Beta oscillations and waves in motor cortex can be accounted for by the interplay of spatially-structured connectivity and fluctuating inputs

  1. Ling Kang
  2. Jonas Ranft
  3. Vincent Hakim  Is a corresponding author
  1. École Normale Supérieure, CNRS, INSERM, France

Abstract

The beta rhythm (13-30 Hz) is a prominent brain rhythm. Recordings in primates during instructed-delay reaching tasks have shown that different types of traveling waves of oscillatory activity are associated with episodes of beta oscillations in motor cortex during movement preparation. We propose here a simple model of motor cortex based on local excitatory-inhibitory neuronal populations coupled by long-range excitation, where additionally inputs to the motor cortex from other neural structures are represented by stochastic inputs on the different model populations. We show that the model accurately reproduces the statistics of recording data when these external inputs are correlated on a short time scale (25 ms) and have two different components, one that targets the motor cortex locally and another one that targets it in a global and synchronized way. The model reproduces the distribution of beta burst durations, the proportion of the different observed wave types, and wave speeds, which we show not to be linked to axonal propagation speed. When the long-range connectivity or the local input targets are anisotropic, traveling waves are found to preferentially propagate along the axis where connectivity decays the fastest. Different from previously proposed mechanistic explanations, the model suggests that traveling waves in motor cortex are the reflection of the dephasing by external inputs, putatively of thalamic origin, of an oscillatory activity that would otherwise be spatially synchronized by recurrent connectivity.

Data availability

The source codes for this manuscript are available on GitHub at https://github.com/LKANG777/Beta-Oscillation.

The following previously published data sets were used

Article and author information

Author details

  1. Ling Kang

    Laboratoire de Physique Statistique, École Normale Supérieure, CNRS, INSERM, Prais, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6532-3773
  2. Jonas Ranft

    Institut de Biologie de l'Ecole Normale Supérieure, École Normale Supérieure, CNRS, INSERM, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7843-7443
  3. Vincent Hakim

    Laboratoire de Physique Statistique, École Normale Supérieure, CNRS, INSERM, Paris, France
    For correspondence
    vincent.hakim@ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7505-8192

Funding

China Scholarship Council (Graduate Student Fellowship)

  • Ling Kang

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

Reviewing Editor

  1. Nicole C Swann, University of Oregon, United States

Version history

  1. Preprint posted: June 17, 2022 (view preprint)
  2. Received: June 27, 2022
  3. Accepted: March 2, 2023
  4. Accepted Manuscript published: March 14, 2023 (version 1)
  5. Version of Record published: April 18, 2023 (version 2)

Copyright

© 2023, Kang 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. Ling Kang
  2. Jonas Ranft
  3. Vincent Hakim
(2023)
Beta oscillations and waves in motor cortex can be accounted for by the interplay of spatially-structured connectivity and fluctuating inputs
eLife 12:e81446.
https://doi.org/10.7554/eLife.81446

Share this article

https://doi.org/10.7554/eLife.81446

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