Targeted memory reactivation elicits temporally compressed reactivation linked to spindles

Abstract Memories reactivate during sleep, however the properties of such reactivation and its relationship to encoding strength and subsequent memory performance are not well understood. We set out to examine memory reactivations associated with a serial reaction time task (SRTT). 48 human participants performed the SRTT, and then slept in the lab while we deliberately induced reactivation in Slow Wave Sleep (SWS) using a Targeted Memory Reactivation (TMR) design. We detected reactivation after TMR cues using multiclass classification that adapted to sleep data by using sleep activity for training and wake activity for testing. We then examined the temporal properties of reactivation in relation to behavioural performance and sleep spindles. In keeping with the rodent literature, the observed reactivation was 3 to 20 times faster than waking activity. Furthermore, we report an inverted-U shaped relationship between TMR-related behavioural improvement and encoding strength, with very strong and very weak memories benefiting little from cueing while medium-strength memories benefit the most. Finally, reactivation was more frequently observed in trials with high sigma power, supporting the idea that sleep spindles are associated with memory reactivation during sleep. These findings bring us closer to understanding the characteristics of human memory reactivation after TMR, demonstrate when cueing is effective, and provide evidence for the positive relationship between the detectability of reactivation and memory consolidation.