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Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure

Compulsive individuals have deficits in model-based planning, but the mechanisms that drive this have not been established. We examined two candidates—that compulsivity is linked to (1) an impaired model of the task environment and/or (2) an inability to engage cognitive control when making choices....

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Autores principales: Seow, Tricia X. F., Benoit, Edith, Dempsey, Caoimhe, Jennings, Maeve, Maxwell, Aoibheann, O'Connell, Redmond, Gillan, Claire M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318073/
https://www.ncbi.nlm.nih.gov/pubmed/34131033
http://dx.doi.org/10.1523/JNEUROSCI.0031-21.2021
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author Seow, Tricia X. F.
Benoit, Edith
Dempsey, Caoimhe
Jennings, Maeve
Maxwell, Aoibheann
O'Connell, Redmond
Gillan, Claire M.
author_facet Seow, Tricia X. F.
Benoit, Edith
Dempsey, Caoimhe
Jennings, Maeve
Maxwell, Aoibheann
O'Connell, Redmond
Gillan, Claire M.
author_sort Seow, Tricia X. F.
collection PubMed
description Compulsive individuals have deficits in model-based planning, but the mechanisms that drive this have not been established. We examined two candidates—that compulsivity is linked to (1) an impaired model of the task environment and/or (2) an inability to engage cognitive control when making choices. To test this, 192 participants performed a two-step reinforcement learning task with concurrent EEG recordings, and we related the neural and behavioral data to their scores on a self-reported transdiagnostic dimension of compulsivity. To examine subjects' internal model of the task, we used established behavioral and neural responses to unexpected events [reaction time (RT) slowing, P300 wave, and parietal-occipital alpha band power] measured when an unexpected transition occurred. To assess cognitive control, we probed theta power at the time of initial choice. As expected, model-based planning was linked to greater behavioral (RT) and neural (alpha power, but not P300) sensitivity to rare transitions. Critically, the sensitivities of both RT and alpha to task structure were weaker in those high in compulsivity. This RT-compulsivity effect was tested and replicated in an independent pre-existing dataset (N = 1413). We also found that mid-frontal theta power at the time of choice was reduced in highly compulsive individuals though its relation to model-based planning was less pronounced. These data suggest that model-based planning deficits in compulsive individuals may arise, at least in part, from having an impaired representation of the environment, specifically how actions lead to future states. SIGNIFICANCE STATEMENT Compulsivity is linked to poorer performance on tasks that require model-based planning, but it is unclear what precise mechanisms underlie this deficit. Do compulsive individuals fail to engage cognitive control at the time of choice? Or do they have difficulty in building and maintaining an accurate representation of their environment, the foundation needed to behave in a goal-directed manner? With reaction time and EEG measures in 192 individuals who performed a two-step decision-making task, we found that compulsive individuals are less sensitive to surprising action–state transitions, where they slow down less and show less alpha band suppression following a rare transition. These findings implicate failures in maintaining an accurate model of the world in model-based planning deficits in compulsivity.
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spelling pubmed-83180732021-07-29 Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure Seow, Tricia X. F. Benoit, Edith Dempsey, Caoimhe Jennings, Maeve Maxwell, Aoibheann O'Connell, Redmond Gillan, Claire M. J Neurosci Research Articles Compulsive individuals have deficits in model-based planning, but the mechanisms that drive this have not been established. We examined two candidates—that compulsivity is linked to (1) an impaired model of the task environment and/or (2) an inability to engage cognitive control when making choices. To test this, 192 participants performed a two-step reinforcement learning task with concurrent EEG recordings, and we related the neural and behavioral data to their scores on a self-reported transdiagnostic dimension of compulsivity. To examine subjects' internal model of the task, we used established behavioral and neural responses to unexpected events [reaction time (RT) slowing, P300 wave, and parietal-occipital alpha band power] measured when an unexpected transition occurred. To assess cognitive control, we probed theta power at the time of initial choice. As expected, model-based planning was linked to greater behavioral (RT) and neural (alpha power, but not P300) sensitivity to rare transitions. Critically, the sensitivities of both RT and alpha to task structure were weaker in those high in compulsivity. This RT-compulsivity effect was tested and replicated in an independent pre-existing dataset (N = 1413). We also found that mid-frontal theta power at the time of choice was reduced in highly compulsive individuals though its relation to model-based planning was less pronounced. These data suggest that model-based planning deficits in compulsive individuals may arise, at least in part, from having an impaired representation of the environment, specifically how actions lead to future states. SIGNIFICANCE STATEMENT Compulsivity is linked to poorer performance on tasks that require model-based planning, but it is unclear what precise mechanisms underlie this deficit. Do compulsive individuals fail to engage cognitive control at the time of choice? Or do they have difficulty in building and maintaining an accurate representation of their environment, the foundation needed to behave in a goal-directed manner? With reaction time and EEG measures in 192 individuals who performed a two-step decision-making task, we found that compulsive individuals are less sensitive to surprising action–state transitions, where they slow down less and show less alpha band suppression following a rare transition. These findings implicate failures in maintaining an accurate model of the world in model-based planning deficits in compulsivity. Society for Neuroscience 2021-07-28 /pmc/articles/PMC8318073/ /pubmed/34131033 http://dx.doi.org/10.1523/JNEUROSCI.0031-21.2021 Text en Copyright © 2021 Seow et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Seow, Tricia X. F.
Benoit, Edith
Dempsey, Caoimhe
Jennings, Maeve
Maxwell, Aoibheann
O'Connell, Redmond
Gillan, Claire M.
Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title_full Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title_fullStr Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title_full_unstemmed Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title_short Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure
title_sort model-based planning deficits in compulsivity are linked to faulty neural representations of task structure
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318073/
https://www.ncbi.nlm.nih.gov/pubmed/34131033
http://dx.doi.org/10.1523/JNEUROSCI.0031-21.2021
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