Recent studies from us and others suggest that traditionally declarative structures mediate some aspects of the encoding and consolidation of procedural memories. This evidence points to the existence of converging physiological pathways across memory systems. Here, we examined whether the coupling between slow oscillations (SO) and spindles, a mechanism well established in the consolidation of declarative memories, is relevant for the stabilization of human motor memories. To this aim, we conducted an electroencephalography study in which we quantified various parameters of these oscillations during a night of sleep that took place immediately after learning a visuomotor adaptation (VMA) task. We found that VMA increased the overall density of fast (≥12 Hz), but not slow (<12 Hz), spindles during nonrapid eye movement sleep, stage 3 (NREM3). This modulation occurred rather locally over the hemisphere contralateral to the trained hand. Although adaptation learning did not affect the density of SOs, it substantially enhanced the number of fast spindles locked to the active phase of SOs. The fact that only coupled spindles predicted overnight memory retention points to the relevance of this association in motor memory consolidation. Our work provides evidence in favor of a common mechanism at the basis of the stabilization of declarative and motor memories.

Sleep spindles are thought to promote memory consolidation. Recently, we have shown that visuomotor adaptation (VMA) learning increases the density of spindles and promotes the coupling between spindles and slow oscillations, locally, with the level of spindle-SO synchrony predicting overnight memory retention. Yet, growing evidence suggests that the rhythmicity in spindle occurrence may also influence the stabilization of declarative and procedural memories. Here, we examined if VMA learning promotes the temporal organization of sleep spindles into trains. We found that VMA increased the proportion of spindles and spindle-SO couplings in trains. In agreement with our previous work, this modulation was observed over the contralateral hemisphere to the trained hand, and predicted overnight memory retention. Interestingly, spindles grouped in a cluster showed greater amplitude and duration than isolated spindles. The fact that these features increased as a function of train length, provides evidence supporting a biological advantage of this temporal arrangement. Our work opens the possibility that the periodicity of NREM oscillations may be relevant in the stabilization of procedural memories.

Abstract-

The precise coupling between slow oscillations (SO) and spindles is critical for sleep-dependent consolidation of declarative memories. Here, we examined whether this mechanism also operates in the stabilization of human motor memories during NREM sleep. We hypothesized that if the coupling of these oscillations is instrumental to motor memory consolidation then only SO-coupled spindles would predict long-term memory. We found that sleep enhanced long-term memory retention by 34%. Motor learning increased the density of spindles but not their frequency, duration or amplitude during NREM sleep. This modulation was manifested locally over the hemisphere contralateral to the trained hand. Although motor learning did not affect the density of SOs, it substantially modulated the spindle-SO coupling in an inter-hemispheric manner, suggesting it may rather increase the ability of slow oscillations to promote thalamic spindles. The fact that only coupled spindles predicted long-term memory points to the association of these oscillations as a fundamental signature of motor memory consolidation. Our work provides evidence in favor of a common mechanism at the basis of the stabilization of declarative and non-declarative memories.

Sleep spindles are thought to promote memory consolidation. Recently, we have shown that visuomotor adaptation (VMA) learning increases the density of spindles and promotes the coupling between spindles and slow oscillations, locally, with the level of spindle-SO synchrony predicting overnight memory retention. Yet, growing evidence suggests that the rhythmicity in spindle occurrence may also influence the stabilization of declarative and procedural memories. Here, we examined if VMA learning promotes the temporal organization of sleep spindles into trains. We found that VMA increased the proportion of spindles and spindle-SO couplings in trains. In agreement with our previous work, this modulation was observed over the contralateral hemisphere to the trained hand, and predicted overnight memory retention. Interestingly, spindles grouped in a cluster showed greater amplitude and duration than isolated spindles. The fact that these features increased as a function of train length, provides evidence supporting a biological advantage of this temporal arrangement. Our work opens the possibility that the periodicity of NREM oscillations may be relevant in the stabilization of procedural memories.CONTRIBUTION STATEMENTEver since the discovery of memory systems, the study of the mechanisms supporting the consolidation of declarative and procedural memories has progressed somewhat in parallel. We now know, however, that structures originally thought of as purely declarative such as the hippocampus, participate in the consolidation of procedural tasks. Recently, we showed that sleep predicts long-term motor memory through the local synchrony between fast sleep spindles and slow oscillations, a mechanism initially described for the consolidation of declarative memories. Novel evidence has linked the rhythmicity in the occurrence of spindles to memory stabilization. This framework proposes that temporally clustered spindles into trains of two or more separated by 3-6 seconds, may favor the reinstatement and subsequent reprocessing of previously acquired memories. This temporal arrangement may facilitate mnemonic replay and neocortical integration. In the present study, we show that motor learning promotes the organization of spindles into trains, locally, over the contralateral hemisphere, and that this modulation predicts overnight memory retention. Spindle grouping also augmented the proportion of spindle-SO couplings in trains. Importantly, spindles in a cluster increased their duration and amplitude as a function of train length, pointing to a physiological benefit of this temporal organization.