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

Abstract
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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.

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William Menegas

Center for Brain Science, Harvard University, Cambridge, United States

Competing interests
No competing interests declared.
Benedicte M Babayan

Center for Brain Science, Harvard University, Cambridge, United States

Competing interests
No competing interests declared.
Naoshige Uchida

Center for Brain Science, Harvard University, Cambridge, United States

Competing interests
Naoshige Uchida, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-5755-9409
Mitsuko Watabe-Uchida

Center for Brain Science, Harvard University, Cambridge, United States

For correspondence
mitsuko@mcb.harvard.edu

Competing interests
No competing interests declared.

"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.

Copyright

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.