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Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans

Anxiety has been linked to altered belief formation and uncertainty estimation, impacting learning. Identifying the neural processes underlying these changes is important for understanding brain pathology. Here, we show that oscillatory activity in the medial prefrontal, anterior cingulate and orbit...

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Autores principales: Hein, Thomas P., Gong, Zheng, Ivanova, Marina, Fedele, Tommaso, Nikulin, Vadim, Herrojo Ruiz, Maria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10017780/
https://www.ncbi.nlm.nih.gov/pubmed/36922553
http://dx.doi.org/10.1038/s42003-023-04628-1
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author Hein, Thomas P.
Gong, Zheng
Ivanova, Marina
Fedele, Tommaso
Nikulin, Vadim
Herrojo Ruiz, Maria
author_facet Hein, Thomas P.
Gong, Zheng
Ivanova, Marina
Fedele, Tommaso
Nikulin, Vadim
Herrojo Ruiz, Maria
author_sort Hein, Thomas P.
collection PubMed
description Anxiety has been linked to altered belief formation and uncertainty estimation, impacting learning. Identifying the neural processes underlying these changes is important for understanding brain pathology. Here, we show that oscillatory activity in the medial prefrontal, anterior cingulate and orbitofrontal cortex (mPFC, ACC, OFC) explains anxiety-related learning alterations. In a magnetoencephalography experiment, two groups of human participants pre-screened with high and low trait anxiety (HTA, LTA: 39) performed a probabilistic reward-based learning task. HTA undermined learning through an overestimation of volatility, leading to faster belief updating, more stochastic decisions and pronounced lose-shift tendencies. On a neural level, we observed increased gamma activity in the ACC, dmPFC, and OFC during encoding of precision-weighted prediction errors in HTA, accompanied by suppressed ACC alpha/beta activity. Our findings support the association between altered learning and belief updating in anxiety and changes in gamma and alpha/beta activity in the ACC, dmPFC, and OFC.
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spelling pubmed-100177802023-03-17 Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans Hein, Thomas P. Gong, Zheng Ivanova, Marina Fedele, Tommaso Nikulin, Vadim Herrojo Ruiz, Maria Commun Biol Article Anxiety has been linked to altered belief formation and uncertainty estimation, impacting learning. Identifying the neural processes underlying these changes is important for understanding brain pathology. Here, we show that oscillatory activity in the medial prefrontal, anterior cingulate and orbitofrontal cortex (mPFC, ACC, OFC) explains anxiety-related learning alterations. In a magnetoencephalography experiment, two groups of human participants pre-screened with high and low trait anxiety (HTA, LTA: 39) performed a probabilistic reward-based learning task. HTA undermined learning through an overestimation of volatility, leading to faster belief updating, more stochastic decisions and pronounced lose-shift tendencies. On a neural level, we observed increased gamma activity in the ACC, dmPFC, and OFC during encoding of precision-weighted prediction errors in HTA, accompanied by suppressed ACC alpha/beta activity. Our findings support the association between altered learning and belief updating in anxiety and changes in gamma and alpha/beta activity in the ACC, dmPFC, and OFC. Nature Publishing Group UK 2023-03-15 /pmc/articles/PMC10017780/ /pubmed/36922553 http://dx.doi.org/10.1038/s42003-023-04628-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hein, Thomas P.
Gong, Zheng
Ivanova, Marina
Fedele, Tommaso
Nikulin, Vadim
Herrojo Ruiz, Maria
Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title_full Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title_fullStr Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title_full_unstemmed Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title_short Anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
title_sort anterior cingulate and medial prefrontal cortex oscillations underlie learning alterations in trait anxiety in humans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10017780/
https://www.ncbi.nlm.nih.gov/pubmed/36922553
http://dx.doi.org/10.1038/s42003-023-04628-1
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