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Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle

Obsessive-compulsive disorder (OCD) has been suggested to be associated with impairment of model-based behavioral control. Meanwhile, recent work suggested shorter memory trace for negative than positive prediction errors (PEs) in OCD. We explored relations between these two suggestions through comp...

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Autores principales: Sato, Reo, Shimomura, Kanji, Morita, Kenji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10306209/
https://www.ncbi.nlm.nih.gov/pubmed/37319256
http://dx.doi.org/10.1371/journal.pcbi.1011206
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author Sato, Reo
Shimomura, Kanji
Morita, Kenji
author_facet Sato, Reo
Shimomura, Kanji
Morita, Kenji
author_sort Sato, Reo
collection PubMed
description Obsessive-compulsive disorder (OCD) has been suggested to be associated with impairment of model-based behavioral control. Meanwhile, recent work suggested shorter memory trace for negative than positive prediction errors (PEs) in OCD. We explored relations between these two suggestions through computational modeling. Based on the properties of cortico-basal ganglia pathways, we modeled human as an agent having a combination of successor representation (SR)-based system that enables model-based-like control and individual representation (IR)-based system that only hosts model-free control, with the two systems potentially learning from positive and negative PEs in different rates. We simulated the agent’s behavior in the environmental model used in the recent work that describes potential development of obsession-compulsion cycle. We found that the dual-system agent could develop enhanced obsession-compulsion cycle, similarly to the agent having memory trace imbalance in the recent work, if the SR- and IR-based systems learned mainly from positive and negative PEs, respectively. We then simulated the behavior of such an opponent SR+IR agent in the two-stage decision task, in comparison with the agent having only SR-based control. Fitting of the agents’ behavior by the model weighing model-based and model-free control developed in the original two-stage task study resulted in smaller weights of model-based control for the opponent SR+IR agent than for the SR-only agent. These results reconcile the previous suggestions about OCD, i.e., impaired model-based control and memory trace imbalance, raising a novel possibility that opponent learning in model(SR)-based and model-free controllers underlies obsession-compulsion. Our model cannot explain the behavior of OCD patients in punishment, rather than reward, contexts, but it could be resolved if opponent SR+IR learning operates also in the recently revealed non-canonical cortico-basal ganglia-dopamine circuit for threat/aversiveness, rather than reward, reinforcement learning, and the aversive SR + appetitive IR agent could actually develop obsession-compulsion if the environment is modeled differently.
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spelling pubmed-103062092023-06-29 Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle Sato, Reo Shimomura, Kanji Morita, Kenji PLoS Comput Biol Research Article Obsessive-compulsive disorder (OCD) has been suggested to be associated with impairment of model-based behavioral control. Meanwhile, recent work suggested shorter memory trace for negative than positive prediction errors (PEs) in OCD. We explored relations between these two suggestions through computational modeling. Based on the properties of cortico-basal ganglia pathways, we modeled human as an agent having a combination of successor representation (SR)-based system that enables model-based-like control and individual representation (IR)-based system that only hosts model-free control, with the two systems potentially learning from positive and negative PEs in different rates. We simulated the agent’s behavior in the environmental model used in the recent work that describes potential development of obsession-compulsion cycle. We found that the dual-system agent could develop enhanced obsession-compulsion cycle, similarly to the agent having memory trace imbalance in the recent work, if the SR- and IR-based systems learned mainly from positive and negative PEs, respectively. We then simulated the behavior of such an opponent SR+IR agent in the two-stage decision task, in comparison with the agent having only SR-based control. Fitting of the agents’ behavior by the model weighing model-based and model-free control developed in the original two-stage task study resulted in smaller weights of model-based control for the opponent SR+IR agent than for the SR-only agent. These results reconcile the previous suggestions about OCD, i.e., impaired model-based control and memory trace imbalance, raising a novel possibility that opponent learning in model(SR)-based and model-free controllers underlies obsession-compulsion. Our model cannot explain the behavior of OCD patients in punishment, rather than reward, contexts, but it could be resolved if opponent SR+IR learning operates also in the recently revealed non-canonical cortico-basal ganglia-dopamine circuit for threat/aversiveness, rather than reward, reinforcement learning, and the aversive SR + appetitive IR agent could actually develop obsession-compulsion if the environment is modeled differently. Public Library of Science 2023-06-15 /pmc/articles/PMC10306209/ /pubmed/37319256 http://dx.doi.org/10.1371/journal.pcbi.1011206 Text en © 2023 Sato 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
Sato, Reo
Shimomura, Kanji
Morita, Kenji
Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title_full Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title_fullStr Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title_full_unstemmed Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title_short Opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
title_sort opponent learning with different representations in the cortico-basal ganglia pathways can develop obsession-compulsion cycle
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10306209/
https://www.ncbi.nlm.nih.gov/pubmed/37319256
http://dx.doi.org/10.1371/journal.pcbi.1011206
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