Right inferior frontal gyrus implements motor inhibitory control via beta-band oscillations in humans

  1. Michael Schaum  Is a corresponding author
  2. Edoardo Pinzuti
  3. Alexandra Sebastian
  4. Klaus Lieb
  5. Pascal Fries
  6. Arian Mobascher
  7. Patrick Jung
  8. Michael Wibral
  9. Oliver Tüscher
  1. Leibniz Institute for Resilience Research, Germany
  2. University Medical Center of the Johannes Gutenberg University, Germany
  3. Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
  4. Georg-August University, Germany

Abstract

Motor inhibitory control implemented as response inhibition is an essential cognitive function required to dynamically adapt to rapidly changing environments. Despite of over a decade of research on the neural mechanisms of response inhibition, it remains unclear, how exactly response inhibition is initiated and implemented. Using a multimodal MEG/fMRI approach in 59 subjects our results reliably reveal that response inhibition is initiated by the right inferior frontal gyrus (rIFG) as a form of attention-independent top-down control that involves the modulation of beta-band activity. Furthermore, stopping performance was predicted by beta-band power and beta-band connectivity was directed from rIFG to pre-supplementary motor area (pre-SMA), indicating rIFG's dominance over pre-SMA. Thus, these results strongly support the hypothesis that rIFG initiates stopping, implemented by beta-band oscillations with potential to open up new ways of spatially localized oscillation-based interventions.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. All source data files are available on Dryad Digital repository (https://doi.org/10.5061/dryad.x3ffbg7gp). All custom Matlab codes used in these analyses are available at https://github.com/meglab/acSST).

The following data sets were generated

Article and author information

Author details

  1. Michael Schaum

    Systemic Mechanisms of Resilience, Leibniz Institute for Resilience Research, Mainz, Germany
    For correspondence
    Michael.Schaum@lir-mainz.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6589-4530
  2. Edoardo Pinzuti

    System mechanisms of resilience, Leibniz Institute for Resilience Research, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexandra Sebastian

    Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8381-8312
  4. Klaus Lieb

    Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Pascal Fries

    Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4270-1468
  6. Arian Mobascher

    Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Patrick Jung

    Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Wibral

    Georg-August University, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Oliver Tüscher

    Department of Psychiatry and Psychotherapy, University Medical Center of the Johannes Gutenberg University, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (SFB 1193)

  • Michael Schaum

Deutsche Forschungsgemeinschaft (SFB 1193)

  • Edoardo Pinzuti

Deutsche Forschungsgemeinschaft (SFB 1193)

  • Alexandra Sebastian

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

Reviewing Editor

  1. Simon Little, UCSF, United States

Ethics

Human subjects: All individual participants included in the study provided written informed consent before participation and consent to publish any research findings based on their provided data in anonymized form. The study was approved by the local ethics committees (Johann Wolfgang Goethe University, Frankfurt, Germany, and Medical Board of Rhineland-Palatinate, Mainz, Germany¸ IRB Protocol no. 837.128.11), and participants were financially compensated for their time.

Version history

  1. Received: July 31, 2020
  2. Accepted: March 23, 2021
  3. Accepted Manuscript published: March 23, 2021 (version 1)
  4. Version of Record published: May 4, 2021 (version 2)

Copyright

© 2021, Schaum 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. Michael Schaum
  2. Edoardo Pinzuti
  3. Alexandra Sebastian
  4. Klaus Lieb
  5. Pascal Fries
  6. Arian Mobascher
  7. Patrick Jung
  8. Michael Wibral
  9. Oliver Tüscher
(2021)
Right inferior frontal gyrus implements motor inhibitory control via beta-band oscillations in humans
eLife 10:e61679.
https://doi.org/10.7554/eLife.61679

Share this article

https://doi.org/10.7554/eLife.61679

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