Offline cerebello-cortico-striatal dynamics predict motor strategy exploration and retention in skill learning

Abstract

Learning a motor skill requires exploring multiple possible solutions to find and retain an optimal strategy1-3. The exploration and consolidation of the motor strategy are usually considered to be segregated respectively between task practice and rest periods4-7. Here we show that two types of offline reactivations of neuronal representations of locomotor strategies in a brain-wide motor circuit are associated with exploration and retention. During short rests between trials, replays of these brainwide representations predict subsequent shifts in strategies indicating that distributed offline processes participate in strategy exploration. Shifts in strategy are consolidated, and their retention follows population reactivation in cerebellar sleep spindles and stabilization of cerebello-cerebral functional connectivity patterns, consistent with the role of spindles in brain plasticity. Overall, motor strategy optimization and consolidation are supported by two intertwined but distinct types of offline distributed reactivation events involving interregional interactions.