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Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction

The learning of stimulus-outcome associations allows for predictions about the environment. Ventral striatum and dopaminergic midbrain neurons form a larger network for generating reward prediction signals from sensory cues. Yet, the network plasticity mechanisms to generate predictive signals in th...

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Autores principales: Oettl, Lars-Lennart, Scheller, Max, Filosa, Carla, Wieland, Sebastian, Haag, Franziska, Loeb, Cathrin, Durstewitz, Daniel, Shusterman, Roman, Russo, Eleonora, Kelsch, Wolfgang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7351739/
https://www.ncbi.nlm.nih.gov/pubmed/32651365
http://dx.doi.org/10.1038/s41467-020-17257-7
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author Oettl, Lars-Lennart
Scheller, Max
Filosa, Carla
Wieland, Sebastian
Haag, Franziska
Loeb, Cathrin
Durstewitz, Daniel
Shusterman, Roman
Russo, Eleonora
Kelsch, Wolfgang
author_facet Oettl, Lars-Lennart
Scheller, Max
Filosa, Carla
Wieland, Sebastian
Haag, Franziska
Loeb, Cathrin
Durstewitz, Daniel
Shusterman, Roman
Russo, Eleonora
Kelsch, Wolfgang
author_sort Oettl, Lars-Lennart
collection PubMed
description The learning of stimulus-outcome associations allows for predictions about the environment. Ventral striatum and dopaminergic midbrain neurons form a larger network for generating reward prediction signals from sensory cues. Yet, the network plasticity mechanisms to generate predictive signals in these distributed circuits have not been entirely clarified. Also, direct evidence of the underlying interregional assembly formation and information transfer is still missing. Here we show that phasic dopamine is sufficient to reinforce the distinctness of stimulus representations in the ventral striatum even in the absence of reward. Upon such reinforcement, striatal stimulus encoding gives rise to interregional assemblies that drive dopaminergic neurons during stimulus-outcome learning. These assemblies dynamically encode the predicted reward value of conditioned stimuli. Together, our data reveal that ventral striatal and midbrain reward networks form a reinforcing loop to generate reward prediction coding.
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spelling pubmed-73517392020-07-13 Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction Oettl, Lars-Lennart Scheller, Max Filosa, Carla Wieland, Sebastian Haag, Franziska Loeb, Cathrin Durstewitz, Daniel Shusterman, Roman Russo, Eleonora Kelsch, Wolfgang Nat Commun Article The learning of stimulus-outcome associations allows for predictions about the environment. Ventral striatum and dopaminergic midbrain neurons form a larger network for generating reward prediction signals from sensory cues. Yet, the network plasticity mechanisms to generate predictive signals in these distributed circuits have not been entirely clarified. Also, direct evidence of the underlying interregional assembly formation and information transfer is still missing. Here we show that phasic dopamine is sufficient to reinforce the distinctness of stimulus representations in the ventral striatum even in the absence of reward. Upon such reinforcement, striatal stimulus encoding gives rise to interregional assemblies that drive dopaminergic neurons during stimulus-outcome learning. These assemblies dynamically encode the predicted reward value of conditioned stimuli. Together, our data reveal that ventral striatal and midbrain reward networks form a reinforcing loop to generate reward prediction coding. Nature Publishing Group UK 2020-07-10 /pmc/articles/PMC7351739/ /pubmed/32651365 http://dx.doi.org/10.1038/s41467-020-17257-7 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Oettl, Lars-Lennart
Scheller, Max
Filosa, Carla
Wieland, Sebastian
Haag, Franziska
Loeb, Cathrin
Durstewitz, Daniel
Shusterman, Roman
Russo, Eleonora
Kelsch, Wolfgang
Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title_full Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title_fullStr Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title_full_unstemmed Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title_short Phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
title_sort phasic dopamine reinforces distinct striatal stimulus encoding in the olfactory tubercle driving dopaminergic reward prediction
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7351739/
https://www.ncbi.nlm.nih.gov/pubmed/32651365
http://dx.doi.org/10.1038/s41467-020-17257-7
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