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Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action

It is well established that dopamine transmission is integral in mediating the influence of reward expectations on reward-seeking actions. However, the precise causal role of dopamine transmission in moment-to-moment reward-motivated behavioral control remains contentious, particularly in contexts w...

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Autores principales: Grima, Laura L., Panayi, Marios C., Härmson, Oliver, Syed, Emilie C. J., Manohar, Sanjay G., Husain, Masud, Walton, Mark E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9283443/
https://www.ncbi.nlm.nih.gov/pubmed/35478011
http://dx.doi.org/10.1038/s41386-022-01312-6
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author Grima, Laura L.
Panayi, Marios C.
Härmson, Oliver
Syed, Emilie C. J.
Manohar, Sanjay G.
Husain, Masud
Walton, Mark E.
author_facet Grima, Laura L.
Panayi, Marios C.
Härmson, Oliver
Syed, Emilie C. J.
Manohar, Sanjay G.
Husain, Masud
Walton, Mark E.
author_sort Grima, Laura L.
collection PubMed
description It is well established that dopamine transmission is integral in mediating the influence of reward expectations on reward-seeking actions. However, the precise causal role of dopamine transmission in moment-to-moment reward-motivated behavioral control remains contentious, particularly in contexts where it is necessary to refrain from responding to achieve a beneficial outcome. To examine this, we manipulated dopamine transmission pharmacologically as rats performed a Go/No-Go task that required them to either make or withhold action to gain either a small or large reward. D1R Stimulation potentiated cue-driven action initiation, including fast impulsive actions on No-Go trials. By contrast, D1R blockade primarily disrupted the successful completion of Go trial sequences. Surprisingly, while after global D1R blockade this was characterized by a general retardation of reward-seeking actions, nucleus accumbens core (NAcC) D1R blockade had no effect on the speed of action initiation or impulsive actions. Instead, fine-grained analyses showed that this manipulation decreased the precision of animals’ goal-directed actions, even though they usually still followed the appropriate response sequence. Strikingly, such “unfocused” responding could also be observed off-drug, particularly when only a small reward was on offer. These findings suggest that the balance of activity at NAcC D1Rs plays a key role in enabling the rapid activation of a focused, reward-seeking state to enable animals to efficiently and accurately achieve their goal.
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spelling pubmed-92834432022-07-16 Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action Grima, Laura L. Panayi, Marios C. Härmson, Oliver Syed, Emilie C. J. Manohar, Sanjay G. Husain, Masud Walton, Mark E. Neuropsychopharmacology Article It is well established that dopamine transmission is integral in mediating the influence of reward expectations on reward-seeking actions. However, the precise causal role of dopamine transmission in moment-to-moment reward-motivated behavioral control remains contentious, particularly in contexts where it is necessary to refrain from responding to achieve a beneficial outcome. To examine this, we manipulated dopamine transmission pharmacologically as rats performed a Go/No-Go task that required them to either make or withhold action to gain either a small or large reward. D1R Stimulation potentiated cue-driven action initiation, including fast impulsive actions on No-Go trials. By contrast, D1R blockade primarily disrupted the successful completion of Go trial sequences. Surprisingly, while after global D1R blockade this was characterized by a general retardation of reward-seeking actions, nucleus accumbens core (NAcC) D1R blockade had no effect on the speed of action initiation or impulsive actions. Instead, fine-grained analyses showed that this manipulation decreased the precision of animals’ goal-directed actions, even though they usually still followed the appropriate response sequence. Strikingly, such “unfocused” responding could also be observed off-drug, particularly when only a small reward was on offer. These findings suggest that the balance of activity at NAcC D1Rs plays a key role in enabling the rapid activation of a focused, reward-seeking state to enable animals to efficiently and accurately achieve their goal. Springer International Publishing 2022-04-27 2022-08 /pmc/articles/PMC9283443/ /pubmed/35478011 http://dx.doi.org/10.1038/s41386-022-01312-6 Text en © The Author(s) 2022, corrected publication 2022 https://creativecommons.org/licenses/by/4.0/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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Grima, Laura L.
Panayi, Marios C.
Härmson, Oliver
Syed, Emilie C. J.
Manohar, Sanjay G.
Husain, Masud
Walton, Mark E.
Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title_full Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title_fullStr Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title_full_unstemmed Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title_short Nucleus accumbens D1-receptors regulate and focus transitions to reward-seeking action
title_sort nucleus accumbens d1-receptors regulate and focus transitions to reward-seeking action
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9283443/
https://www.ncbi.nlm.nih.gov/pubmed/35478011
http://dx.doi.org/10.1038/s41386-022-01312-6
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