Cell-type specific responses to associative learning in the primary motor cortex

Abstract

The primary motor cortex (M1) is known to be a critical site for movement initiation and motor learning. Surprisingly, it has also been shown to possess reward-related activity, presumably to facilitate reward-based learning of new movements. However, whether reward-related signals are represented among different cell types in M1, and whether their response properties change after cue-reward conditioning remains unclear. Here, we performed longitudinal in vivo two-photon Ca2+ imaging to monitor the activity of different neuronal cell types in M1 while mice engaged in a classical conditioning task. Our results demonstrate that most of the major neuronal cell types in M1 showed robust but differential responses to both the conditioned cue stimulus (CS) and reward, and their response properties undergo cell-type specific modifications after associative learning. PV-INs' responses became more reliable to the CS, while VIP-INs' responses became more reliable to reward. PNs only showed robust responses to novel reward, and they habituated to it after associative learning. Lastly, SOM-INs' responses emerged and became more reliable to both the CS and reward after conditioning. These observations suggest that cue- and reward-related signals are preferentially represented among different neuronal cell types in M1, and the distinct modifications they undergo during associative learning could be essential in triggering different aspects of local circuit reorganization in M1 during reward-based motor skill learning.

Data availability

Codes to reproduce the analysis for figures 1-2 and 4-7 are available at https://github.com/clee162/Analysis-of-Cell-type-Specific-Responses-to-Associative-Learning-in-M1. Codes to reproduce the analysis and figure 3 are available at https://github.com/nauralcodinglab/interneuron-reward. Data can be found on Dryad at https://doi.org/10.5061/dryad.q573n5tjj

The following data sets were generated

Article and author information

Author details

  1. Candice Lee

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Emerson F Harkin

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0698-5894
  3. Xuming Yin

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Richard Naud

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7383-3095
  5. Simon Chen

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    For correspondence
    schen2@uottawa.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7595-7443

Funding

Natural Sciences and Engineering Research Council of Canada (05308)

  • Simon Chen

Canada Research Chairs (950-231274)

  • Simon Chen

Natural Sciences and Engineering Research Council of Canada (06972)

  • Richard Naud

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

Ethics

Animal experimentation: All animal experiments were approved by the University of Ottawa Animal Care Committee and in accordance with the Canadian Council on Animal Care guidelines (protocol #: CMM-2737)

Copyright

© 2022, Lee 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. Candice Lee
  2. Emerson F Harkin
  3. Xuming Yin
  4. Richard Naud
  5. Simon Chen
(2022)
Cell-type specific responses to associative learning in the primary motor cortex
eLife 11:e72549.
https://doi.org/10.7554/eLife.72549

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https://doi.org/10.7554/eLife.72549