Competition between parallel sensorimotor learning systems

  1. Scott T Albert  Is a corresponding author
  2. Jihoon Jang
  3. Shanaathanan Modchalingam
  4. Marius 't Hart
  5. Denise Henriques
  6. Gonzalo Lerner
  7. Valeria Della-Maggiore
  8. Adrian M Haith
  9. John W Krakauer
  10. Reza Shadmehr
  1. Johns Hopkins School of Medicine, United States
  2. York University, Canada
  3. University of Buenos Aires, Argentina
  4. Johns Hopkins University School of Medicine, United States

Abstract

Sensorimotor learning is supported by at least two parallel systems: a strategic process that benefits from explicit knowledge, and an implicit process that adapts subconsciously. How do these systems interact? Does one system's contributions suppress the other, or do they operate independently? Here we illustrate that during reaching, implicit and explicit systems both learn from visual target errors. This shared error leads to competition such that an increase in the explicit system's response siphons away resources that are needed for implicit adaptation, thus reducing its learning. As a result, steady-state implicit learning can vary across experimental conditions, due to changes in strategy. Furthermore, strategies can mask changes in implicit learning properties, such as its error sensitivity. These ideas, however, become more complex in conditions where subjects adapt using multiple visual landmarks, a situation which introduces learning from sensory prediction errors in addition to target errors. These two types of implicit errors can oppose each other, leading to another type of competition. Thus, during sensorimotor adaptation, implicit and explicit learning systems compete for a common resource: error.

Data availability

Source data files generated or analyzed during this study, as well as the associated analysis code, are included as supplements to Figures 1-10, as well as their associated Figure Supplements, and have also been deposited in OSF under accession code MZS6A

The following data sets were generated

Article and author information

Author details

  1. Scott T Albert

    Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    For correspondence
    scottalbert1@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9140-1077
  2. Jihoon Jang

    Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shanaathanan Modchalingam

    Department of Kinesiology and Health Science, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Marius 't Hart

    Department of Kinesiology and Health Science, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Denise Henriques

    Department of Kinesiology and Health Science, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Gonzalo Lerner

    Deparamento de Fisiología y Biofísia, University of Buenos Aires, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7791-9408
  7. Valeria Della-Maggiore

    Deparamento de Fisiología y Biofísia, University of Buenos Aires, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  8. Adrian M Haith

    Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5658-8654
  9. John W Krakauer

    Department of Neurology, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4316-1846
  10. Reza Shadmehr

    Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7686-2569

Funding

National Institute of Neurological Disorders and Stroke (F32NS095706)

  • Scott T Albert

National Science Foundation (CNS-1714623)

  • Reza Shadmehr

National Institute of Neurological Disorders and Stroke (R01NS078311)

  • Reza Shadmehr

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

Ethics

Human subjects: Informed consent was obtained from all study participants. All human subjects work was approved by the Johns Hopkins School of Medicine Institutional Review Board (protocol number NA_00037510) or the York Human Participants Review Sub-committee.

Copyright

© 2022, Albert 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. Scott T Albert
  2. Jihoon Jang
  3. Shanaathanan Modchalingam
  4. Marius 't Hart
  5. Denise Henriques
  6. Gonzalo Lerner
  7. Valeria Della-Maggiore
  8. Adrian M Haith
  9. John W Krakauer
  10. Reza Shadmehr
(2022)
Competition between parallel sensorimotor learning systems
eLife 11:e65361.
https://doi.org/10.7554/eLife.65361

Share this article

https://doi.org/10.7554/eLife.65361

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