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Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation
Brain–body interactions are thought to be essential in emotions but their physiological basis remains poorly understood. In mice, regular 4 Hz breathing appears during freezing after cue-fear conditioning. Here we show that the olfactory bulb (OB) transmits this rhythm to the dorsomedial prefrontal...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8110519/ https://www.ncbi.nlm.nih.gov/pubmed/33972521 http://dx.doi.org/10.1038/s41467-021-22798-6 |
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author | Bagur, Sophie Lefort, Julie M. Lacroix, Marie M. de Lavilléon, Gaëtan Herry, Cyril Chouvaeff, Mathilde Billand, Clara Geoffroy, Hélène Benchenane, Karim |
author_facet | Bagur, Sophie Lefort, Julie M. Lacroix, Marie M. de Lavilléon, Gaëtan Herry, Cyril Chouvaeff, Mathilde Billand, Clara Geoffroy, Hélène Benchenane, Karim |
author_sort | Bagur, Sophie |
collection | PubMed |
description | Brain–body interactions are thought to be essential in emotions but their physiological basis remains poorly understood. In mice, regular 4 Hz breathing appears during freezing after cue-fear conditioning. Here we show that the olfactory bulb (OB) transmits this rhythm to the dorsomedial prefrontal cortex (dmPFC) where it organizes neural activity. Reduction of the respiratory-related 4 Hz oscillation, via bulbectomy or optogenetic perturbation of the OB, reduces freezing. Behavioural modelling shows that this is due to a specific reduction in freezing maintenance without impacting its initiation, thus dissociating these two phenomena. dmPFC LFP and firing patterns support the region’s specific function in freezing maintenance. In particular, population analysis reveals that network activity tracks 4 Hz power dynamics during freezing and reaches a stable state at 4 Hz peak that lasts until freezing termination. These results provide a potential mechanism and a functional role for bodily feedback in emotions and therefore shed light on the historical James–Cannon debate. |
format | Online Article Text |
id | pubmed-8110519 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-81105192021-05-11 Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation Bagur, Sophie Lefort, Julie M. Lacroix, Marie M. de Lavilléon, Gaëtan Herry, Cyril Chouvaeff, Mathilde Billand, Clara Geoffroy, Hélène Benchenane, Karim Nat Commun Article Brain–body interactions are thought to be essential in emotions but their physiological basis remains poorly understood. In mice, regular 4 Hz breathing appears during freezing after cue-fear conditioning. Here we show that the olfactory bulb (OB) transmits this rhythm to the dorsomedial prefrontal cortex (dmPFC) where it organizes neural activity. Reduction of the respiratory-related 4 Hz oscillation, via bulbectomy or optogenetic perturbation of the OB, reduces freezing. Behavioural modelling shows that this is due to a specific reduction in freezing maintenance without impacting its initiation, thus dissociating these two phenomena. dmPFC LFP and firing patterns support the region’s specific function in freezing maintenance. In particular, population analysis reveals that network activity tracks 4 Hz power dynamics during freezing and reaches a stable state at 4 Hz peak that lasts until freezing termination. These results provide a potential mechanism and a functional role for bodily feedback in emotions and therefore shed light on the historical James–Cannon debate. Nature Publishing Group UK 2021-05-10 /pmc/articles/PMC8110519/ /pubmed/33972521 http://dx.doi.org/10.1038/s41467-021-22798-6 Text en © The Author(s) 2021 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 Bagur, Sophie Lefort, Julie M. Lacroix, Marie M. de Lavilléon, Gaëtan Herry, Cyril Chouvaeff, Mathilde Billand, Clara Geoffroy, Hélène Benchenane, Karim Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title | Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title_full | Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title_fullStr | Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title_full_unstemmed | Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title_short | Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
title_sort | breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8110519/ https://www.ncbi.nlm.nih.gov/pubmed/33972521 http://dx.doi.org/10.1038/s41467-021-22798-6 |
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