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Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making

Even simple behaviour requires us to make decisions based on combining multiple pieces of learned and new information. Making such decisions requires both learning the optimal response to each given stimulus as well as combining probabilistic information from multiple stimuli before selecting a resp...

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Autores principales: Coulthard, Elizabeth J., Bogacz, Rafal, Javed, Shazia, Mooney, Lucy K., Murphy, Gillian, Keeley, Sophie, Whone, Alan L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3525052/
https://www.ncbi.nlm.nih.gov/pubmed/23114368
http://dx.doi.org/10.1093/brain/aws273
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author Coulthard, Elizabeth J.
Bogacz, Rafal
Javed, Shazia
Mooney, Lucy K.
Murphy, Gillian
Keeley, Sophie
Whone, Alan L.
author_facet Coulthard, Elizabeth J.
Bogacz, Rafal
Javed, Shazia
Mooney, Lucy K.
Murphy, Gillian
Keeley, Sophie
Whone, Alan L.
author_sort Coulthard, Elizabeth J.
collection PubMed
description Even simple behaviour requires us to make decisions based on combining multiple pieces of learned and new information. Making such decisions requires both learning the optimal response to each given stimulus as well as combining probabilistic information from multiple stimuli before selecting a response. Computational theories of decision making predict that learning individual stimulus–response associations and rapid combination of information from multiple stimuli are dependent on different components of basal ganglia circuitry. In particular, learning and retention of memory, required for optimal response choice, are significantly reliant on dopamine, whereas integrating information probabilistically is critically dependent upon functioning of the glutamatergic subthalamic nucleus (computing the ‘normalization term’ in Bayes’ theorem). Here, we test these theories by investigating 22 patients with Parkinson’s disease either treated with deep brain stimulation to the subthalamic nucleus and dopaminergic therapy or managed with dopaminergic therapy alone. We use computerized tasks that probe three cognitive functions—information acquisition (learning), memory over a delay and information integration when multiple pieces of sequentially presented information have to be combined. Patients performed the tasks ON or OFF deep brain stimulation and/or ON or OFF dopaminergic therapy. Consistent with the computational theories, we show that stopping dopaminergic therapy impairs memory for probabilistic information over a delay, whereas deep brain stimulation to the region of the subthalamic nucleus disrupts decision making when multiple pieces of acquired information must be combined. Furthermore, we found that when participants needed to update their decision on the basis of the last piece of information presented in the decision-making task, patients with deep brain stimulation of the subthalamic nucleus region did not slow down appropriately to revise their plan, a pattern of behaviour that mirrors the impulsivity described clinically in some patients with subthalamic nucleus deep brain stimulation. Thus, we demonstrate distinct mechanisms for two important facets of human decision making: first, a role for dopamine in memory consolidation, and second, the critical importance of the subthalamic nucleus in successful decision making when multiple pieces of information must be combined.
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spelling pubmed-35250522012-12-18 Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making Coulthard, Elizabeth J. Bogacz, Rafal Javed, Shazia Mooney, Lucy K. Murphy, Gillian Keeley, Sophie Whone, Alan L. Brain Original Articles Even simple behaviour requires us to make decisions based on combining multiple pieces of learned and new information. Making such decisions requires both learning the optimal response to each given stimulus as well as combining probabilistic information from multiple stimuli before selecting a response. Computational theories of decision making predict that learning individual stimulus–response associations and rapid combination of information from multiple stimuli are dependent on different components of basal ganglia circuitry. In particular, learning and retention of memory, required for optimal response choice, are significantly reliant on dopamine, whereas integrating information probabilistically is critically dependent upon functioning of the glutamatergic subthalamic nucleus (computing the ‘normalization term’ in Bayes’ theorem). Here, we test these theories by investigating 22 patients with Parkinson’s disease either treated with deep brain stimulation to the subthalamic nucleus and dopaminergic therapy or managed with dopaminergic therapy alone. We use computerized tasks that probe three cognitive functions—information acquisition (learning), memory over a delay and information integration when multiple pieces of sequentially presented information have to be combined. Patients performed the tasks ON or OFF deep brain stimulation and/or ON or OFF dopaminergic therapy. Consistent with the computational theories, we show that stopping dopaminergic therapy impairs memory for probabilistic information over a delay, whereas deep brain stimulation to the region of the subthalamic nucleus disrupts decision making when multiple pieces of acquired information must be combined. Furthermore, we found that when participants needed to update their decision on the basis of the last piece of information presented in the decision-making task, patients with deep brain stimulation of the subthalamic nucleus region did not slow down appropriately to revise their plan, a pattern of behaviour that mirrors the impulsivity described clinically in some patients with subthalamic nucleus deep brain stimulation. Thus, we demonstrate distinct mechanisms for two important facets of human decision making: first, a role for dopamine in memory consolidation, and second, the critical importance of the subthalamic nucleus in successful decision making when multiple pieces of information must be combined. Oxford University Press 2012-12 2012-10-31 /pmc/articles/PMC3525052/ /pubmed/23114368 http://dx.doi.org/10.1093/brain/aws273 Text en © The Author (2012). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/2.0/uk/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Coulthard, Elizabeth J.
Bogacz, Rafal
Javed, Shazia
Mooney, Lucy K.
Murphy, Gillian
Keeley, Sophie
Whone, Alan L.
Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title_full Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title_fullStr Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title_full_unstemmed Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title_short Distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
title_sort distinct roles of dopamine and subthalamic nucleus in learning and probabilistic decision making
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3525052/
https://www.ncbi.nlm.nih.gov/pubmed/23114368
http://dx.doi.org/10.1093/brain/aws273
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