Reproducibility in TMS–EEG studies: A call for data sharing, standard procedures and effective experimental control

Abstract

A recent study by Conde, Tomasevic et al. (2019) [[1]Conde V. Tomasevic L. Akopian I. Stanek K. Saturnino G.B. Thielscher A. et al.The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies.Neuroimage. 2019; 185: 300-312https://doi.org/10.1016/j.neuroimage.2018.10.052Crossref PubMed Scopus (139) Google Scholar] puts a spotlight on the subtleties of experimental design and analysis of studies involving TMS-evoked EEG potentials (TEPs), specifically focusing on the challenge of disentangling genuine cortical responses to TMS from those resulting from concomitant sensory activation. This is a relevant topic that the TMS–EEG community has previously identified [[2]Ilmoniemi R.J. Kičić D. Methodology for combined TMS and EEG.Brain Topogr. 2010; 22: 233-248https://doi.org/10.1007/s10548-009-0123-4Crossref PubMed Scopus (256) Google Scholar] and addressed with different strategies [3Gordon P.C. Desideri D. Belardinelli P. Zrenner C. Ziemann U. Comparison of cortical EEG responses to realistic sham versus real TMS of human motor cortex.Brain Stimul. 2018; 11: 1322-1330https://doi.org/10.1016/j.brs.2018.08.003Abstract Full Text Full Text PDF PubMed Scopus (52) Google Scholar, 4Gosseries O. Sarasso S. Casarotto S. Boly M. Schnakers C. Napolitani M. et al.On the cerebral origin of EEG responses to TMS: insights from severe cortical lesions.Brain Stimul. 2015; 8: 142-149https://doi.org/10.1016/j.brs.2014.10.008Abstract Full Text Full Text PDF PubMed Scopus (57) Google Scholar, 5Herring J.D. Thut G. Jensen O. Bergmann T.O. Attention modulates TMS-locked alpha oscillations in the visual cortex.J Neurosci. 2015; 35: 14435-14447https://doi.org/10.1523/JNEUROSCI.1833-15.2015Crossref PubMed Scopus (116) Google Scholar, 6Nikouline V. Ruohonen J. Ilmoniemi R.J. The role of the coil click in TMS assessed with simultaneous EEG.Clin Neurophysiol. 1999; 110: 1325-1328https://doi.org/10.1016/S1388-2457(99)00070-XCrossref PubMed Scopus (195) Google Scholar]. Based on the similarity of the evoked EEG responses they obtained in real TMS at different sites and in sham conditions (auditory and somatosensory scalp stimulation), the authors of [[1]Conde V. Tomasevic L. Akopian I. Stanek K. Saturnino G.B. Thielscher A. et al.The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies.Neuroimage. 2019; 185: 300-312https://doi.org/10.1016/j.neuroimage.2018.10.052Crossref PubMed Scopus (139) Google Scholar] inferred that TEPs can be significantly contaminated by the effects of concurrent, non-transcranial stimulation. We acknowledge this is a valuable reminder to the TMS-EEG community; however, we contend that another fundamental implication of the work by Conde, Tomasevic and colleagues [[1]Conde V. Tomasevic L. Akopian I. Stanek K. Saturnino G.B. Thielscher A. et al.The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies.Neuroimage. 2019; 185: 300-312https://doi.org/10.1016/j.neuroimage.2018.10.052Crossref PubMed Scopus (139) Google Scholar] - only incidentally mentioned at the end of their discussion – is that the evoked responses they obtain from both real TMS and sham conditions are substantially different from the TEPs reported in many of the previous studies (see, for example [7Bonato C. Miniussi C. Rossini P.M. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study.Clin Neurophysiol. 2006; 117: 1699-1707https://doi.org/10.1016/j.clinph.2006.05.006Crossref PubMed Scopus (228) Google Scholar, 8Casarotto S. Romero Lauro L.J. Bellina V. Casali A.G. Rosanova M. Pigorini A. et al.EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time.PLoS One. 2010; 5e10281https://doi.org/10.1371/journal.pone.0010281Crossref PubMed Scopus (146) Google Scholar, 9Mäki H. Ilmoniemi R.J. The relationship between peripheral and early cortical activation induced by transcranial magne