Literature DB >> 33972521

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

Sophie Bagur1, Julie M Lefort2, Marie M Lacroix2, Gaëtan de Lavilléon2, Cyril Herry3,4, Mathilde Chouvaeff2, Clara Billand2, Hélène Geoffroy2, Karim Benchenane5.   

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.

Entities:  

Year:  2021        PMID: 33972521     DOI: 10.1038/s41467-021-22798-6

Source DB:  PubMed          Journal:  Nat Commun        ISSN: 2041-1723            Impact factor:   14.919


  57 in total

1.  Hippocampal activity, olfaction, and sniffing: an olfactory input to the dentate gyrus.

Authors:  C H Vanderwolf
Journal:  Brain Res       Date:  1992-10-16       Impact factor: 3.252

Review 2.  Autonomic nervous system activity in emotion: a review.

Authors:  Sylvia D Kreibig
Journal:  Biol Psychol       Date:  2010-04-04       Impact factor: 3.251

3.  Rapid and precise control of sniffing during olfactory discrimination in rats.

Authors:  Adam Kepecs; Naoshige Uchida; Zachary F Mainen
Journal:  J Neurophysiol       Date:  2007-04-25       Impact factor: 2.714

Review 4.  Pontine mechanisms of respiratory control.

Authors:  Mathias Dutschmann; Thomas E Dick
Journal:  Compr Physiol       Date:  2012-10       Impact factor: 9.090

Review 5.  Breathing rhythms and emotions.

Authors:  Ikuo Homma; Yuri Masaoka
Journal:  Exp Physiol       Date:  2008-05-16       Impact factor: 2.969

6.  Slow oscillations in the mouse hippocampus entrained by nasal respiration.

Authors:  Yevgenij Yanovsky; Mareva Ciatipis; Andreas Draguhn; Adriano B L Tort; Jurij Brankačk
Journal:  J Neurosci       Date:  2014-04-23       Impact factor: 6.167

Review 7.  Respiration-Entrained Brain Rhythms Are Global but Often Overlooked.

Authors:  Adriano B L Tort; Jurij Brankačk; Andreas Draguhn
Journal:  Trends Neurosci       Date:  2018-02-09       Impact factor: 13.837

8.  Variable coupling between olfactory system activity and respiration in ketamine/xylazine anesthetized rats.

Authors:  Alfredo Fontanini; James M Bower
Journal:  J Neurophysiol       Date:  2005-02-02       Impact factor: 2.714

Review 9.  The respiratory-vocal system of songbirds: anatomy, physiology, and neural control.

Authors:  Marc F Schmidt; J Martin Wild
Journal:  Prog Brain Res       Date:  2014       Impact factor: 2.453

10.  Hippocampal Respiration-Driven Rhythm Distinct from Theta Oscillations in Awake Mice.

Authors:  Vivan Nguyen Chi; Carola Müller; Thérèse Wolfenstetter; Yevgenij Yanovsky; Andreas Draguhn; Adriano B L Tort; Jurij Brankačk
Journal:  J Neurosci       Date:  2016-01-06       Impact factor: 6.167

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  10 in total

Review 1.  Controlling neuronal assemblies: a fundamental function of respiration-related brain oscillations in neuronal networks.

Authors:  Shani Folschweiller; Jonas-Frederic Sauer
Journal:  Pflugers Arch       Date:  2022-05-31       Impact factor: 3.657

Review 2.  Freezing revisited: coordinated autonomic and central optimization of threat coping.

Authors:  Karin Roelofs; Peter Dayan
Journal:  Nat Rev Neurosci       Date:  2022-06-27       Impact factor: 38.755

3.  Breathing modulates gamma synchronization across species.

Authors:  Joaquín González; Matias Cavelli; Alejandra Mondino; Santiago Castro-Zaballa; Jurij Brankačk; Andreas Draguhn; Pablo Torterolo; Adriano B L Tort
Journal:  Pflugers Arch       Date:  2022-10-03       Impact factor: 4.458

Review 4.  Olfactory modulation of the medial prefrontal cortex circuitry: Implications for social cognition.

Authors:  Janardhan P Bhattarai; Semra Etyemez; Hanna Jaaro-Peled; Emma Janke; Usuy D Leon Tolosa; Atsushi Kamiya; Jay A Gottfried; Akira Sawa; Minghong Ma
Journal:  Semin Cell Dev Biol       Date:  2021-05-09       Impact factor: 7.499

Review 5.  Respiration-Driven Brain Oscillations in Emotional Cognition.

Authors:  Shani Folschweiller; Jonas-Frederic Sauer
Journal:  Front Neural Circuits       Date:  2021-10-27       Impact factor: 3.492

6.  Discriminating Sleep From Freezing With Cortical Spindle Oscillations.

Authors:  Marco N Pompili; Ralitsa Todorova
Journal:  Front Neural Circuits       Date:  2022-03-24       Impact factor: 3.492

Review 7.  Breaking Down a Rhythm: Dissecting the Mechanisms Underlying Task-Related Neural Oscillations.

Authors:  Inés Ibarra-Lecue; Saskia Haegens; Alexander Z Harris
Journal:  Front Neural Circuits       Date:  2022-03-04       Impact factor: 3.492

8.  Testing Emotional Vulnerability to Threat in Adults Using a Virtual Reality Paradigm of Fear Associated With Autonomic Variables.

Authors:  Marcus L Brandão; Manoel Jorge Nobre; Ruth Estevão
Journal:  Front Psychiatry       Date:  2022-04-01       Impact factor: 4.157

Review 9.  Neural Oscillations in Aversively Motivated Behavior.

Authors:  Michael S Totty; Stephen Maren
Journal:  Front Behav Neurosci       Date:  2022-07-01       Impact factor: 3.617

10.  Effect of Sensory Deprivation of Nasal Respiratory on Behavior of C57BL/6J Mice.

Authors:  Yongji Zhu; Yujing Ye; Chenyang Zhou; Siqi Sun; Jingjing Zhang; Zixuan Zhao; Tingting Sun; Jing Li; Jing Yang; Weiyun Li; Shanshan Li
Journal:  Brain Sci       Date:  2021-12-09
  10 in total

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