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Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex

Anxious individuals consistently fail in controlling emotional behavior, leading to excessive avoidance, a trait that prevents learning through exposure. Although the origin of this failure is unclear, one candidate system involves control of emotional actions, coordinated through lateral frontopola...

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Autores principales: Bramson, Bob, Meijer, Sjoerd, van Nuland, Annelies, Toni, Ivan, Roelofs, Karin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10423291/
https://www.ncbi.nlm.nih.gov/pubmed/37573436
http://dx.doi.org/10.1038/s41467-023-40666-3
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author Bramson, Bob
Meijer, Sjoerd
van Nuland, Annelies
Toni, Ivan
Roelofs, Karin
author_facet Bramson, Bob
Meijer, Sjoerd
van Nuland, Annelies
Toni, Ivan
Roelofs, Karin
author_sort Bramson, Bob
collection PubMed
description Anxious individuals consistently fail in controlling emotional behavior, leading to excessive avoidance, a trait that prevents learning through exposure. Although the origin of this failure is unclear, one candidate system involves control of emotional actions, coordinated through lateral frontopolar cortex (FPl) via amygdala and sensorimotor connections. Using structural, functional, and neurochemical evidence, we show how FPl-based emotional action control fails in highly-anxious individuals. Their FPl is overexcitable, as indexed by GABA/glutamate ratio at rest, and receives stronger amygdalofugal projections than non-anxious male participants. Yet, high-anxious individuals fail to recruit FPl during emotional action control, relying instead on dorsolateral and medial prefrontal areas. This functional anatomical shift is proportional to FPl excitability and amygdalofugal projections strength. The findings characterize circuit-level vulnerabilities in anxious individuals, showing that even mild emotional challenges can saturate FPl neural range, leading to a neural bottleneck in the control of emotional action tendencies.
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spelling pubmed-104232912023-08-14 Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex Bramson, Bob Meijer, Sjoerd van Nuland, Annelies Toni, Ivan Roelofs, Karin Nat Commun Article Anxious individuals consistently fail in controlling emotional behavior, leading to excessive avoidance, a trait that prevents learning through exposure. Although the origin of this failure is unclear, one candidate system involves control of emotional actions, coordinated through lateral frontopolar cortex (FPl) via amygdala and sensorimotor connections. Using structural, functional, and neurochemical evidence, we show how FPl-based emotional action control fails in highly-anxious individuals. Their FPl is overexcitable, as indexed by GABA/glutamate ratio at rest, and receives stronger amygdalofugal projections than non-anxious male participants. Yet, high-anxious individuals fail to recruit FPl during emotional action control, relying instead on dorsolateral and medial prefrontal areas. This functional anatomical shift is proportional to FPl excitability and amygdalofugal projections strength. The findings characterize circuit-level vulnerabilities in anxious individuals, showing that even mild emotional challenges can saturate FPl neural range, leading to a neural bottleneck in the control of emotional action tendencies. Nature Publishing Group UK 2023-08-12 /pmc/articles/PMC10423291/ /pubmed/37573436 http://dx.doi.org/10.1038/s41467-023-40666-3 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
Bramson, Bob
Meijer, Sjoerd
van Nuland, Annelies
Toni, Ivan
Roelofs, Karin
Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title_full Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title_fullStr Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title_full_unstemmed Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title_short Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
title_sort anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10423291/
https://www.ncbi.nlm.nih.gov/pubmed/37573436
http://dx.doi.org/10.1038/s41467-023-40666-3
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