Item-specific memory reactivation supports overnight memory consolidation

Abstract Understanding how individual memory traces are reactivated during sleep is instrumental to the theorizing of memory consolidation, a process during which newly acquired information becomes stabilized and long-lasting. Via targeted memory reactivation (TMR), a technique that unobtrusively delivers learning-related memory cues to sleeping participants, we examined the reactivation of individual memories during slow-wave sleep and how canonical neural oscillations support item-specific memory reactivation. Furthermore, we investigated how pre-sleep testing, which presumably induces fast consolidation before sleep, would modulate sleep-mediated memory reactivation. Applying multivariate representational similarity analysis (RSA) to the cue-elicited electroencephalogram (EEG), we identified significant item-specific representations in two post-cue time windows (620-1350 ms and 2270-3190 ms) for post-sleep remembered items, with only the later item-specific representations contributing to memory consolidation. Untested items (i.e., items that were not tested pre-sleep), but not tested items, elicited higher spindles that predicted stronger item-specific representations and post-sleep memories. Notably, for untested items, the strengths of memory reactivation and spindles were temporally coupled to the up-state of the slow oscillation activity. Together, our results unveiled how item-specific memory reactivation and its link with neural oscillations during sleep contributed to memory consolidation. This knowledge will benefit future research aiming to perturb specific memory episodes during sleep.