Spatiotemporal organization of human sensorimotor beta burst activity

  1. Catharina Zich  Is a corresponding author
  2. Andrew J Quinn
  3. James J Bonaiuto
  4. George O'Neill
  5. Lydia C Mardell
  6. Nick S Ward
  7. Sven Bestmann
  1. University College London, United Kingdom
  2. University of Oxford, United Kingdom
  3. Institut des Sciences Cognitives Marc Jeannerod, France

Abstract

Beta oscillations in human sensorimotor cortex are hallmark signatures of healthy and pathological movement. In single trials, beta oscillations include bursts of intermittent, transient periods of high-power activity. These burst events have been linked to a range of sensory and motor processes, but their precise spatial, spectral, and temporal structure remains unclear. Specifically, a role for beta burst activity in information coding and communication suggests spatiotemporal patterns, or travelling wave activity, along specific anatomical gradients. We here show in human magnetoencephalography recordings that burst activity in sensorimotor cortex occurs in planar spatiotemporal wave-like patterns that dominate along two axes either parallel or perpendicular to the central sulcus. Moreover, we find that the two propagation directions are characterised by distinct anatomical and physiological features. Finally, our results suggest that sensorimotor beta bursts occurring before and after a movement can be distinguished by their anatomical, spectral and spatiotemporal characteristics, indicating distinct functional roles.

Data availability

Data are available via the Open Science Framework (OSF) at https://osf. io/eu6nx. Data are also archived at the Open MEG Archive (OMEGA; Nisoetal.,2016) and may be accessed via http://dx .doi.org/10.23686/ 0015896 (Niso et al.,2018) after registration at https:// www.mcgill.ca/bic/resources/omega.

Article and author information

Author details

  1. Catharina Zich

    Department of Clinical and Movement Neuroscience, University College London, London, United Kingdom
    For correspondence
    catharina.zich@ndcn.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0705-9297
  2. Andrew J Quinn

    Department of Psychiatry, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2267-9897
  3. James J Bonaiuto

    Institut des Sciences Cognitives Marc Jeannerod, Bron, France
    Competing interests
    The authors declare that no competing interests exist.
  4. George O'Neill

    Department of Imaging Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Lydia C Mardell

    Department of Clinical and Movement Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3180-3239
  6. Nick S Ward

    Department of Clinical and Movement Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Sven Bestmann

    epartment for Clinical and Movement Neuroscience, Institute of Neurology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6867-9545

Funding

Brain Research UK (201718-13)

  • Catharina Zich

Brain Research UK (201617-03)

  • Catharina Zich

Wellcome Trust (098369/Z/12/Z)

  • Andrew J Quinn

Engineering and Physical Sciences Research Council (EP/T001046/1)

  • George O'Neill

Medical Research Council (MR/N013867/1)

  • Lydia C Mardell

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

Reviewing Editor

  1. Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany

Ethics

Human subjects: The study protocol was in full accordance with the Declaration of Helsinki, and all participants gave written informed consent after being fully informed about the purpose of the study. The study protocol, participant information, and form of consent, were approved by the UCL Research Ethics Committee (reference number 5833/001).

Version history

  1. Received: May 11, 2022
  2. Preprint posted: May 20, 2022 (view preprint)
  3. Accepted: March 23, 2023
  4. Accepted Manuscript published: March 24, 2023 (version 1)
  5. Version of Record published: April 17, 2023 (version 2)

Copyright

© 2023, Zich 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. Catharina Zich
  2. Andrew J Quinn
  3. James J Bonaiuto
  4. George O'Neill
  5. Lydia C Mardell
  6. Nick S Ward
  7. Sven Bestmann
(2023)
Spatiotemporal organization of human sensorimotor beta burst activity
eLife 12:e80160.
https://doi.org/10.7554/eLife.80160

Share this article

https://doi.org/10.7554/eLife.80160

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