Sigma oscillations protect or reinstate motor memory depending on their temporal coordination with slow waves

  1. Judith Nicolas  Is a corresponding author
  2. Bradley R King
  3. David Levesque
  4. Latifa Lazzouni
  5. Emily BJ Coffey
  6. Stephan Swinnen
  7. Julien Doyon
  8. Julie Carrier
  9. Genevieve Albouy  Is a corresponding author
  1. KU Leuven, Belgium
  2. Unversity of Utah, United States
  3. Universite de Montreal, Canada
  4. McGill University, Canada
  5. Concordia University, Canada
  6. Université de Montréal, Canada

Abstract

Targeted memory reactivation (TMR) during post-learning sleep is known to enhance motor memory consolidation but the underlying neurophysiological processes remain unclear. Here, we confirm the beneficial effect of auditory TMR on motor performance. At the neural level, TMR enhanced slow wave (SW) characteristics. Additionally, greater TMR-related phase-amplitude coupling between slow (0.5-2 Hz) and sigma (12-16 Hz) oscillations after the SW peak was related to higher TMR effect on performance. Importantly, sounds that were not associated to learning strengthened SW-sigma coupling at the SW trough. Moreover, the increase in sigma power nested in the trough of the potential evoked by the unassociated sounds was related to the TMR benefit. Altogether, our data suggest that, depending on their precise temporal coordination during post learning sleep, slow and sigma oscillations play a crucial role in either memory reinstatement or protection against irrelevant information; two processes that critically contribute to motor memory consolidation.

Data availability

All data can be found at https://zenodo.org/record/6642860#.YqoI46hBzD5. The source code is available at https://github.com/judithnicolas/MotorMemory_OpenLoop_TMR

The following data sets were generated

Article and author information

Author details

  1. Judith Nicolas

    Department of Movement Sciences, KU Leuven, Leuven, Belgium
    For correspondence
    nicolasjdh@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7142-1449
  2. Bradley R King

    Department of Health and Kinesiology, Unversity of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3010-8755
  3. David Levesque

    Center for Advanced Research in Sleep Medicine, Universite de Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Latifa Lazzouni

    Department of Neurology and Neurosurgery, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Emily BJ Coffey

    Department of Psychology, Concordia University, Quebec, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Stephan Swinnen

    Department of Movement Sciences, KU Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7173-435X
  7. Julien Doyon

    Department of Neurology and Neurosurgery, McGill University, Montréal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3788-4271
  8. Julie Carrier

    Centre for Advanced Research in Sleep Medicine, Université de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5311-2370
  9. Genevieve Albouy

    Department of Movement Sciences, KU Leuven, Leuven, Belgium
    For correspondence
    genevieve.albouy@kuleuven.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5437-023X

Funding

Fonds Wetenschappelijk Onderzoek (G0D7918N)

  • Judith Nicolas
  • Bradley R King
  • David Levesque
  • Latifa Lazzouni
  • Stephan Swinnen
  • Julien Doyon
  • Julie Carrier
  • Genevieve Albouy

Fonds de Recherche du Québec - Santé (RRQNT-2018-264146)

  • Judith Nicolas
  • Bradley R King
  • David Levesque
  • Latifa Lazzouni
  • Stephan Swinnen
  • Julien Doyon
  • Julie Carrier
  • Genevieve Albouy

Fonds Wetenschappelijk Onderzoek (G0B1419N)

  • Genevieve Albouy

Fonds Wetenschappelijk Onderzoek (G099516N)

  • Genevieve Albouy

Fonds Wetenschappelijk Onderzoek (1524218N)

  • Genevieve Albouy

Fonds Wetenschappelijk Onderzoek (30446199)

  • Stephan Swinnen
  • Genevieve Albouy

HORIZON EUROPE Marie Sklodowska-Curie Actions (887955)

  • Bradley R King

HORIZON EUROPE Marie Sklodowska-Curie Actions (703490)

  • Judith Nicolas

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

Reviewing Editor

  1. Randolph F Helfrich, University of Tübingen, Germany

Ethics

Human subjects: Young healthy volunteers were recruited by local advertisements to participate in the present study. Participants gave written informed consent before participating in this research protocol, approved by the local Ethics Committee (B322201525025) and conducted according to the declaration of Helsinki (2013). The participants received a monetary compensation for their time and effort.

Version history

  1. Preprint posted: September 3, 2021 (view preprint)
  2. Received: September 15, 2021
  3. Accepted: June 7, 2022
  4. Accepted Manuscript published: June 21, 2022 (version 1)
  5. Version of Record published: July 6, 2022 (version 2)

Copyright

© 2022, Nicolas 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. Judith Nicolas
  2. Bradley R King
  3. David Levesque
  4. Latifa Lazzouni
  5. Emily BJ Coffey
  6. Stephan Swinnen
  7. Julien Doyon
  8. Julie Carrier
  9. Genevieve Albouy
(2022)
Sigma oscillations protect or reinstate motor memory depending on their temporal coordination with slow waves
eLife 11:e73930.
https://doi.org/10.7554/eLife.73930

Share this article

https://doi.org/10.7554/eLife.73930

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