A quantitative reward prediction error signal in the ventral pallidum

David J. Ottenheimer; Bilal A. Bari; Elissa Sutlief; Kurt M. Fraser; Tabitha H. Kim; Jocelyn M. Richard; Jeremiah Y. Cohen; Patricia H. Janak

doi:10.1038/s41593-020-0688-5

A quantitative reward prediction error signal in the ventral pallidum

David J. Ottenheimer, Bilal A. Bari, Elissa Sutlief, Kurt M. Fraser, Tabitha H. Kim, Jocelyn M. Richard, Jeremiah Y. Cohen, Patricia H. Janak

Neuroscience

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

The nervous system is hypothesized to compute reward prediction errors (RPEs) to promote adaptive behavior. Correlates of RPEs have been observed in the midbrain dopamine system, but the extent to which RPE signals exist in other reward-processing regions is less well understood. In the present study, we quantified outcome history-based RPE signals in the ventral pallidum (VP), a basal ganglia region functionally linked to reward-seeking behavior. We trained rats to respond to reward-predicting cues, and we fit computational models to predict the firing rates of individual neurons at the time of reward delivery. We found that a subset of VP neurons encoded RPEs and did so more robustly than the nucleus accumbens, an input to the VP. VP RPEs predicted changes in task engagement, and optogenetic manipulation of the VP during reward delivery bidirectionally altered rats’ subsequent reward-seeking behavior. Our data suggest a pivotal role for the VP in computing teaching signals that influence adaptive reward seeking.

Original language	English (US)
Pages (from-to)	1267-1276
Number of pages	10
Journal	Nature neuroscience
Volume	23
Issue number	10
DOIs	https://doi.org/10.1038/s41593-020-0688-5
State	Published - Oct 1 2020

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health (grant nos. 5T32NS91018-17 (to D.J.O.), F30MH110084 (to B.A.B.), K99AA025384 (to J.M.R.), R01DA042038 and R01NS104834 (to J.Y.C.), and R01DA035943 (to P.H.J.)), by Klingenstein-Simons, MQ, NARSAD, and Whitehall (to J.Y.C.), by a NARSAD Young Investigator Award (to J.M.R.) and by the National Science Foundation Graduate Research Fellowship (grant no. DGE1746891 to D.J.O.). We thank K. Wang and X. Tong for technical assistance.

Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

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title = "A quantitative reward prediction error signal in the ventral pallidum",

abstract = "The nervous system is hypothesized to compute reward prediction errors (RPEs) to promote adaptive behavior. Correlates of RPEs have been observed in the midbrain dopamine system, but the extent to which RPE signals exist in other reward-processing regions is less well understood. In the present study, we quantified outcome history-based RPE signals in the ventral pallidum (VP), a basal ganglia region functionally linked to reward-seeking behavior. We trained rats to respond to reward-predicting cues, and we fit computational models to predict the firing rates of individual neurons at the time of reward delivery. We found that a subset of VP neurons encoded RPEs and did so more robustly than the nucleus accumbens, an input to the VP. VP RPEs predicted changes in task engagement, and optogenetic manipulation of the VP during reward delivery bidirectionally altered rats{\textquoteright} subsequent reward-seeking behavior. Our data suggest a pivotal role for the VP in computing teaching signals that influence adaptive reward seeking.",

author = "Ottenheimer, {David J.} and Bari, {Bilal A.} and Elissa Sutlief and Fraser, {Kurt M.} and Kim, {Tabitha H.} and Richard, {Jocelyn M.} and Cohen, {Jeremiah Y.} and Janak, {Patricia H.}",

note = "Funding Information: This work was supported by the National Institutes of Health (grant nos. 5T32NS91018-17 (to D.J.O.), F30MH110084 (to B.A.B.), K99AA025384 (to J.M.R.), R01DA042038 and R01NS104834 (to J.Y.C.), and R01DA035943 (to P.H.J.)), by Klingenstein-Simons, MQ, NARSAD, and Whitehall (to J.Y.C.), by a NARSAD Young Investigator Award (to J.M.R.) and by the National Science Foundation Graduate Research Fellowship (grant no. DGE1746891 to D.J.O.). We thank K. Wang and X. Tong for technical assistance. Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature America, Inc. Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",

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A quantitative reward prediction error signal in the ventral pallidum

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