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Behavioral encoding across timescales by region-specific dopamine dynamics

The dorsal (DS) and ventral striatum (VS) receive dopaminergic projections that control motor functions and reward-related behavior. It remains poorly understood how dopamine release dynamics across different temporal scales in these regions are coupled to behavioral outcomes. Here, we employ the do...

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Autores principales: Jørgensen, Søren H., Ejdrup, Aske L., Lycas, Matthew D., Posselt, Leonie P., Madsen, Kenneth L., Tian, Lin, Dreyer, Jakob K., Herborg, Freja, Sørensen, Andreas T., Gether, Ulrik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963838/
https://www.ncbi.nlm.nih.gov/pubmed/36749722
http://dx.doi.org/10.1073/pnas.2215230120
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author Jørgensen, Søren H.
Ejdrup, Aske L.
Lycas, Matthew D.
Posselt, Leonie P.
Madsen, Kenneth L.
Tian, Lin
Dreyer, Jakob K.
Herborg, Freja
Sørensen, Andreas T.
Gether, Ulrik
author_facet Jørgensen, Søren H.
Ejdrup, Aske L.
Lycas, Matthew D.
Posselt, Leonie P.
Madsen, Kenneth L.
Tian, Lin
Dreyer, Jakob K.
Herborg, Freja
Sørensen, Andreas T.
Gether, Ulrik
author_sort Jørgensen, Søren H.
collection PubMed
description The dorsal (DS) and ventral striatum (VS) receive dopaminergic projections that control motor functions and reward-related behavior. It remains poorly understood how dopamine release dynamics across different temporal scales in these regions are coupled to behavioral outcomes. Here, we employ the dopamine sensor dLight1.3b together with multiregion fiber photometry and machine learning-based analysis to decode dopamine dynamics across the striatum during self-paced exploratory behavior in mice. Our data show a striking coordination of rapidly fluctuating signal in the DS, carrying information across dopamine levels, with a slower signal in the VS, consisting mainly of slow-paced transients. Importantly, these release dynamics correlated with discrete behavioral motifs, such as turns, running, and grooming on a subsecond-to-minute time scale. Disruption of dopamine dynamics with cocaine caused randomization of action selection sequencing and disturbance of DS–VS coordination. The data suggest that distinct dopamine dynamics of DS and VS jointly encode behavioral sequences during unconstrained activity with DS modulating the stringing together of actions and VS the signal to initiate and sustain the selected action.
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spelling pubmed-99638382023-08-07 Behavioral encoding across timescales by region-specific dopamine dynamics Jørgensen, Søren H. Ejdrup, Aske L. Lycas, Matthew D. Posselt, Leonie P. Madsen, Kenneth L. Tian, Lin Dreyer, Jakob K. Herborg, Freja Sørensen, Andreas T. Gether, Ulrik Proc Natl Acad Sci U S A Biological Sciences The dorsal (DS) and ventral striatum (VS) receive dopaminergic projections that control motor functions and reward-related behavior. It remains poorly understood how dopamine release dynamics across different temporal scales in these regions are coupled to behavioral outcomes. Here, we employ the dopamine sensor dLight1.3b together with multiregion fiber photometry and machine learning-based analysis to decode dopamine dynamics across the striatum during self-paced exploratory behavior in mice. Our data show a striking coordination of rapidly fluctuating signal in the DS, carrying information across dopamine levels, with a slower signal in the VS, consisting mainly of slow-paced transients. Importantly, these release dynamics correlated with discrete behavioral motifs, such as turns, running, and grooming on a subsecond-to-minute time scale. Disruption of dopamine dynamics with cocaine caused randomization of action selection sequencing and disturbance of DS–VS coordination. The data suggest that distinct dopamine dynamics of DS and VS jointly encode behavioral sequences during unconstrained activity with DS modulating the stringing together of actions and VS the signal to initiate and sustain the selected action. National Academy of Sciences 2023-02-07 2023-02-14 /pmc/articles/PMC9963838/ /pubmed/36749722 http://dx.doi.org/10.1073/pnas.2215230120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This 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
Jørgensen, Søren H.
Ejdrup, Aske L.
Lycas, Matthew D.
Posselt, Leonie P.
Madsen, Kenneth L.
Tian, Lin
Dreyer, Jakob K.
Herborg, Freja
Sørensen, Andreas T.
Gether, Ulrik
Behavioral encoding across timescales by region-specific dopamine dynamics
title Behavioral encoding across timescales by region-specific dopamine dynamics
title_full Behavioral encoding across timescales by region-specific dopamine dynamics
title_fullStr Behavioral encoding across timescales by region-specific dopamine dynamics
title_full_unstemmed Behavioral encoding across timescales by region-specific dopamine dynamics
title_short Behavioral encoding across timescales by region-specific dopamine dynamics
title_sort behavioral encoding across timescales by region-specific dopamine dynamics
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9963838/
https://www.ncbi.nlm.nih.gov/pubmed/36749722
http://dx.doi.org/10.1073/pnas.2215230120
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