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Dorsal Raphe Dopamine Neurons Signal Motivational Salience Dependent on Internal State, Expectation, and Behavioral Context

Cho, Jounhong Ryan and Chen, Xinhong and Kahan, Anat and Robinson, J. Elliott and Wagenaar, Daniel A. and Gradinaru, Viviana (2021) Dorsal Raphe Dopamine Neurons Signal Motivational Salience Dependent on Internal State, Expectation, and Behavioral Context. Journal of Neuroscience, 41 (12). pp. 2645-2655. ISSN 0270-6474. PMCID PMC8018733. doi:10.1523/JNEUROSCI.2690-20.2021. https://resolver.caltech.edu/CaltechAUTHORS:20200728-094010838

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Abstract

The ability to recognize motivationally salient events and respond to them adaptively is critical for survival. Here we tested whether dopamine (DA) neurons in the dorsal raphe nucleus (DRN) contribute to this process. Population recordings of DRN^(DA) neurons during associative learning tasks showed that their activity dynamically tracks salience, developing excitation to both reward- and punishment-paired cues. The DRNDA response to reward-predicting cues was diminished after satiety, suggesting modulation by internal states. DRN^(DA) activity was also greater for unexpected outcomes than for expected outcomes. Two-photon imaging of DRN^(DA) neurons demonstrated that the majority of individual neurons developed activation to reward predicting cues but not to punishment-predicting cues, which was surprising and qualitatively distinct from the population results. Head-fixation during fear learning abolished the neural response to aversive cues, indicating modulation by behavioral context. Overall, these results suggest that DRN^(DA) neurons encode motivational salience, dependent on internal and external factors.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/JNEUROSCI.2690-20.2021DOIArticle
https://doi.org/10.1101/2020.07.27.222729DOIDiscussion Paper
http://github.com/GradinaruLab/dLight1Related ItemData/Code
ORCID:
AuthorORCID
Cho, Jounhong Ryan0000-0001-9542-716X
Chen, Xinhong0000-0003-0408-0813
Robinson, J. Elliott0000-0001-9417-3938
Wagenaar, Daniel A.0000-0002-6222-761X
Gradinaru, Viviana0000-0001-5868-348X
Alternate Title:Dorsal raphe dopamine neurons signal motivational salience dependent on internal and external states
Additional Information:© 2021 the authors. Received Oct. 19, 2020; revised Jan. 19, 2021; accepted Jan. 26, 2021. This work was supported by the National Institutes of Health (NIH) Director’s New Innovator Grant IDP20D091182-01, Presidential Early Career Award for Scientists and Engineers, the NIH/National Institute on Aging Grant 1R01AG047664-01, the NIH Grant BRAIN 1U01NS090577, Heritage Medical Research Institute, Chen Institute (V.G.), Beckman Institute (V.G. and D.A.W.), Tianqiao & Chrissy Chen Institute Chen Graduate Fellowship (X.C.), Colvin Divisional Fellowship at Caltech (A.K.), and the Children’s Tumor Foundation Young Investigator Award 2016-01-00 (to J.E.R.). We thank the entire Gradinaru lab for critical feedback. Author contributions: J.R.C. and V.G. designed research; J.R.C., X.C., A.K., and J.E.R. performed research; A. K. and D.A.W. contributed unpublished reagents/analytic tools; J.R.C. and X.C. analyzed data; J.R.C. and V.G. wrote the paper. The authors declare no competing financial interests.
Group:Heritage Medical Research Institute, Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NIHIDP20D091182-01
NIH1R01AG047664-01
NIH1U01NS090577
Heritage Medical Research InstituteUNSPECIFIED
Tianqiao and Chrissy Chen Institute for NeuroscienceUNSPECIFIED
Caltech Beckman InstituteUNSPECIFIED
Caltech Division of Biology and Biological EngineeringUNSPECIFIED
Children’s Tumor Foundation2016-01-00
Subject Keywords:dopamine; dorsal raphe nucleus; fiber photometry; head fixation; motivational salience; two-photon imaging
Issue or Number:12
PubMed Central ID:PMC8018733
DOI:10.1523/JNEUROSCI.2690-20.2021
Record Number:CaltechAUTHORS:20200728-094010838
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200728-094010838
Official Citation:Dorsal Raphe Dopamine Neurons Signal Motivational Salience Dependent on Internal State, Expectation, and Behavioral Context. Jounhong Ryan Cho, Xinhong Chen, Anat Kahan, J. Elliott Robinson, Daniel A. Wagenaar, Viviana Gradinaru. Journal of Neuroscience 24 March 2021, 41 (12) 2645-2655; DOI: 10.1523/JNEUROSCI.2690-20.2021
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104602
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:28 Jul 2020 19:56
Last Modified:23 Apr 2021 17:49

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