Associability-modulated loss learning is increased in posttraumatic stress disorder

Disproportionate reactions to unexpected stimuli in the environment are a cardinal symptom of posttraumatic stress disorder (PTSD). Here, we test whether these heightened responses are associated with disruptions in distinct components of reinforcement learning. Specifically, using functional neuroi...

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Main Authors: Vanessa M Brown, Lusha Zhu, John M Wang, B Christopher Frueh, Brooks King-Casas, Pearl H Chiu
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/30150
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author Vanessa M Brown
Lusha Zhu
John M Wang
B Christopher Frueh
Brooks King-Casas
Pearl H Chiu
author_facet Vanessa M Brown
Lusha Zhu
John M Wang
B Christopher Frueh
Brooks King-Casas
Pearl H Chiu
author_sort Vanessa M Brown
collection DOAJ
description Disproportionate reactions to unexpected stimuli in the environment are a cardinal symptom of posttraumatic stress disorder (PTSD). Here, we test whether these heightened responses are associated with disruptions in distinct components of reinforcement learning. Specifically, using functional neuroimaging, a loss-learning task, and a computational model-based approach, we assessed the mechanistic hypothesis that overreactions to stimuli in PTSD arise from anomalous gating of attention during learning (i.e., associability). Behavioral choices of combat-deployed veterans with and without PTSD were fit to a reinforcement learning model, generating trial-by-trial prediction errors (signaling unexpected outcomes) and associability values (signaling attention allocation to the unexpected outcomes). Neural substrates of associability value and behavioral parameter estimates of associability updating, but not prediction error, increased with PTSD during loss learning. Moreover, the interaction of PTSD severity with neural markers of associability value predicted behavioral choices. These results indicate that increased attention-based learning may underlie aspects of PTSD and suggest potential neuromechanistic treatment targets.
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spelling doaj.art-aa3899d4c1e543e68634c5f0bf980f8e2022-12-22T03:53:05ZengeLife Sciences Publications LtdeLife2050-084X2018-01-01710.7554/eLife.30150Associability-modulated loss learning is increased in posttraumatic stress disorderVanessa M Brown0https://orcid.org/0000-0003-0284-0890Lusha Zhu1https://orcid.org/0000-0001-8717-6356John M Wang2B Christopher Frueh3Brooks King-Casas4Pearl H Chiu5https://orcid.org/0000-0002-8767-7406Virginia Tech Carilion Research Institute, Roanoke, United States; Department of Psychology, Virginia Tech, Blacksburg, United StatesVirginia Tech Carilion Research Institute, Roanoke, United States; School of Psychological and Cognitive Sciences, IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking–Tsinghua Center for Life Sciences, Peking University, Beijing, ChinaVirginia Tech Carilion Research Institute, Roanoke, United States; Department of Psychology, Virginia Tech, Blacksburg, United StatesUniversity of Hawaii, Hilo, United StatesVirginia Tech Carilion Research Institute, Roanoke, United States; Department of Psychology, Virginia Tech, Blacksburg, United States; Salem Veterans Affairs Medical Center, Salem, United States; School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, United StatesVirginia Tech Carilion Research Institute, Roanoke, United States; Department of Psychology, Virginia Tech, Blacksburg, United States; Salem Veterans Affairs Medical Center, Salem, United StatesDisproportionate reactions to unexpected stimuli in the environment are a cardinal symptom of posttraumatic stress disorder (PTSD). Here, we test whether these heightened responses are associated with disruptions in distinct components of reinforcement learning. Specifically, using functional neuroimaging, a loss-learning task, and a computational model-based approach, we assessed the mechanistic hypothesis that overreactions to stimuli in PTSD arise from anomalous gating of attention during learning (i.e., associability). Behavioral choices of combat-deployed veterans with and without PTSD were fit to a reinforcement learning model, generating trial-by-trial prediction errors (signaling unexpected outcomes) and associability values (signaling attention allocation to the unexpected outcomes). Neural substrates of associability value and behavioral parameter estimates of associability updating, but not prediction error, increased with PTSD during loss learning. Moreover, the interaction of PTSD severity with neural markers of associability value predicted behavioral choices. These results indicate that increased attention-based learning may underlie aspects of PTSD and suggest potential neuromechanistic treatment targets.https://elifesciences.org/articles/30150PTSDreinforcement learningamygdalafMRIassociabilitycomputational psychiatry
spellingShingle Vanessa M Brown
Lusha Zhu
John M Wang
B Christopher Frueh
Brooks King-Casas
Pearl H Chiu
Associability-modulated loss learning is increased in posttraumatic stress disorder
eLife
PTSD
reinforcement learning
amygdala
fMRI
associability
computational psychiatry
title Associability-modulated loss learning is increased in posttraumatic stress disorder
title_full Associability-modulated loss learning is increased in posttraumatic stress disorder
title_fullStr Associability-modulated loss learning is increased in posttraumatic stress disorder
title_full_unstemmed Associability-modulated loss learning is increased in posttraumatic stress disorder
title_short Associability-modulated loss learning is increased in posttraumatic stress disorder
title_sort associability modulated loss learning is increased in posttraumatic stress disorder
topic PTSD
reinforcement learning
amygdala
fMRI
associability
computational psychiatry
url https://elifesciences.org/articles/30150
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AT bchristopherfrueh associabilitymodulatedlosslearningisincreasedinposttraumaticstressdisorder
AT brookskingcasas associabilitymodulatedlosslearningisincreasedinposttraumaticstressdisorder
AT pearlhchiu associabilitymodulatedlosslearningisincreasedinposttraumaticstressdisorder