Increasing human motor skill acquisition by driving theta-gamma coupling

  1. Haya Akkad  Is a corresponding author
  2. Joshua Dupont-Hadwen
  3. Edward Kane
  4. Carys Evans
  5. Liam Barrett
  6. Amba Frese
  7. Irena Tetkovic
  8. Sven Bestmann  Is a corresponding author
  9. Charlotte J Stagg  Is a corresponding author
  1. University College London, United Kingdom
  2. University of Oxford, United Kingdom

Abstract

Skill learning is a fundamental adaptive process, but the mechanisms remain poorly understood. Some learning paradigms, particularly in the memory domain, are closely associated with gamma activity that is amplitude-modulated by the phase of underlying theta activity, but whether such nested activity patterns also underpin skill learning is unknown. Here we addressed this question by using transcranial alternating current stimulation (tACS) over sensorimotor cortex to modulate theta-gamma activity during motor skill acquisition, as an exemplar of a non-hippocampal-dependent task. We demonstrated, and then replicated, a significant improvement in skill acquisition with theta-gamma tACS, which outlasted the stimulation by an hour. Our results suggest that theta-gamma activity may be a common mechanism for learning across the brain and provides a putative novel intervention for optimising functional improvements in response to training or therapy.

Data availability

All data generated or analysed during this study are included in the manuscript and freely available on the open science framework (https://osf.io/xjpef). Details of data analysis, experimental design and protocol were pre-registered prior to data collection and freely available on the open science framework - Registration form: osf.io/xjpef; Files: osf.io/452f8/files/

Article and author information

Author details

  1. Haya Akkad

    epartment for Clinical and Movement Neuroscience, Institute of Neurology, University College London, London, United Kingdom
    For correspondence
    haya.akkad.14@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5621-3318
  2. Joshua Dupont-Hadwen

    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.
  3. Edward Kane

    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.
  4. Carys Evans

    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.
  5. Liam Barrett

    Department of Experimental Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Amba Frese

    Department of Experimental Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Irena Tetkovic

    Department of Experimental Psychology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Sven Bestmann

    epartment for Clinical and Movement Neuroscience, Institute of Neurology, University College London, London, United Kingdom
    For correspondence
    s.bestmann@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6867-9545
  9. Charlotte J Stagg

    FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    For correspondence
    charlotte.stagg@ndcn.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Funding

Royal Society (Sir Henry Dale Fellowship,102584/Z/13/Z)

  • Charlotte J Stagg

Brain Research UK (201617-03)

  • Sven Bestmann

Brain Research UK (Graduate Student Fellowship)

  • Haya Akkad

Wellcome Trust (Sir Henry Dale Fellowship - 102584/Z/13/Z)

  • Charlotte J Stagg

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

Ethics

Human subjects: Ethical permission for this study was granted by the University College London Research Ethics Committee (UCLREC: 6285/001). Written informed consent was obtained from all volunteers prior to data collection.

Reviewing Editor

  1. Thorsten Kahnt, Northwestern University, United States

Publication history

  1. Preprint posted: December 20, 2019 (view preprint)
  2. Received: February 8, 2021
  3. Accepted: November 23, 2021
  4. Accepted Manuscript published: November 23, 2021 (version 1)
  5. Version of Record published: December 20, 2021 (version 2)

Copyright

© 2021, Akkad 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. Haya Akkad
  2. Joshua Dupont-Hadwen
  3. Edward Kane
  4. Carys Evans
  5. Liam Barrett
  6. Amba Frese
  7. Irena Tetkovic
  8. Sven Bestmann
  9. Charlotte J Stagg
(2021)
Increasing human motor skill acquisition by driving theta-gamma coupling
eLife 10:e67355.
https://doi.org/10.7554/eLife.67355

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