Persistence of amygdala gamma oscillations during extinction learning predicts spontaneous fear recovery

Abstract

Extinction of auditory fear conditioning induces a temporary inhibition of conditioned fear responses that can spontaneously reappear with the passage of time. Several lines of evidence indicate that extinction learning relies on the recruitment of specific neuronal populations within the basolateral amygdala. In contrast, post-extinction spontaneous fear recovery is thought to result from deficits in the consolidation of extinction memory within prefrontal neuronal circuits. Interestingly, recent data indicates that the strength of gamma oscillations in the basolateral amygdala during auditory fear conditioning correlates with retrieval of conditioned fear responses. In the present manuscript we evaluated the hypothesis that post-extinction spontaneous fear recovery might depend on the maintenance of gamma oscillations within the basolateral amygdala by using single unit and local field potential recordings in behaving mice. Our results indicate that gamma oscillations in the basolateral amygdala were enhanced following fear conditioning, whereas during extinction learning gamma profiles were more heterogeneous despite similar extinction learning rates. Remarkably, variations in the strength of gamma power within the basolateral amygdala between early and late stages of extinction linearly predicted the level of post-extinction spontaneous fear recovery. These data suggest that maintenance of gamma oscillations in the basolateral amygdala during extinction learning is a strong predictive factor of long term spontaneous fear recovery.