Scalp EEG detects motor sequence replay signatures during wakeful rest

Abstract

Brief wakeful rest may support motor-memory processing through replay of recently practiced neural sequences, but human motor replay has been demonstrated mainly with invasive recordings or magnetoencephalography. Here we tested whether ordered motor-sequence replay can be detected from scalp EEG across wakeful rest during motor skill learning. During rest, participants received no cue, regular or accelerated auditory targeted-memory reactivation (TMR), or randomized tones. Neural states re-emerged in the practiced sequence order, revealing forward replay across conditions. Accelerated TMR enhanced total learning; within this condition, stronger forward replay showed the clearest exploratory relationship with micro-offline gains, while forward and reverse replay also covaried with gains across the cohort. The apparent replay timescale shifted systematically with decoder temporal resolution, showing that measured timing reflects both neural dynamics and the observation model. These findings support scalp EEG as a scalable approach for studying ordered motor-sequence reactivation during wakeful rest.