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Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models

Choosing actions that result in advantageous outcomes is a fundamental function of nervous systems. All computational decision-making models contain a mechanism that controls the variability of (or confidence in) action selection, but its neural implementation is unclear—especially in humans. We inv...

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Autores principales: Adams, Rick A, Moutoussis, Michael, Nour, Matthew M, Dahoun, Tarik, Lewis, Declan, Illingworth, Benjamin, Veronese, Mattia, Mathys, Christoph, de Boer, Lieke, Guitart-Masip, Marc, Friston, Karl J, Howes, Oliver D, Roiser, Jonathan P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7233027/
https://www.ncbi.nlm.nih.gov/pubmed/32083297
http://dx.doi.org/10.1093/cercor/bhz327
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author Adams, Rick A
Moutoussis, Michael
Nour, Matthew M
Dahoun, Tarik
Lewis, Declan
Illingworth, Benjamin
Veronese, Mattia
Mathys, Christoph
de Boer, Lieke
Guitart-Masip, Marc
Friston, Karl J
Howes, Oliver D
Roiser, Jonathan P
author_facet Adams, Rick A
Moutoussis, Michael
Nour, Matthew M
Dahoun, Tarik
Lewis, Declan
Illingworth, Benjamin
Veronese, Mattia
Mathys, Christoph
de Boer, Lieke
Guitart-Masip, Marc
Friston, Karl J
Howes, Oliver D
Roiser, Jonathan P
author_sort Adams, Rick A
collection PubMed
description Choosing actions that result in advantageous outcomes is a fundamental function of nervous systems. All computational decision-making models contain a mechanism that controls the variability of (or confidence in) action selection, but its neural implementation is unclear—especially in humans. We investigated this mechanism using two influential decision-making frameworks: active inference (AI) and reinforcement learning (RL). In AI, the precision (inverse variance) of beliefs about policies controls action selection variability—similar to decision ‘noise’ parameters in RL—and is thought to be encoded by striatal dopamine signaling. We tested this hypothesis by administering a ‘go/no-go’ task to 75 healthy participants, and measuring striatal dopamine 2/3 receptor (D(2/3)R) availability in a subset (n = 25) using [(11)C]-(+)-PHNO positron emission tomography. In behavioral model comparison, RL performed best across the whole group but AI performed best in participants performing above chance levels. Limbic striatal D(2/3)R availability had linear relationships with AI policy precision (P = 0.029) as well as with RL irreducible decision ‘noise’ (P = 0.020), and this relationship with D(2/3)R availability was confirmed with a ‘decision stochasticity’ factor that aggregated across both models (P = 0.0006). These findings are consistent with occupancy of inhibitory striatal D(2/3)Rs decreasing the variability of action selection in humans.
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spelling pubmed-72330272020-05-21 Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models Adams, Rick A Moutoussis, Michael Nour, Matthew M Dahoun, Tarik Lewis, Declan Illingworth, Benjamin Veronese, Mattia Mathys, Christoph de Boer, Lieke Guitart-Masip, Marc Friston, Karl J Howes, Oliver D Roiser, Jonathan P Cereb Cortex Original Article Choosing actions that result in advantageous outcomes is a fundamental function of nervous systems. All computational decision-making models contain a mechanism that controls the variability of (or confidence in) action selection, but its neural implementation is unclear—especially in humans. We investigated this mechanism using two influential decision-making frameworks: active inference (AI) and reinforcement learning (RL). In AI, the precision (inverse variance) of beliefs about policies controls action selection variability—similar to decision ‘noise’ parameters in RL—and is thought to be encoded by striatal dopamine signaling. We tested this hypothesis by administering a ‘go/no-go’ task to 75 healthy participants, and measuring striatal dopamine 2/3 receptor (D(2/3)R) availability in a subset (n = 25) using [(11)C]-(+)-PHNO positron emission tomography. In behavioral model comparison, RL performed best across the whole group but AI performed best in participants performing above chance levels. Limbic striatal D(2/3)R availability had linear relationships with AI policy precision (P = 0.029) as well as with RL irreducible decision ‘noise’ (P = 0.020), and this relationship with D(2/3)R availability was confirmed with a ‘decision stochasticity’ factor that aggregated across both models (P = 0.0006). These findings are consistent with occupancy of inhibitory striatal D(2/3)Rs decreasing the variability of action selection in humans. Oxford University Press 2020-05 2020-02-21 /pmc/articles/PMC7233027/ /pubmed/32083297 http://dx.doi.org/10.1093/cercor/bhz327 Text en © The Author(s) 2020. Published by Oxford University Press. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Adams, Rick A
Moutoussis, Michael
Nour, Matthew M
Dahoun, Tarik
Lewis, Declan
Illingworth, Benjamin
Veronese, Mattia
Mathys, Christoph
de Boer, Lieke
Guitart-Masip, Marc
Friston, Karl J
Howes, Oliver D
Roiser, Jonathan P
Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title_full Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title_fullStr Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title_full_unstemmed Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title_short Variability in Action Selection Relates to Striatal Dopamine 2/3 Receptor Availability in Humans: A PET Neuroimaging Study Using Reinforcement Learning and Active Inference Models
title_sort variability in action selection relates to striatal dopamine 2/3 receptor availability in humans: a pet neuroimaging study using reinforcement learning and active inference models
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7233027/
https://www.ncbi.nlm.nih.gov/pubmed/32083297
http://dx.doi.org/10.1093/cercor/bhz327
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