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Cited by 131Memory and Neural MechanismsNeural dynamics and brain functionNeuroscience of respiration and sleep

Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation

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Bagur, Sophie, Lefort, Julie M., Lacroix, Marie M., de Lavilléon, Gaëtan, Herry, Cyril, Chouvaeff, Mathilde, Billand, Clara, Geoffroy, Hélène +1 more·2021·Nature Communications
DOI 10.1038/s41467-021-22798-6PMC PMC8110519

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Abstract

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.

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  • Respiration also modulates neural activity in medial prefrontal cortex in rodents.

    “Respiration also modulates neural activity in medial prefrontal cortex in rodents 130,133-135 ,”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [134]

  • The coupling between nasal respiration and neural activity in limbic regions is associated with the modulation of memory performance and of emotional ratings in humans, and it influences freezing behavior in mice.

    “The coupling between nasal respiration and neural activity in limbic regions is also associated with the modulation of memory performance 120,138,139 and of emotional ratings in humans 120 , and it influences freezing behavior in mice 134,135 .”

    From Interoceptive rhythms in the brain (2023) · cites this paper as [134]

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Cited by

Sorted by citations

Authors
Bagur, S., Lefort, J. M., Lacroix, M. M., de Lavilléon, G., Herry, C., Chouvaeff, M., Billand, C., Geoffroy, H., & Benchenane, K.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Université de Bordeaux (FR)
Corresponding author
  • Bagur, Sophie
  • Benchenane, Karim
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2021-05-10
Volume
12
Issue
1
Pages
2605-2605
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-021-22798-6
PMC
PMC8110519
OpenAlex
W3162448660
Cited by
131
References
14
Citations by year
2026: 14 · 2025: 17 · 2024: 34 · 2023: 25 · 2022: 23 · 2021: 14 · 2020: 2 · 2019: 2
FWCI
12.62
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by-nc)
  • HAL (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion, cc-by)
Funders
  • Fondation pour la Recherche Médicale
  • Université de Recherche Paris Sciences et Lettres
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
Keywords
fear conditioning, freezing behavior, respiratory rhythm, olfactory bulb, dorsomedial prefrontal cortex, brain-body interaction, emotions, local field potentials, olfactory bulbectomy, optogenetics
MeSH terms
Action Potentials, Animals, Electrophysiology, Fear, Interneurons, Male, Markov Chains, Methimazole, Mice, Inbred C57BL, Models, Psychological, Olfactory Bulb, Periodicity, Respiration, Antithyroid Agents, Prefrontal Cortex, Pyramidal Cells, Mice, Optogenetics

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