TMS combined with EEG: Recommendations and open issues for data collection and analysis

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  • Julio C. Hernandez-Pavon
  • Domenica Veniero
  • Til Ole Bergmann
  • Paolo Belardinelli
  • Marta Bortoletto
  • Silvia Casarotto
  • Elias P. Casula
  • Faranak Farzan
  • Matteo Fecchio
  • Petro Julkunen
  • Elisa Kallioniemi
  • Pantelis Lioumis
  • Johanna Metsomaa
  • Carlo Miniussi
  • Tuomas P. Mutanen
  • Lorenzo Rocchi
  • Nigel C. Rogasch
  • Mouhsin M. Shafi
  • Gregor Thut
  • Christoph Zrenner
  • Ulf Ziemann
  • Risto J. Ilmoniemi
Transcranial magnetic stimulation (TMS) evokes neuronal activity in the targeted cortex and connected brain regions. The evoked brain response can be measured with electroencephalography (EEG). TMS combined with simultaneous EEG (TMS−EEG) is widely used for studying cortical reactivity and connectivity at high spatiotemporal resolution. Methodologically, the combination of TMS with EEG is challenging, and there are many open questions in the field. Different TMS−EEG equipment and approaches for data collection and analysis are used. The lack of standardization may affect reproducibility and limit the comparability of results produced in different research laboratories. In addition, there is controversy about the extent to which auditory and somatosensory inputs contribute to transcranially evoked EEG. This review provides a guide for researchers who wish to use TMS−EEG to study the reactivity of the human cortex. A worldwide panel of experts working on TMS−EEG covered all aspects that should be considered in TMS−EEG experiments, providing methodological recommendations (when possible) for effective TMS−EEG recordings and analysis. The panel identified and discussed the challenges of the technique, particularly regarding recording procedures, artifact correction, analysis, and interpretation of the transcranial evoked potentials (TEPs). Therefore, this work offers an extensive overview of TMS−EEG methodology and thus may promote standardization of experimental and computational procedures across groups.
OriginalsprogEngelsk
TidsskriftBrain Stimulation
Vol/bind16
Udgave nummer2
Sider (fra-til)567-593
Antal sider27
ISSN1935-861X
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
JCHP and RJI want to dedicate this work to the memory of Prof. Jukka Sarvas, one of the most beautiful minds and humble hearts that have existed in this world. HRS holds a 5-year professorship in precision medicine at the Faculty of Health Sciences and Medicine, University of Copenhagen which is sponsored by the Lundbeck Foundation (Grant Nr. R186-2015-2138). TPM has been supported by the Academy of Finland (Grant No. 321631 ).

Funding Information:
The Brain Electrophysiological recording and STimulation (BEST) toolbox (www.best-toolbox.org) is an open-source MATLAB toolbox with GUI [216], which enables the user to easily design, save/load, run, and online analyze multi-protocol/multi-session experiments involving a variety of brain stimulation techniques, such as TMS, TES and also transcranial ultrasound stimulation. It interfaces with many recording and stimulation devices and can online analyze and display the input signals from EMG and EEG and change TMS parameters on the fly (via the MAGIC toolbox, [246]), thereby facilitating real-time applications. Besides several modules for conducting MEP measurements of all kinds (such as motor hotspot search, threshold hunting, MEP measurements, dose-response curves, as well as paired-pulse and double-coil protocols), the BEST toolbox also supports TEP hotspot search and TEP measurements by providing online graphical feedback for re-referenced EEG signals (also lead fields for arbitrary spatial filters can be defined), incremental condition-wise time-locked TEP averages and topographical maps of selected TEP components. Future releases are planned to also provide real-time artifact rejection methods. The BEST toolbox does not provide a built-in TMS–EEG artifact correction pipeline but can interact with all MATLAB-based pipelines or toolboxes. The internal data format is based on FieldTrip.The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: PJ has received consulting fees and shares a patent with Nexstim Oyj. PL has received consulting fees from Nexstim Oyj. HRS has received honoraria as speaker from Sanofi Genzyme, Denmark, Lundbeck AS, Denmark, and Novartis, Denmark, as consultant from Sanofi Genzyme, Denmark, Lophora, Denmark, and Lundbeck AS, Denmark, and as editor-in-chief (Neuroimage Clinical) and senior editor (NeuroImage) from Elsevier Publishers, Amsterdam, The Netherlands. He has received royalties as book editor from Springer Publishers, Stuttgart, Germany and from Gyldendal Publishers, Copenhagen, Denmark. TPM has successfully applied for funding for a collaborative research project (project not started at the time of the submission) with Bittium Biosignals Oy (Kuopio, Finland). SC is advisor and share-holder of Intrinsic Power, a spinf-off of the University of Milan.JCHP and RJI want to dedicate this work to the memory of Prof. Jukka Sarvas, one of the most beautiful minds and humble hearts that have existed in this world. HRS holds a 5-year professorship in precision medicine at the Faculty of Health Sciences and Medicine, University of Copenhagen which is sponsored by the Lundbeck Foundation (Grant Nr. R186-2015-2138). TPM has been supported by the Academy of Finland (Grant No. 321631).

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© 2023 The Authors

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