Time-dependent neural arbitration between cue associative and episodic fear memories

Abstract

AbstractAfter traumatic events, simple cue-threat associative memories strengthen while episodic memories become fragmented. However, how the brain prioritizes cue associations over episodic coding of traumatic events remains unclear. Here, we developed a new episodic threat conditioning paradigm in which participants concurrently form two memory representations: cue associations and episodic cue sequence. We discovered that these two distinct memories compete for physiological fear expression, reorganizing overnight from an overgeneralized cue-based to a precise sequence-based expression. With multivariate fMRI, we track inter-area communication of the memory representations and demonstrate that a shift from hippocampal-dominant to prefrontal-dominant control of the fear regulatory circuit governs this memory maturation. Critically, this overnight reorganization is altered in individuals with heightened trait anxiety. Together, these findings suggest the brain prioritizes generalizable associative memories under recent traumatic stress, but resorts to selective episodic memories 24 hrs later. Time-dependent memory competition provides a unifying account for memory dysfunctions in posttraumatic stress disorders.