Consolidation of human skill linked to waking hippocampo-neocortical replay

SummaryThe 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 highly prominent, fast waking neural replay during the same rest periods in which rapid consolidation occurs. The observed replay was temporally compressed by approximately 20x relative to the acquired skill, occurred in both forward and reverse directions, was selective for the trained sequence and predicted the magnitude of skill consolidation. Replay representations extended beyond the hippocampus and entrorhinal cortex to the contralateral sensorimotor cortex. These results document the presence of robust hippocampo-neocortical replay supporting rapid wakeful consolidation of skill.