Reward prediction error does not explain movement selectivity in DMS-projecting dopamine neurons

Abstract

Although midbrain dopamine (DA) neurons have been thought to primarily encode reward prediction error (RPE), recent studies have also found movement-related DAergic signals. For example, we recently reported that DA neurons in mice projecting to dorsomedial striatum are modulated by choices contralateral to the recording side. Here, we introduce, and ultimately reject, a candidate resolution for the puzzling RPE vs movement dichotomy, by showing how seemingly movement-related activity might be explained by an action-specific RPE. By considering both choice and RPE on a trial-by-trial basis, we find that DA signals are modulated by contralateral choice in a manner that is distinct from RPE, implying that choice encoding is better explained by movement direction. This fundamental separation between RPE and movement encoding may help shed light on the diversity of functions and dysfunctions of the DA system.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Rachel S Lee

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Marcelo G Mattar

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Nathan F Parker

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ilana B Witten

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    For correspondence
    iwitten@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0548-2160
  5. Nathaniel D Daw

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    For correspondence
    ndaw@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5029-1430

Funding

National Institute for Health Research (5R01MH106689-02)

  • Ilana B Witten

New York Stem Cell Foundation (Robertson Investigator)

  • Ilana B Witten

Army Research Office (W911NF-16-1-0474)

  • Nathaniel D Daw

Army Research Office (W911NF-17-1-0554)

  • Ilana B Witten

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

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, United States

Version history

  1. Received: October 19, 2018
  2. Accepted: April 3, 2019
  3. Accepted Manuscript published: April 4, 2019 (version 1)
  4. Version of Record published: April 15, 2019 (version 2)

Copyright

© 2019, 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. Rachel S Lee
  2. Marcelo G Mattar
  3. Nathan F Parker
  4. Ilana B Witten
  5. Nathaniel D Daw
(2019)
Reward prediction error does not explain movement selectivity in DMS-projecting dopamine neurons
eLife 8:e42992.
https://doi.org/10.7554/eLife.42992

Share this article

https://doi.org/10.7554/eLife.42992

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