Amygdala-prefrontal synchronization underlies resistance to extinction of aversive memories

Emotional memories can persist for a lifetime but can also undergo extinction. Although we know about the mechanisms involved in expression and extinction, we know very little about the mechanisms that determine whether a specific memory would persist or not. Here, we use partial reinforcement extinction effect (PREE) to explore the neural mechanisms that differentiate persistent from labile memories. We recorded the simultaneous activity of neurons in the amygdala and the dorsal anterior cingulate cortex (dACC) while monkeys engaged in tone-odor aversive conditioning. We report that under continuous reinforcement schedule (ConS), activity in the amygdala precedes behavioral response, whereas under partial schedule (ParS), dACC activity precedes it. Moreover, we find that ParS induced cross-regional pairwise correlations throughout the entire acquisition session, and their magnitude and precision predicted the later resistance to extinction. Our results suggest that memory persistence depends on distributed representations and, specifically, resistance to extinction of aversive memories is maintained by correlated amygdala-dACC activity.