Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Bagur, Sophie, Lefort, Julie M., Lacroix, Marie M., de Lavilléon, Gaëtan, Herry, Cyril, Chouvaeff, Mathilde, Billand, Clara, Geoffroy, Hélène, Benchenane, Karim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
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
_version_ 1783690315473879040
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
work_keys_str_mv AT bagursophie breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT lefortjuliem breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT lacroixmariem breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT delavilleongaetan breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT herrycyril breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT chouvaeffmathilde breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT billandclara breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT geoffroyhelene breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation
AT benchenanekarim breathingdrivenprefrontaloscillationsregulatemaintenanceofconditionedfearevokedfreezingindependentlyofinitiation