Cargando…

Dopamine Modulates Dynamic Decision-Making during Foraging

The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to...

Descripción completa

Detalles Bibliográficos
Autores principales: Le Heron, Campbell, Kolling, Nils, Plant, Olivia, Kienast, Annika, Janska, Rebecca, Ang, Yuen-Siang, Fallon, Sean, Husain, Masud, Apps, Matthew A.J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7329313/
https://www.ncbi.nlm.nih.gov/pubmed/32457071
http://dx.doi.org/10.1523/JNEUROSCI.2586-19.2020
_version_ 1783552880141139968
author Le Heron, Campbell
Kolling, Nils
Plant, Olivia
Kienast, Annika
Janska, Rebecca
Ang, Yuen-Siang
Fallon, Sean
Husain, Masud
Apps, Matthew A.J.
author_facet Le Heron, Campbell
Kolling, Nils
Plant, Olivia
Kienast, Annika
Janska, Rebecca
Ang, Yuen-Siang
Fallon, Sean
Husain, Masud
Apps, Matthew A.J.
author_sort Le Heron, Campbell
collection PubMed
description The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to be compared continuously with potential rewards that could be obtained by traveling elsewhere (background reward rate), to determine the opportunity cost of staying versus leaving. We hypothesized that dopamine specifically modulates the influence of background, but not foreground, reward information when making a dynamic comparison of these variables for optimal behavior. On a novel foraging task based on an ecological account of animal behavior (marginal value theorem), human participants of either sex decided when to leave locations in situations where foreground rewards depleted at different rates, either in rich or poor environments with high or low background reward rates. In line with theoretical accounts, people's decisions to move from current locations were independently modulated by changes in both foreground and background reward rates. Pharmacological manipulation of dopamine D2 receptor activity using the agonist cabergoline significantly affected decisions to move on, specifically modulating the effect of background reward rates. In particular, when on cabergoline, people left patches in poor environments much earlier. These results demonstrate a role of dopamine in signaling the opportunity cost of rewards, not value per se. Using this ecologically derived framework, we uncover a specific mechanism by which D2 dopamine receptor activity modulates decision-making when foreground and background reward rates are dynamically compared. SIGNIFICANCE STATEMENT Many decisions, across economic, political, and social spheres, involve choices to “leave”. Such decisions depend on a continuous comparison of a current location's value, with that of other locations you could move on to. However, how the brain makes such decisions is poorly understood. Here, we developed a computerized task, based around theories of how animals make decisions to move on when foraging for food. Healthy human participants had to decide when to leave collecting financial rewards in a location, and travel to collect rewards elsewhere. Using a pharmacological manipulation, we show that the activity of dopamine in the brain modulates decisions to move on, with people valuing other locations differently depending on their dopaminergic state.
format Online
Article
Text
id pubmed-7329313
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Society for Neuroscience
record_format MEDLINE/PubMed
spelling pubmed-73293132020-07-02 Dopamine Modulates Dynamic Decision-Making during Foraging Le Heron, Campbell Kolling, Nils Plant, Olivia Kienast, Annika Janska, Rebecca Ang, Yuen-Siang Fallon, Sean Husain, Masud Apps, Matthew A.J. J Neurosci Research Articles The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to be compared continuously with potential rewards that could be obtained by traveling elsewhere (background reward rate), to determine the opportunity cost of staying versus leaving. We hypothesized that dopamine specifically modulates the influence of background, but not foreground, reward information when making a dynamic comparison of these variables for optimal behavior. On a novel foraging task based on an ecological account of animal behavior (marginal value theorem), human participants of either sex decided when to leave locations in situations where foreground rewards depleted at different rates, either in rich or poor environments with high or low background reward rates. In line with theoretical accounts, people's decisions to move from current locations were independently modulated by changes in both foreground and background reward rates. Pharmacological manipulation of dopamine D2 receptor activity using the agonist cabergoline significantly affected decisions to move on, specifically modulating the effect of background reward rates. In particular, when on cabergoline, people left patches in poor environments much earlier. These results demonstrate a role of dopamine in signaling the opportunity cost of rewards, not value per se. Using this ecologically derived framework, we uncover a specific mechanism by which D2 dopamine receptor activity modulates decision-making when foreground and background reward rates are dynamically compared. SIGNIFICANCE STATEMENT Many decisions, across economic, political, and social spheres, involve choices to “leave”. Such decisions depend on a continuous comparison of a current location's value, with that of other locations you could move on to. However, how the brain makes such decisions is poorly understood. Here, we developed a computerized task, based around theories of how animals make decisions to move on when foraging for food. Healthy human participants had to decide when to leave collecting financial rewards in a location, and travel to collect rewards elsewhere. Using a pharmacological manipulation, we show that the activity of dopamine in the brain modulates decisions to move on, with people valuing other locations differently depending on their dopaminergic state. Society for Neuroscience 2020-07-01 /pmc/articles/PMC7329313/ /pubmed/32457071 http://dx.doi.org/10.1523/JNEUROSCI.2586-19.2020 Text en Copyright © 2020 Le Heron et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Le Heron, Campbell
Kolling, Nils
Plant, Olivia
Kienast, Annika
Janska, Rebecca
Ang, Yuen-Siang
Fallon, Sean
Husain, Masud
Apps, Matthew A.J.
Dopamine Modulates Dynamic Decision-Making during Foraging
title Dopamine Modulates Dynamic Decision-Making during Foraging
title_full Dopamine Modulates Dynamic Decision-Making during Foraging
title_fullStr Dopamine Modulates Dynamic Decision-Making during Foraging
title_full_unstemmed Dopamine Modulates Dynamic Decision-Making during Foraging
title_short Dopamine Modulates Dynamic Decision-Making during Foraging
title_sort dopamine modulates dynamic decision-making during foraging
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7329313/
https://www.ncbi.nlm.nih.gov/pubmed/32457071
http://dx.doi.org/10.1523/JNEUROSCI.2586-19.2020
work_keys_str_mv AT leheroncampbell dopaminemodulatesdynamicdecisionmakingduringforaging
AT kollingnils dopaminemodulatesdynamicdecisionmakingduringforaging
AT plantolivia dopaminemodulatesdynamicdecisionmakingduringforaging
AT kienastannika dopaminemodulatesdynamicdecisionmakingduringforaging
AT janskarebecca dopaminemodulatesdynamicdecisionmakingduringforaging
AT angyuensiang dopaminemodulatesdynamicdecisionmakingduringforaging
AT fallonsean dopaminemodulatesdynamicdecisionmakingduringforaging
AT husainmasud dopaminemodulatesdynamicdecisionmakingduringforaging
AT appsmatthewaj dopaminemodulatesdynamicdecisionmakingduringforaging