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Neural Traces of Forgotten Memories Persist in Humans and are Behaviorally Relevant

Tom WillemsiD, Konstantinos ZervasiD, Luzius BrogliiD, Finn RabeiD, Andrea FederspieliD, Katharina HenkeiD

Abstract

For a long time, forgetting has been taken as the dissipation of the neural memory traces (engrams). However, recent engram research in mice suggests that the engrams of forgotten memories do persist. This raises the question of whether engrams underlying human episodic memories also persist despite forgetting? And do forgotten memories influence human behavior implicitly? To address these questions, we used high-resolution functional magnetic resonance imaging at 7 Tesla to map the fate of 96 associative memories at the systems level from learning to a 30-minute and onward to a 24-hour memory test. Upon each retrieval attempt, participants indicated whether they remembered or forgot the memory. Univariate and multivariate analyses of the functional brain data revealed that the engrams of forgotten memories remain implemented in the episodic memory network and continue to influence the accuracy of guessing responses at the memory test. Overnight, the engrams of forgotten memories became implemented more deeply within bilateral hippocampus, while consciously accessible memories were neocorticalized overnight. The engrams of both consciously accessible and inaccessible (forgotten) memories shifted from the 30-minute to the 24-hour memory test within the right hippocampus and anterior cingulate gyrus as evidenced by the occurrence of pattern dissimilarities that supported correct retrieval responses at 24 hours. Hence, forgotten human episodic memories remain implemented in the episodic memory system and continue to influence decisions.

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