Affective memory rehearsal with temporal sequences in amygdala neurons

Affective learning and memory are essential for daily behavior, with both adaptive and maladaptive learning depending on stimulus-evoked activity in the amygdala circuitry. Behavioral studies further suggest that post-association offline processing contributes to memory formation. Here we investigated spike sequences across simultaneously recorded neurons while monkeys learned to discriminate between aversive and pleasant tone-odor associations. We show that triplets of neurons exhibit consistent temporal sequences of spiking activity that differed from firing patterns of individual neurons and pairwise correlations. These sequences occurred throughout the long post-trial period, contained valence-related information, declined as learning progressed and were selectively present in activity evoked by the recent pairing of a conditioned stimulus with an unconditioned stimulus. Our findings reveal that temporal sequences across neurons in the primate amygdala serve as a coding mechanism and might aid memory formation through the rehearsal of the recently experienced association.