Dynamic switching between distinct oscillatory rhythms in prefrontal-amygdala circuits across diverse behaviors under natural threats

Abstract

The prefrontal cortex and amygdala are involved in the regulation of defensive behavior under threat, but how they are engaged in flexible shift among behaviors remain unclear. Recent reports from the Pavlovian fear conditioning experiments have indicated that a long-range synchrony in the prefrontal-amygdala network is crucial for a representative type of defensive behavior, i.e., freezing; however, its role with respect to a vast repertoire of naturalistic threat-induced behaviors remains unknown. We used a predatory robot and investigated the rhythmic activities in the network of the prefrontal cortex (PFC) and basolateral amygdala (BLA) during natural behavior of mice. We found that mice exhibited freezing or flight in react to the threat of robot, and both regions increased low theta (3-7 Hz, PFC→BLA) during freezing, and high theta (8-14 Hz, BLA→PFC) and high beta (22-34 Hz, PFC→BLA) during flight. Similar to how freezing and flight cannot coexist, the coexistence of freeze- and flight-related oscillatory states in PFC-BLA network was rarely found. Trajectory analysis of flight showed that the prefrontal-to-amygdala beta bursts were prominent during flights with intention (e.g., flight towards the gate to the safe-zone) and suppressed but temporally coordinated fast gamma activities (60-120 Hz) in the amygdala, suggesting its role in the top-down processing. These results demonstrate a neurodynamic substrate of the prefrontal-amygdala circuits to freeze-or-flight under a naturalistic threat and provide a unified understanding of neural dynamics underlying flexible selection of behaviors.