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Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments

Humans are able to adapt to the fast-changing world by estimating statistical regularities of the environment. Although fear can profoundly impact adaptive behaviors, the computational and neural mechanisms underlying this phenomenon remain elusive. Here, we conducted a behavioral experiment (n = 21...

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Autores principales: Wang, Zhihao, Nan, Tian, Goerlich, Katharina S., Li, Yiman, Aleman, André, Luo, Yuejia, Xu, Pengfei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10174591/
https://www.ncbi.nlm.nih.gov/pubmed/37126501
http://dx.doi.org/10.1371/journal.pbio.3001724
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author Wang, Zhihao
Nan, Tian
Goerlich, Katharina S.
Li, Yiman
Aleman, André
Luo, Yuejia
Xu, Pengfei
author_facet Wang, Zhihao
Nan, Tian
Goerlich, Katharina S.
Li, Yiman
Aleman, André
Luo, Yuejia
Xu, Pengfei
author_sort Wang, Zhihao
collection PubMed
description Humans are able to adapt to the fast-changing world by estimating statistical regularities of the environment. Although fear can profoundly impact adaptive behaviors, the computational and neural mechanisms underlying this phenomenon remain elusive. Here, we conducted a behavioral experiment (n = 21) and a functional magnetic resonance imaging experiment (n = 37) with a novel cue-biased adaptation learning task, during which we simultaneously manipulated emotional valence (fearful/neutral expressions of the cue) and environmental volatility (frequent/infrequent reversals of reward probabilities). Across 2 experiments, computational modeling consistently revealed a higher learning rate for the environment with frequent versus infrequent reversals following neutral cues. In contrast, this flexible adjustment was absent in the environment with fearful cues, suggesting a suppressive role of fear in adaptation to environmental volatility. This suppressive effect was underpinned by activity of the ventral striatum, hippocampus, and dorsal anterior cingulate cortex (dACC) as well as increased functional connectivity between the dACC and temporal-parietal junction (TPJ) for fear with environmental volatility. Dynamic causal modeling identified that the driving effect was located in the TPJ and was associated with dACC activation, suggesting that the suppression of fear on adaptive behaviors occurs at the early stage of bottom-up processing. These findings provide a neuro-computational account of how fear interferes with adaptation to volatility during dynamic environments.
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spelling pubmed-101745912023-05-12 Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments Wang, Zhihao Nan, Tian Goerlich, Katharina S. Li, Yiman Aleman, André Luo, Yuejia Xu, Pengfei PLoS Biol Research Article Humans are able to adapt to the fast-changing world by estimating statistical regularities of the environment. Although fear can profoundly impact adaptive behaviors, the computational and neural mechanisms underlying this phenomenon remain elusive. Here, we conducted a behavioral experiment (n = 21) and a functional magnetic resonance imaging experiment (n = 37) with a novel cue-biased adaptation learning task, during which we simultaneously manipulated emotional valence (fearful/neutral expressions of the cue) and environmental volatility (frequent/infrequent reversals of reward probabilities). Across 2 experiments, computational modeling consistently revealed a higher learning rate for the environment with frequent versus infrequent reversals following neutral cues. In contrast, this flexible adjustment was absent in the environment with fearful cues, suggesting a suppressive role of fear in adaptation to environmental volatility. This suppressive effect was underpinned by activity of the ventral striatum, hippocampus, and dorsal anterior cingulate cortex (dACC) as well as increased functional connectivity between the dACC and temporal-parietal junction (TPJ) for fear with environmental volatility. Dynamic causal modeling identified that the driving effect was located in the TPJ and was associated with dACC activation, suggesting that the suppression of fear on adaptive behaviors occurs at the early stage of bottom-up processing. These findings provide a neuro-computational account of how fear interferes with adaptation to volatility during dynamic environments. Public Library of Science 2023-05-01 /pmc/articles/PMC10174591/ /pubmed/37126501 http://dx.doi.org/10.1371/journal.pbio.3001724 Text en © 2023 Wang 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
Wang, Zhihao
Nan, Tian
Goerlich, Katharina S.
Li, Yiman
Aleman, André
Luo, Yuejia
Xu, Pengfei
Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title_full Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title_fullStr Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title_full_unstemmed Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title_short Neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
title_sort neurocomputational mechanisms underlying fear-biased adaptation learning in changing environments
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10174591/
https://www.ncbi.nlm.nih.gov/pubmed/37126501
http://dx.doi.org/10.1371/journal.pbio.3001724
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