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Coordination of rapid cholinergic and dopaminergic signaling in striatum during spontaneous movement

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Cite this article as: eLife 2019;8:e44903 doi: 10.7554/eLife.44903

Abstract

Interplay between dopaminergic and cholinergic neuromodulation in the striatum is crucial for movement control, with prominent models proposing pro-kinetic and anti-kinetic effects of dopamine and acetylcholine release, respectively. However, the natural, movement-related signals of striatum cholinergic neurons and their relationship to simultaneous variations in dopamine signaling are unknown. Here, functional optical recordings in mice were used to establish rapid cholinergic signals in dorsal striatum during spontaneous movements. Bursts across the cholinergic population occurred at transitions between movement states and were marked by widespread network synchronization which diminished during sustained locomotion. Simultaneous cholinergic and dopaminergic recordings revealed distinct but coordinated sub-second signals, suggesting a new model where cholinergic population synchrony signals rapid changes in movement states while dopamine signals the drive to enact or sustain those states.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting files. Processed data from large data files (time-series movies) that support the findings of this study are available at Dryad Dataverse (doi:10.5061/dryad.244nt37).

The following data sets were generated

Article and author information

Author details

  1. Mark Howe

    Department of Neurobiology, Northwestern University, Evanston, United States
    For correspondence
    mwhowe@bu.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Imane Ridouh

    Department of Neurobiology, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Anna Letizia Allegra Mascaro

    Department of Neurobiology, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8489-0076
  4. Alyssa Larios

    Department of Neurobiology, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Maite Azcorra Sedano

    Department of Neurobiology, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniel Dombeck

    Department of Neurobiology, Northwestern University, Evanston, United States
    For correspondence
    d-dombeck@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2576-5918

Funding

National Institutes of Health (R01MH110556)

  • Daniel Dombeck

McKnight Foundation

  • Daniel Dombeck

National Institutes of Health (T32 AG20506)

  • Mark Howe

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 experiments were approved by the Northwestern University Animal Care and Use Committee (Protocol #IS00005043 and IS00003736).

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Publication history

  1. Received: January 5, 2019
  2. Accepted: March 26, 2019
  3. Accepted Manuscript published: March 28, 2019 (version 1)
  4. Version of Record published: April 10, 2019 (version 2)

Copyright

© 2019, Howe 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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