Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhong, Shan, Choi, Jeong Woo, Hashoush, Nadia G., Babayan, Diana, Malekmohammadi, Mahsa, Pouratian, Nader, Christopoulos, Vassilios
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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
_version_ 1784842331835334656
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
work_keys_str_mv AT zhongshan aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT choijeongwoo aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT hashoushnadiag aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT babayandiana aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT malekmohammadimahsa aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT pouratiannader aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT christopoulosvassilios aneurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT zhongshan neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT choijeongwoo neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT hashoushnadiag neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT babayandiana neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT malekmohammadimahsa neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT pouratiannader neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease
AT christopoulosvassilios neurocomputationaltheoryofactionregulationpredictsmotorbehaviorinneurotypicalindividualsandpatientswithparkinsonsdisease