Midbrain dopamine neurons signal aversion in a reward-context-dependent manner

Dopamine is thought to regulate learning from appetitive and aversive events. Here we examined how optogenetically-identified dopamine neurons in the lateral ventral tegmental area of mice respond to aversive events in different conditions. In low reward contexts, most dopamine neurons were exclusiv...

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Main Authors: Hideyuki Matsumoto, Ju Tian, Naoshige Uchida, Mitsuko Watabe-Uchida
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/17328
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spelling doaj-26cb12d1273f4524a43d3409173d82472021-05-05T00:38:45ZengeLife Sciences Publications LtdeLife2050-084X2016-10-01510.7554/eLife.17328Midbrain dopamine neurons signal aversion in a reward-context-dependent mannerHideyuki Matsumoto0Ju Tian1Naoshige Uchida2https://orcid.org/0000-0002-5755-9409Mitsuko Watabe-Uchida3https://orcid.org/0000-0001-7864-754XCenter for Brain Science, Harvard University, Cambridge, United States; Department of Molecular and Cellular Biology, Harvard University, Cambridge, United StatesCenter for Brain Science, Harvard University, Cambridge, United States; Department of Molecular and Cellular Biology, Harvard University, Cambridge, United StatesCenter for Brain Science, Harvard University, Cambridge, United States; Department of Molecular and Cellular Biology, Harvard University, Cambridge, United StatesCenter for Brain Science, Harvard University, Cambridge, United States; Department of Molecular and Cellular Biology, Harvard University, Cambridge, United StatesDopamine is thought to regulate learning from appetitive and aversive events. Here we examined how optogenetically-identified dopamine neurons in the lateral ventral tegmental area of mice respond to aversive events in different conditions. In low reward contexts, most dopamine neurons were exclusively inhibited by aversive events, and expectation reduced dopamine neurons’ responses to reward and punishment. When a single odor predicted both reward and punishment, dopamine neurons’ responses to that odor reflected the integrated value of both outcomes. Thus, in low reward contexts, dopamine neurons signal value prediction errors (VPEs) integrating information about both reward and aversion in a common currency. In contrast, in high reward contexts, dopamine neurons acquired a short-latency excitation to aversive events that masked their VPE signaling. Our results demonstrate the importance of considering the contexts to examine the representation in dopamine neurons and uncover different modes of dopamine signaling, each of which may be adaptive for different environments.https://elifesciences.org/articles/17328dopaminevalueprediction erroraversioncontexteye blink
collection DOAJ
language English
format Article
sources DOAJ
author Hideyuki Matsumoto
Ju Tian
Naoshige Uchida
Mitsuko Watabe-Uchida
spellingShingle Hideyuki Matsumoto
Ju Tian
Naoshige Uchida
Mitsuko Watabe-Uchida
Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
eLife
dopamine
value
prediction error
aversion
context
eye blink
author_facet Hideyuki Matsumoto
Ju Tian
Naoshige Uchida
Mitsuko Watabe-Uchida
author_sort Hideyuki Matsumoto
title Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
title_short Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
title_full Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
title_fullStr Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
title_full_unstemmed Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
title_sort midbrain dopamine neurons signal aversion in a reward-context-dependent manner
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2016-10-01
description Dopamine is thought to regulate learning from appetitive and aversive events. Here we examined how optogenetically-identified dopamine neurons in the lateral ventral tegmental area of mice respond to aversive events in different conditions. In low reward contexts, most dopamine neurons were exclusively inhibited by aversive events, and expectation reduced dopamine neurons’ responses to reward and punishment. When a single odor predicted both reward and punishment, dopamine neurons’ responses to that odor reflected the integrated value of both outcomes. Thus, in low reward contexts, dopamine neurons signal value prediction errors (VPEs) integrating information about both reward and aversion in a common currency. In contrast, in high reward contexts, dopamine neurons acquired a short-latency excitation to aversive events that masked their VPE signaling. Our results demonstrate the importance of considering the contexts to examine the representation in dopamine neurons and uncover different modes of dopamine signaling, each of which may be adaptive for different environments.
topic dopamine
value
prediction error
aversion
context
eye blink
url https://elifesciences.org/articles/17328
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