Coupling between motor cortex and striatum increases during sleep over long-term skill learning

Abstract

The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or 'offline' during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-REM (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.

Data availability

The data and corresponding code used for analyses have been made available on Dryad (DOI: 10.7272/Q6KK9927).

The following data sets were generated

Article and author information

Author details

  1. Stefan M Lemke

    Neurology, UCSF, San Francicso, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1721-5425
  2. Dhakshin S Ramanathan

    Psychiatry, UCSD, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David Darevksy

    Neurology, UCSF, San Francicso, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Daniel Egert

    Neurology, UCSF, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Joshua D Berke

    Neurology, UCSF, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1436-6823
  6. Karunesh Ganguly

    Neurology, UCSF, San Francisco, United States
    For correspondence
    karunesh.ganguly@ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2570-9943

Funding

Veterans Health Association (I01RX001640-06)

  • Karunesh Ganguly

NIMH (R01MH111871-04)

  • Karunesh Ganguly

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

Ethics

Animal experimentation: This study was performed in strict accordance with guidelines from the USDA Animal Welfare Act and United States Public Health Science Policy. Procedures were in accordance with protocols approved by the Institutional Animal Care and Use Committee at the San Francisco Veterans Affairs Medical Center (Protocol 19-002).

Reviewing Editor

  1. Aryn H Gittis, Carnegie Mellon University, United States

Version history

  1. Received: October 24, 2020
  2. Accepted: August 9, 2021
  3. Accepted Manuscript published: September 10, 2021 (version 1)
  4. Version of Record published: September 14, 2021 (version 2)
  5. Version of Record updated: October 18, 2021 (version 3)

Copyright

© 2021, Lemke 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. Stefan M Lemke
  2. Dhakshin S Ramanathan
  3. David Darevksy
  4. Daniel Egert
  5. Joshua D Berke
  6. Karunesh Ganguly
(2021)
Coupling between motor cortex and striatum increases during sleep over long-term skill learning
eLife 10:e64303.
https://doi.org/10.7554/eLife.64303

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https://doi.org/10.7554/eLife.64303

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