To test this hypothesis, we recorded simultaneous LFPs in the BLA, mPFC, ventral HPC (vHPC), and dorsal HPC (dHPC), and unit activity in the BLA, during a discriminative fear conditioning paradigm. In the BLA, two distinct bands of gamma-frequency activity were coupled to local theta oscillations, and this theta-gamma modulation was enhanced during fear recall. Surprisingly, though local theta-gamma coupling was weaker during epochs of reduced freezing, power in the fast gamma band (70-120 Hz) was enhanced and reflected an increase in synchronized firing of BLA units. Fast gamma dynamically switched its coupling with behavior, coupling to BLA theta during fear expression (presentation of a CS+), and mPFC theta during safety (presentation of a CS−). We further explored this fast gamma frequency oscillation as a putative safety signal following fear extinction, and in the open field test of innate anxiety. Consistent with a role in safety, the power of this signal was enhanced and associated with a predominant mPFC-to-BLA directionality both following extinction training and in the periphery of the open field. This pattern reflects an enhanced mPFC theta lead over BLA activity, suggesting that synchronization of BLA gamma to mPFC theta is a general mechanism for fear suppression.
