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A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli

Dopamine signals in the striatum are critical for motivated behavior. However, their regional specificity and precise information content are actively debated. Dopaminergic projections to the striatum are topographically organized. Thus, we quantified dopamine release in response to motivational sti...

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Autores principales: van Elzelingen, Wouter, Goedhoop, Jessica, Warnaar, Pascal, Denys, Damiaan, Arbab, Tara, Willuhn, Ingo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9171911/
https://www.ncbi.nlm.nih.gov/pubmed/35594399
http://dx.doi.org/10.1073/pnas.2117270119
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author van Elzelingen, Wouter
Goedhoop, Jessica
Warnaar, Pascal
Denys, Damiaan
Arbab, Tara
Willuhn, Ingo
author_facet van Elzelingen, Wouter
Goedhoop, Jessica
Warnaar, Pascal
Denys, Damiaan
Arbab, Tara
Willuhn, Ingo
author_sort van Elzelingen, Wouter
collection PubMed
description Dopamine signals in the striatum are critical for motivated behavior. However, their regional specificity and precise information content are actively debated. Dopaminergic projections to the striatum are topographically organized. Thus, we quantified dopamine release in response to motivational stimuli and associated predictive cues in six principal striatal regions of unrestrained, behaving rats. Absolute signal size and its modulation by stimulus value and by subjective state of the animal were interregionally heterogeneous on a medial to lateral gradient. In contrast, dopamine-concentration direction of change was homogeneous across all regions: appetitive stimuli increased and aversive stimuli decreased dopamine concentration. Although cues predictive of such motivational stimuli acquired the same influence over dopamine homogeneously across all regions, dopamine-mediated prediction-error signals were restricted to the ventromedial, limbic striatum. Together, our findings demonstrate a nuanced striatal landscape of unidirectional but not uniform dopamine signals, topographically encoding distinct aspects of motivational stimuli and their prediction.
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spelling pubmed-91719112022-06-08 A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli van Elzelingen, Wouter Goedhoop, Jessica Warnaar, Pascal Denys, Damiaan Arbab, Tara Willuhn, Ingo Proc Natl Acad Sci U S A Biological Sciences Dopamine signals in the striatum are critical for motivated behavior. However, their regional specificity and precise information content are actively debated. Dopaminergic projections to the striatum are topographically organized. Thus, we quantified dopamine release in response to motivational stimuli and associated predictive cues in six principal striatal regions of unrestrained, behaving rats. Absolute signal size and its modulation by stimulus value and by subjective state of the animal were interregionally heterogeneous on a medial to lateral gradient. In contrast, dopamine-concentration direction of change was homogeneous across all regions: appetitive stimuli increased and aversive stimuli decreased dopamine concentration. Although cues predictive of such motivational stimuli acquired the same influence over dopamine homogeneously across all regions, dopamine-mediated prediction-error signals were restricted to the ventromedial, limbic striatum. Together, our findings demonstrate a nuanced striatal landscape of unidirectional but not uniform dopamine signals, topographically encoding distinct aspects of motivational stimuli and their prediction. National Academy of Sciences 2022-05-20 2022-05-24 /pmc/articles/PMC9171911/ /pubmed/35594399 http://dx.doi.org/10.1073/pnas.2117270119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
van Elzelingen, Wouter
Goedhoop, Jessica
Warnaar, Pascal
Denys, Damiaan
Arbab, Tara
Willuhn, Ingo
A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title_full A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title_fullStr A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title_full_unstemmed A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title_short A unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
title_sort unidirectional but not uniform striatal landscape of dopamine signaling for motivational stimuli
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9171911/
https://www.ncbi.nlm.nih.gov/pubmed/35594399
http://dx.doi.org/10.1073/pnas.2117270119
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