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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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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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. |
format | Online Article Text |
id | pubmed-10174591 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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