Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex

Psychostimulants such as d-amphetamine (AMPH) often have behavioral effects that appear paradoxical within the framework of optimal choice theory. AMPH typically increases task engagement and the effort animals exert for reward, despite decreasing reward valuation. We investigated neural correlates...

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Autores principales: Hashemnia, Saeedeh, Euston, David R, Gruber, Aaron J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455243/
https://www.ncbi.nlm.nih.gov/pubmed/32812864
http://dx.doi.org/10.7554/eLife.56755
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author Hashemnia, Saeedeh
Euston, David R
Gruber, Aaron J
author_facet Hashemnia, Saeedeh
Euston, David R
Gruber, Aaron J
author_sort Hashemnia, Saeedeh
collection PubMed
description Psychostimulants such as d-amphetamine (AMPH) often have behavioral effects that appear paradoxical within the framework of optimal choice theory. AMPH typically increases task engagement and the effort animals exert for reward, despite decreasing reward valuation. We investigated neural correlates of this phenomenon in the anterior cingulate cortex (ACC), a brain structure implicated in signaling cost-benefit utility. AMPH decreased signaling of reward, but not effort, in the ACC of freely-moving rats. Ensembles of simultaneously recorded neurons generated task-specific trajectories of neural activity encoding past, present, and future events. Low-dose AMPH contracted these trajectories and reduced their variance, whereas high-dose AMPH expanded both. We propose that under low-dose AMPH, increased network stability balances moderately increased excitability, which promotes accelerated unfolding of a neural ‘script’ for task execution, despite reduced reward valuation. Noise from excessive excitability at high doses overcomes stability enhancement to drive frequent deviation from the script, impairing task execution.
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spelling pubmed-74552432020-08-31 Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex Hashemnia, Saeedeh Euston, David R Gruber, Aaron J eLife Neuroscience Psychostimulants such as d-amphetamine (AMPH) often have behavioral effects that appear paradoxical within the framework of optimal choice theory. AMPH typically increases task engagement and the effort animals exert for reward, despite decreasing reward valuation. We investigated neural correlates of this phenomenon in the anterior cingulate cortex (ACC), a brain structure implicated in signaling cost-benefit utility. AMPH decreased signaling of reward, but not effort, in the ACC of freely-moving rats. Ensembles of simultaneously recorded neurons generated task-specific trajectories of neural activity encoding past, present, and future events. Low-dose AMPH contracted these trajectories and reduced their variance, whereas high-dose AMPH expanded both. We propose that under low-dose AMPH, increased network stability balances moderately increased excitability, which promotes accelerated unfolding of a neural ‘script’ for task execution, despite reduced reward valuation. Noise from excessive excitability at high doses overcomes stability enhancement to drive frequent deviation from the script, impairing task execution. eLife Sciences Publications, Ltd 2020-08-19 /pmc/articles/PMC7455243/ /pubmed/32812864 http://dx.doi.org/10.7554/eLife.56755 Text en © 2020, Hashemnia et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Hashemnia, Saeedeh
Euston, David R
Gruber, Aaron J
Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title_full Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title_fullStr Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title_full_unstemmed Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title_short Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
title_sort amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7455243/
https://www.ncbi.nlm.nih.gov/pubmed/32812864
http://dx.doi.org/10.7554/eLife.56755
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