Neural reinstatement of encoding context mediates the switch between fear and extinction recall

Fear conditioning and extinction generate conflicting memory representations for a conditioned stimulus (CS). Retrieval of either memory is largely determined by the context where the CS is encountered. While fear typically generalizes to CSs encountered in new contexts, extinction is specific to the environment in which it was learned. Here we used an fMRI design (N = 30) to tag and track the extent which individual participants reinstated competing episodic mental contexts associated with threat conditioning and extinction. We examined whether reactivation of past encoding contexts influences threat expectancy behavior and neural responses to a threat-ambiguous CS encountered in a new context. Results showed that the relative balance between conditioning and extinction context reinstatement in higher-order visual cortex influenced threat expectancy and neural activity in canonical threat processing regions. The link between context reinstatement and fear-related processes was specific to an extinguished CS, as opposed to an unextinguished CS that had never been encountered in the extinction context. These effects were observed 24 hours later, but not after 3 weeks. Additionally, threat conditioning produced long-lasting changes in primary sensory cortex that persisted up to 3 weeks following extinction. These findings show that neural representations of threat can endure over long durations, even in the healthy brain. Our results indicate competition between divergent mental contexts determines feelings of danger or safety when the meaning of the CS is ambiguous, and suggest a mechanism by which the brain resolves ambiguity by reinstating the more dominant context associated with either fear or extinction.