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A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease
Surviving in an uncertain environment requires not only the ability to select the best action, but also the flexibility to withhold inappropriate actions when the environmental conditions change. Although selecting and withholding actions have been extensively studied in both human and animals, ther...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9714880/ https://www.ncbi.nlm.nih.gov/pubmed/36395336 http://dx.doi.org/10.1371/journal.pcbi.1010111 |
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author | Zhong, Shan Choi, Jeong Woo Hashoush, Nadia G. Babayan, Diana Malekmohammadi, Mahsa Pouratian, Nader Christopoulos, Vassilios |
author_facet | Zhong, Shan Choi, Jeong Woo Hashoush, Nadia G. Babayan, Diana Malekmohammadi, Mahsa Pouratian, Nader Christopoulos, Vassilios |
author_sort | Zhong, Shan |
collection | PubMed |
description | Surviving in an uncertain environment requires not only the ability to select the best action, but also the flexibility to withhold inappropriate actions when the environmental conditions change. Although selecting and withholding actions have been extensively studied in both human and animals, there is still lack of consensus on the mechanism underlying these action regulation functions, and more importantly, how they inter-relate. A critical gap impeding progress is the lack of a computational theory that will integrate the mechanisms of action regulation into a unified framework. The current study aims to advance our understanding by developing a neurodynamical computational theory that models the mechanism of action regulation that involves suppressing responses, and predicts how disruption of this mechanism can lead to motor deficits in Parkinson’s disease (PD) patients. We tested the model predictions in neurotypical individuals and PD patients in three behavioral tasks that involve free action selection between two opposed directions, action selection in the presence of conflicting information and abandoning an ongoing action when a stop signal is presented. Our results and theory suggest an integrated mechanism of action regulation that affects both action initiation and inhibition. When this mechanism is disrupted, motor behavior is affected, leading to longer reaction times and higher error rates in action inhibition. |
format | Online Article Text |
id | pubmed-9714880 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-97148802022-12-02 A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease Zhong, Shan Choi, Jeong Woo Hashoush, Nadia G. Babayan, Diana Malekmohammadi, Mahsa Pouratian, Nader Christopoulos, Vassilios PLoS Comput Biol Research Article Surviving in an uncertain environment requires not only the ability to select the best action, but also the flexibility to withhold inappropriate actions when the environmental conditions change. Although selecting and withholding actions have been extensively studied in both human and animals, there is still lack of consensus on the mechanism underlying these action regulation functions, and more importantly, how they inter-relate. A critical gap impeding progress is the lack of a computational theory that will integrate the mechanisms of action regulation into a unified framework. The current study aims to advance our understanding by developing a neurodynamical computational theory that models the mechanism of action regulation that involves suppressing responses, and predicts how disruption of this mechanism can lead to motor deficits in Parkinson’s disease (PD) patients. We tested the model predictions in neurotypical individuals and PD patients in three behavioral tasks that involve free action selection between two opposed directions, action selection in the presence of conflicting information and abandoning an ongoing action when a stop signal is presented. Our results and theory suggest an integrated mechanism of action regulation that affects both action initiation and inhibition. When this mechanism is disrupted, motor behavior is affected, leading to longer reaction times and higher error rates in action inhibition. Public Library of Science 2022-11-17 /pmc/articles/PMC9714880/ /pubmed/36395336 http://dx.doi.org/10.1371/journal.pcbi.1010111 Text en © 2022 Zhong 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 (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Zhong, Shan Choi, Jeong Woo Hashoush, Nadia G. Babayan, Diana Malekmohammadi, Mahsa Pouratian, Nader Christopoulos, Vassilios A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title | A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title_full | A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title_fullStr | A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title_full_unstemmed | A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title_short | A neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with Parkinson’s disease |
title_sort | neurocomputational theory of action regulation predicts motor behavior in neurotypical individuals and patients with parkinson’s disease |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9714880/ https://www.ncbi.nlm.nih.gov/pubmed/36395336 http://dx.doi.org/10.1371/journal.pcbi.1010111 |
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