Abstract

Reinforcement has long been thought to require striatal synaptic plasticity. Indeed, direct striatal manipulations such as self-stimulation of direct-pathway projection neurons (dMSNs) are sufficient to induce reinforcement within minutes. However, it's unclear what role, if any, is played by downstream circuitry. Here, we used dMSN self-stimulation in mice as a model for striatum-driven reinforcement and mapped the underlying circuitry across multiple basal ganglia nuclei and output targets. We found that mimicking the effects of dMSN activation on downstream circuitry, through optogenetic suppression of basal ganglia output nucleus substantia nigra reticulata (SNr) or activation of SNr targets in the brainstem or thalamus, was also sufficient to drive rapid reinforcement. Remarkably, silencing motor thalamus-but not other selected targets of SNr-was the only manipulation that reduced dMSN-driven reinforcement. Together, these results point to an unexpected role for basal ganglia output to motor thalamus in striatum-driven reinforcement.

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. Arnaud L Lalive

    Neurological Disease, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Anthony D Lien

    Neurological Disease, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Thomas K Roseberry

    Neurological Disease, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Christopher H Donahue

    Neurological Disease, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Anatol C Kreitzer

    Neurological Disease, Gladstone Institutes, San Francisco, United States
    For correspondence
    akreitzer@gladstone.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7423-2398

Funding

Swiss National Science Foundation

  • Arnaud L Lalive

National Institutes of Health (U01 NS094342)

  • Anatol C Kreitzer

National Institutes of Health (P01 DA010154)

  • Anatol C Kreitzer

National Institutes of Health (R01 NS064984)

  • Anatol C Kreitzer

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 the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (AN144957) of the University of California, San Francisco. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Copyright

© 2018, Lalive 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. Arnaud L Lalive
  2. Anthony D Lien
  3. Thomas K Roseberry
  4. Christopher H Donahue
  5. Anatol C Kreitzer
(2018)
Motor thalamus supports striatum-driven reinforcement
eLife 7:e34032.
https://doi.org/10.7554/eLife.34032

Share this article

https://doi.org/10.7554/eLife.34032

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