Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice

  1. William Menegas
  2. Benedicte M Babayan
  3. Naoshige Uchida
  4. Mitsuko Watabe-Uchida  Is a corresponding author
  1. Harvard University, United States

Abstract

Dopamine neurons are thought to encode novelty in addition to reward prediction error (the discrepancy between actual and predicted values). In this study, we compared dopamine activity across the striatum using fiber fluorometry in mice. During classical conditioning, we observed opposite dynamics in dopamine axon signals in the ventral striatum ('VS dopamine') and the posterior tail of the striatum ('TS dopamine'). TS dopamine showed strong excitation to novel cues, whereas VS dopamine showed no responses to novel cues until they had been paired with reward. TS dopamine cue responses decreased over time, depending on what the cue predicted. Additionally, TS dopamine showed excitation to several types of stimuli including rewarding, aversive, and neutral stimuli whereas VS dopamine showed excitation only to reward or reward-predicting cues. Together, these results demonstrate that dopamine novelty signals are localized in TS along with general salience signals, while VS dopamine reliably encodes reward prediction error.

Article and author information

Author details

  1. William Menegas

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  2. Benedicte M Babayan

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  3. Naoshige Uchida

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    Naoshige Uchida, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5755-9409
  4. Mitsuko Watabe-Uchida

    Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    mitsuko@mcb.harvard.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7864-754X

Funding

National Institute of Mental Health (R01MH095953)

  • Naoshige Uchida

Harvard Mind Brain and Behavior

  • Naoshige Uchida

National Institute of Mental Health (R01MH101207)

  • Naoshige Uchida

National Institute of Mental Health (R01MH110404)

  • Naoshige Uchida

Foundation pour la Recherche Medicale (SPE20150331860)

  • Benedicte M Babayan

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

Ethics

Animal experimentation: 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 Harvard animal care and use committee (IACUC) protocols (#26-03) of Harvard University. All surgery was performed under isofluorane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Gary L Westbrook, Vollum Institute, United States

Publication history

  1. Received: September 27, 2016
  2. Accepted: January 4, 2017
  3. Accepted Manuscript published: January 5, 2017 (version 1)
  4. Version of Record published: January 27, 2017 (version 2)

Copyright

© 2017, Menegas 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. William Menegas
  2. Benedicte M Babayan
  3. Naoshige Uchida
  4. Mitsuko Watabe-Uchida
(2017)
Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice
eLife 6:e21886.
https://doi.org/10.7554/eLife.21886

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