Dissociation of fear initiation and maintenance by breathing-driven prefrontal oscillations

Abstract

Does the body play an active role in emotions? Since the original James/Cannon controversy this debate has mainly been fueled by introspective accounts of human experience. Here, we use the animal model to demonstrate a physiological mechanism for bodily feedback and its causal role in the stabilization of emotional states. We report that during fear-related freezing mice breathe at 4Hz and show, using probabilistic modelling, that optogenetic perturbation of this feedback specifically reduces freezing maintenance without impacting its initiation. This rhythm is transmitted by the olfactory bulb to the prefrontal cortex where it organizes neural firing and optogenetic probing of the circuit demonstrates frequency-specific tuning that maximizes prefrontal cortex responsivity at 4Hz, the breathing frequency during freezing. These results point to a brain-body-brain loop in which the initiation of emotional behavior engenders somatic changes which then feedback to the cortex to directly participate in sustaining emotional states.