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

Author

Listed:
  • Sophie Bagur

    (PSL University)

  • Julie M. Lefort

    (PSL University)

  • Marie M. Lacroix

    (PSL University)

  • Gaëtan Lavilléon

    (PSL University)

  • Cyril Herry

    (INSERM, Neurocentre Magendie
    University of Bordeaux, Neurocentre Magendie)

  • Mathilde Chouvaeff

    (PSL University)

  • Clara Billand

    (PSL University)

  • Hélène Geoffroy

    (PSL University)

  • Karim Benchenane

    (PSL University)

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.

Suggested Citation

  • Sophie Bagur & Julie M. Lefort & Marie M. Lacroix & Gaëtan Lavilléon & Cyril Herry & Mathilde Chouvaeff & Clara Billand & Hélène Geoffroy & Karim Benchenane, 2021. "Breathing-driven prefrontal oscillations regulate maintenance of conditioned-fear evoked freezing independently of initiation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-22798-6
    DOI: 10.1038/s41467-021-22798-6
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    Cited by:

    1. Michael S. Totty & Tuğçe Tuna & Karthik R. Ramanathan & Jingji Jin & Shaun E. Peters & Stephen Maren, 2023. "Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Jun Ma & John J. O’Malley & Malaz Kreiker & Yan Leng & Isbah Khan & Morgan Kindel & Mario A. Penzo, 2024. "Convergent direct and indirect cortical streams shape avoidance decisions in mice via the midline thalamus," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Jimena L. Frontera & Romain W. Sala & Ioana A. Georgescu & Hind Baba Aissa & Marion N. d’Almeida & Daniela Popa & Clément Léna, 2023. "The cerebellum regulates fear extinction through thalamo-prefrontal cortex interactions in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Joseph W. Arthurs & Anna J. Bowen & Richard D. Palmiter & Nathan A. Baertsch, 2023. "Parabrachial tachykinin1-expressing neurons involved in state-dependent breathing control," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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