Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

Abstract

Emotion has a significant impact on how related experiences are organized into integrated memories. However, the neurobiological mechanisms of how emotion modulates memory integration for related information with different valences remain unclear. In this between-subject functional magnetic resonance imaging (fMRI) study, we investigated different emotional modulations of memory integration by manipulating the valence of stimuli used in an associative memory paradigm. Three groups of participants were tested: one group integrated emotional (i.e., negative) information with neutral information, one group integrated two emotional pieces of information, and one control group integrated two neutral pieces of information. Behaviorally, emotional information facilitated its integration with neutral information but interfered with the other emotional information. Neurally, the emotion-induced facilitation effect, occurring on memory integration of neutral and emotional information, was associated with increased trial-specific reactivation in the hippocampus during both encoding and retrieval. This facilitated integration was also supported by strengthened hippocampal connectivity with the amygdala, as well as a set of neocortical areas related to emotion regulation and the default mode network (DMN). In contrast, the emotion-induced interference effect, occurring on memory integration of two emotional pieces of information, was associated with impaired hippocampal trial-specific reactivation during retrieval that appeared to offset the facilitating effect of increased reactivation during encoding. Similar but relatively weak hippocampal connectivity was found underlying this interfered integration. Taken together, emotional information facilitates memory integration with neutral information, while disrupting the integration with other emotional information, through distinct dynamical processes of hippocampal trial-specific reactivation and connectivity.