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.
Highlights
Brain–body interactions are thought to be essential in emotions but their physiological basis remains poorly understood
In this study we have shown that freezing is associated with regular 4 Hz breathing in mice and that this rhythm, via the olfactory bulb (OB), feeds back to the dorsomedial prefrontal cortex (dmPFC) where it organizes neuronal activity
We found that the OB respiratory rhythm is transmitted to the dmPFC, as shown in previous studies[12,23]
Summary
Brain–body interactions are thought to be essential in emotions but their physiological basis remains poorly understood. 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 shed light on the historical James–Cannon debate. Numerous lines of evidence suggest that the respiratory rhythm is principally relayed to these structures via the olfactory bulb (OB)[9,12,16] somatosensation could be involved[14] This rhythm is originally generated in the brainstem[20] which induces muscular movement and causes air to flow through the nose. In the prefrontal cortex (PFC), in the dorsomedial region (dmPFC), a strong 4 Hz oscillation has been identified during freezing[25,26] This rhythm organizes neural activity within this structure and with the amygdala.
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