Sleep-related motor skill consolidation and generalizability after physical practice, motor imagery, and action observation

Conessa, Adrien; Debarnot, Ursula; Siegler, Isabelle; Boutin, Arnaud

doi:10.1016/j.isci.2023.107314

Cited by 3 publications

(2 citation statements)

References 86 publications

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“…A large body of research has provided substantial evidence that sleep, and spindles in particular, facilitates neuroplasticity and the associated consolidation of both declarative and motor memories [19,41]. Recent empirical research and theoretical frameworks have also outlined the essential contribution of the clustering and hierarchical rhythmicity of sleep spindle activity in the memory consolidation process [9,14,16], especially during NREM2 sleep when it relates to the consolidation of a newly learned motor skill [5,7,13,37]. The present results thus confirm the positive effects of NREM2 sleep spindles in the consolidation of motor sequences.…”

Section: Discussionsupporting

confidence: 89%

“…However, the post hoc analysis failed to detect significant changes in performance from the test to the retest (M Test = 302 and M Retest = 284, p = 0.18), thus revealing a sleep-based stabilization rather than an enhancement of the consolidated memory [36]. At the group level, the absence of delayed performance changes over the retention interval may be due to the non-averaging of performance blocks during training and testing sessions, since block averaging is known to be a confounding factor that accounts for, and further exacerbates, the offline gains [10,37]. Figure 1b,d (left panel) depicts the grand average TF maps zoomed in on epoch windows of ±6 s around spindle onsets during NREM2 and NREM3 sleep periods, respectively.…”

Section: Results (A) Behavioural Performancesupporting

confidence: 71%

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Temporal cluster-based organization of sleep spindles underlies motor memory consolidation

Boutin,

Gabitov,

Pinsard

et al. 2024

Proc. R. Soc. B.

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Sleep benefits motor memory consolidation, which is mediated by sleep spindle activity and associated memory reactivations during non-rapid eye movement (NREM) sleep. However, the particular role of NREM2 and NREM3 sleep spindles and the mechanisms triggering this memory consolidation process remain unclear. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEG-fMRI) recordings were collected during night-time sleep following the learning of a motor sequence task. Adopting a time-based clustering approach, we provide evidence that spindles iteratively occur within clustered and temporally organized patterns during both NREM2 and NREM3 sleep. However, the clustering of spindles in trains is related to motor memory consolidation during NREM2 sleep only. Altogether, our findings suggest that spindles' clustering and rhythmic occurrence during NREM2 sleep may serve as an intrinsic rhythmic sleep mechanism for the timed reactivation and subsequent consolidation of motor memories, through synchronized oscillatory activity within a subcortical–cortical network involved during learning.

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Section: Discussionsupporting

confidence: 89%

Section: Results (A) Behavioural Performancesupporting

confidence: 71%

Temporal cluster-based organization of sleep spindles underlies motor memory consolidation

Boutin,

Gabitov,

Pinsard

et al. 2024

Proc. R. Soc. B.

Self Cite

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Across-task binding: The development of a representation in learning a continuous movement sequence

Panzer,

Pfeifer,

Daniel

et al. 2024

Human Movement Science

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Brain plasticity underlying sleep-dependent motor consolidation after motor imagery

Di Rienzo,

Debarnot,

Daligault

et al. 2023

Cerebral Cortex

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Motor imagery can, similarly to physical practice, improve motor performance through experience-based plasticity. Using magnetoencephalography, we investigated changes in brain activity associated with offline consolidation of motor sequence learning through physical practice or motor imagery. After an initial training session with either physical practice or motor imagery, participants underwent overnight consolidation. As control condition, participants underwent wake-related consolidation after training with motor imagery. Behavioral analyses revealed that overnight consolidation of motor learning through motor imagery outperformed wake-related consolidation (95% CI [0.02, 0.07], P < 0.001, RP2 = 0.05). As regions of interest, we selected the generators of event-related synchronization/desynchronization of alpha (8–12 Hz) and beta (15–30 Hz) oscillations, which predicted the level of performance on the motor sequence. This yielded a primary sensorimotor-premotor network for alpha oscillations and a cortico-cerebellar network for beta oscillations. The alpha network exhibited increased neural desynchronization after overnight consolidation compared to wake-related consolidation. By contrast, the beta network exhibited an increase in neural synchronization after wake-related consolidation compared to overnight consolidation. We provide the first evidence of parallel brain plasticity underlying behavioral changes associated with sleep-dependent consolidation of motor skill learning through motor imagery and physical practice.

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Sleep-related motor skill consolidation and generalizability after physical practice, motor imagery, and action observation

Cited by 3 publications

References 86 publications

Temporal cluster-based organization of sleep spindles underlies motor memory consolidation

Temporal cluster-based organization of sleep spindles underlies motor memory consolidation

Across-task binding: The development of a representation in learning a continuous movement sequence

Brain plasticity underlying sleep-dependent motor consolidation after motor imagery

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