1. Neuroscience
Download icon

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
Research Article
  • Cited 0
  • Views 368
  • Annotations
Cite this article as: eLife 2021;10:e61679 doi: 10.7554/eLife.61679

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.

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.

Reviewing Editor

  1. Simon Little, UCSF, United States

Publication history

  1. Received: July 31, 2020
  2. Accepted: March 23, 2021
  3. Accepted Manuscript published: March 23, 2021 (version 1)

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.

Metrics

  • 368
    Page views
  • 96
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Piotr Michaluk et al.
    Research Article

    Glutamate uptake by astroglial transporters confines excitatory transmission to the synaptic cleft. The efficiency of this mechanism depends on the transporter dynamics in the astrocyte membrane, which remains poorly understood. Here, we visualise the main glial glutamate transporter GLT1 by generating its pH-sensitive fluorescent analogue, GLT1-SEP. FRAP-based imaging shows that 70-75% of GLT1-SEP dwell on the surface of rat brain astroglia, recycling with a lifetime of ~22 s. Genetic deletion of the C-terminus accelerates GLT1-SEP membrane turnover while disrupting its surface pattern, as revealed by single-molecule localisation microscopy. Excitatory activity boosts surface mobility of GLT1-SEP, involving its C-terminus, metabotropic glutamate receptors, intracellular Ca2+ and calcineurin-phosphatase activity, but not the broad-range kinase activity. The results suggest that membrane turnover, rather than lateral diffusion, is the main 'redeployment' route for the immobile fraction (20-30%) of surface-expressed GLT1. This finding reveals an important mechanism helping to control extrasynaptic escape of glutamate.

    1. Neuroscience
    Eric Torsten Reifenstein et al.
    Research Article

    Remembering the temporal order of a sequence of events is a task easily performed by humans in everyday life, but the underlying neuronal mechanisms are unclear. This problem is particularly intriguing as human behavior often proceeds on a time scale of seconds, which is in stark contrast to the much faster millisecond time-scale of neuronal processing in our brains. One long-held hypothesis in sequence learning suggests that a particular temporal fine-structure of neuronal activity - termed 'phase precession' - enables the compression of slow behavioral sequences down to the fast time scale of the induction of synaptic plasticity. Using mathematical analysis and computer simulations, we find that - for short enough synaptic learning windows - phase precession can improve temporal-order learning tremendously and that the asymmetric part of the synaptic learning window is essential for temporal-order learning. To test these predictions, we suggest experiments that selectively alter phase precession or the learning window and evaluate memory of temporal order.