Temporal clustering of sleep spindles and coupling with slow oscillations in the consolidation and generalization of motor memory

Abstract

Sleep benefits memory consolidation through periodic sleep spindle activity and associated memory reactivations. Recent evidence highlights that iterative spindle onsets follow two periodic rhythms: an infraslow periodicity ([~]0.02 Hz) and a mesoscale periodicity rhythm ([~]0.2-0.3 Hz). Consequently, spindles tend to cluster in "trains" on a low-frequency time scale every 50 seconds during which spindles iterate every 3 to 4 seconds. Such temporal organization of spindles in trains is considered a critical sleep mechanism for the timed and repeated reactivation of memories. Additionally, current trends indicate that a timely phase-locking between slow oscillations (SO) and spindles promotes learning-related synaptic plasticity. In this study, we explored how spindle clustering and coupling with SO contribute to motor memory consolidation by inducing a local reduction in synaptic efficacy over sensorimotor cortical regions through upper-limb immobilization after motor sequence learning. We also evaluated memory generalization using two transfer tests designed to assess the ability to transfer or generalize the newly acquired skill to another one (new sequence) or another effector (inter-limb transfer). Our results reveal that the temporal cluster-based organization of spindles is independent of daytime sensorimotor experience, while distinct overnight behavioral outcomes were elicited. Interestingly, immobilization induced a phase shift in the SO-spindle coupling for spindles grouped in trains, but not when isolated outside trains. In addition, the proportion of grouped spindles relative to isolated spindles was positively associated with skill consolidation and negatively correlated with skill generalization following sensorimotor restriction. These results suggest that spindle trains may promote skill-specific strengthening of motor memories, while isolated spindles may instead create memory-instability conditions that facilitate skill generalization.