Consolidation of human skill linked to waking hippocampo-neocortical replay

The introduction of rest intervals interspersed with practice strengthens wakeful consolidation of skill. The mechanisms by which the brain binds discrete action representations into consolidated, highly temporally resolved skill sequences during waking rest are not known. To address this question, we recorded magnetoencephalography (MEG) during acquisition and rapid consolidation of a sequential motor skill. We report the presence of prominent, fast waking neural replay during the same rest periods in which rapid consolidation occurs. The observed replay is temporally compressed by approximately 20-fold relative to the acquired skill, is selective for the trained sequence, and predicts the magnitude of skill consolidation. Replay representations extend beyond the hippocampus and entorhinal cortex to the contralateral sensorimotor cortex. These results document the presence of robust hippocampo-neocortical replay supporting rapid wakeful consolidation of skill. [Display omitted] •Waking replay bursts occur during short rest periods interspersed with practice•Replay is temporally compressed by approximately 20-fold relative to the practiced skill•Replay activity is distributed across the hippocampus and neocortex•Replay rates correlate with rapid wakeful skill consolidation in individuals Substantial jumps in performance immediately following short rest periods account for early motor skill learning. In this study, Buch et al. report waking hippocampo-neocortical replay during these rest periods that is temporally compressed by 20-fold relative to behavior, selective for the trained skill, and predicts the magnitude of rapid consolidation of skill.