JC (2017) Analysing concurrent transcranial magnetic stimulation and electroencephalographic data: A review and introduction to the open-source TESA software. Neuroimage 147:934–951

    Article  Google Scholar 

  43. Romei V, Murray MM, Merabet LB, Thut G (2007) Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: Implications for Multisensory Interactions. J Neurosci 27:11465–11472. https://doi.org/10.1523/jneurosci.2827-07.2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shlens J (2014) A tutorial on principal component analysis. arXiv preprint arXiv:1404.1100

  45. Ter Braack EM, De Jonge B, Van Putten MJAM (2013) Reduction of TMS induced artifacts in EEG using principal component analysis. IEEE Trans Neural Syst Rehabil Eng 21(3):376–382

    Article  Google Scholar 

  46. Thut G, Veniero D, Romei V, Miniussi C, Schyns P, Gross J (2011) Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 21:1176–1185. https://doi.org/10.1016/j.cub.2011.05.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tranulis C, Guéguen B, Pham-Scottez A, Vacheron MN, Cabelguen G, Costantini A, Valero G, Galinovski A (2006) Motor threshold in transcranial magnetic stimulation: comparison of three estimation methods. Neurophysiol Clin/Clin Neurophysiol 36:1–7. https://doi.org/10.1016/j.neucli.2006.01.005

    Article  CAS  Google Scholar 

  48. Veniero D, Bortoletto M, Miniussi C (2009) TMS-EEG co-registration: On TMS-induced artifact. Clin Neurophysiol 120:1392–1399. https://doi.org/10.1016/j.clinph.2009.04.023

    Article  PubMed  Google Scholar 

  49. Virtanen J, Ruohonen J, Näätänen R, Ilmoniemi RJ (1999) Instrumentation for the measurement of the electric brain responses to TMS. Med Biol Eng Comput 37(3):322–326. https://doi.org/10.1007/BF02513307

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the patient for participating in the study.

Author information

Authors and Affiliations

  1. Computation and Neural Systems Program, Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125, USA

    Pantelis Vafidis

  2. Laboratory of Clinical Neurophysiology, Medical School, Aristotle University of Thessaloniki, University Campus, 54124, Thessaloniki, Greece

    Vasilios K. Kimiskidis

  3. Department of Electrical and Computer Engineering, Faculty of Engineering, Aristotle University of Thessaloniki, University Campus, 54124, Thessaloniki, Greece

    Dimitris Kugiumtzis

Authors
  1. Pantelis Vafidis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vasilios K. Kimiskidis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dimitris Kugiumtzis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dimitris Kugiumtzis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vafidis, P., Kimiskidis, V.K. & Kugiumtzis, D. Evaluation of algorithms for correction of transcranial magnetic stimulation-induced artifacts in electroencephalograms. Med Biol Eng Comput 57, 2599–2615 (2019). https://doi.org/10.1007/s11517-019-02053-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-019-02053-3

Keywords

Search

Navigation