Lifting the veil on the dynamics of neuronal activities evoked by transcranial magnetic stimulation

  1. Bingshuo Li
  2. Juha P Virtanen
  3. Axel Oeltermann
  4. Cornelius Schwarz
  5. Martin A Giese
  6. Ulf Ziemann
  7. Alia Benali  Is a corresponding author
  1. University of Tübingen, Germany
  2. Max Planck Institute for Biological Cybernetics, Germany

Abstract

Transcranial magnetic stimulation (TMS) is a widely used non-invasive tool to study and modulate human brain functions. However, TMS-evoked activity of individual neurons has remained largely inaccessible due to the large TMS-induced electromagnetic fields. Here we present a general method providing direct in vivo electrophysiological access to TMS-evoked neuronal activity 0.8-1 ms after TMS onset. We translated human single-pulse TMS to rodents and unveiled time-grained evoked activities of motor cortex layer V neurons that show high-frequency spiking within the first 6 ms depending on TMS-induced current orientation and a multiphasic spike-rhythm alternating between excitation and inhibition in the 6-300 ms epoch, all of which can be linked to various human TMS responses recorded at the level of spinal cord and muscles. The advance here facilitates a new level of insight into the TMS-brain interaction that is vital for developing this non-invasive tool to purposefully explore and effectively treat the human brain.

Article and author information

Author details

  1. Bingshuo Li

    Systems Neurophysiology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9024-8354
  2. Juha P Virtanen

    Systems Neurophysiology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Axel Oeltermann

    Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Cornelius Schwarz

    Systems Neurophysiology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4725-473X
  5. Martin A Giese

    Section on Computational Sensomotorics, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Ulf Ziemann

    Department of Neurology and Stroke, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Alia Benali

    Systems Neurophysiology, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    For correspondence
    alia.benali@uni-tuebingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6047-3713

Funding

Hertie Institute for Clinical Brain Research

  • Cornelius Schwarz
  • Martin A Giese
  • Ulf Ziemann

Centre for Integrative Neuroscience, University of Tübingen

  • Cornelius Schwarz
  • Martin A Giese
  • Ulf Ziemann

Max Planck Institute for Biological Cybernetics

  • Bingshuo Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental procedures involving animals were approved by the Tübingen Regional Council (license number: N1/16) and performed in accordance with the German Animal Welfare Act.

Reviewing Editor

  1. Alexander Rotenberg

Version history

  1. Received: July 19, 2017
  2. Accepted: November 17, 2017
  3. Accepted Manuscript published: November 22, 2017 (version 1)
  4. Accepted Manuscript updated: November 29, 2017 (version 2)
  5. Version of Record published: December 8, 2017 (version 3)

Copyright

© 2017, Li et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Bingshuo Li
  2. Juha P Virtanen
  3. Axel Oeltermann
  4. Cornelius Schwarz
  5. Martin A Giese
  6. Ulf Ziemann
  7. Alia Benali
(2017)
Lifting the veil on the dynamics of neuronal activities evoked by transcranial magnetic stimulation
eLife 6:e30552.
https://doi.org/10.7554/eLife.30552

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