Memory boost for recurring emotional events is driven by initial amygdala response promoting stable neocortical patterns across repetitions.

Abstract

Emotionally arousing events are typically vividly remembered, which is generally adaptive but may contribute to mental disorders such as posttraumatic stress disorder. Previous research on emotional memory focused primarily on events that were experienced only once, leaving the memory mechanisms underlying repeatedly encountered emotional events largely unexplored. Here, we aimed to elucidate the brain mechanisms associated with memory for recurring emotional events. Specifically, we sought to determine whether the memory enhancement for recurring emotional events is linked to more variable neural representations, as predicted by the encoding-variability hypothesis, or to more stable representations across repetitions, as suggested by a memory reinstatement account. To investigate this, healthy men and women were repeatedly presented with images of emotionally negative or neutral scenes during three consecutive runs in an MRI scanner. Subsequent free recall was, as expected, enhanced for emotional compared to neutral images. Neural data showed that this emotional enhancement of memory was linked to (i) activation of the amygdala and anterior hippocampus during the initial encounter of the emotional event and (ii) increased neural pattern similarity in frontoparietal cortices across event repetitions. Most importantly, a multilevel moderated mediation analysis revealed that the impact of neocortical pattern stability across repetitions on emotional memory enhancement was moderated by amygdala activity during the initial exposure to the emotional event. Together, our findings show that the amygdala response during the initial encounter of an emotional event boosts subsequent remembering through a more precise reinstatement of the event representation during subsequent encounters of the same event.Significance statement Despite extensive research on emotional memory, the mechanisms underlying memory formation for recurrent emotional events remain elusive. We show that amygdala and anterior hippocampal activity is most prominent during the initial exposure to an aversive stimulus and decreases markedly with repeated exposure. Neocortical representation patterns of subsequently recalled emotional events, however, are more stable across the repeated encounters of emotional (vs. neutral) events, in line with a memory reinstatement account. Notably, this increased neocortical pattern stability was driven by the amygdala response during the initial exposure to an emotional event. These findings provide novel insights into the mechanisms involved in memory formation for recurrent emotional events, with potential implications for complex post-traumatic stress disorder characterized by multiple traumatic exposures.