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

Abstract

Sleep benefits the consolidation of motor skills learned by physical practice, mainly through periodic thalamocortical sleep spindle activity. However, motor skills can be learned without overt movement through motor imagery or action observation. Here, we investigated whether sleep spindle activity also supports the consolidation of non-physically learned movements. Forty-five electroencephalographic sleep recordings were collected during a daytime nap after motor sequence learning by physical practice, motor imagery, or action observation. Our findings reveal that a temporal cluster-based organization of sleep spindles underlies motor memory consolidation in all groups, albeit with distinct behavioral outcomes. A daytime nap offers an early sleep window promoting the retention of motor skills learned by physical practice and motor imagery, and its generalizability toward the inter-manual transfer of skill after action observation. Findings may further have practical impacts with the development of non-physical rehabilitation interventions for patients having to remaster skills following peripherical or brain injury.

Keywords: Health sciences; Medical imaging; Medicine; Neurology.

Graphical abstract

Figure 1

Experimental design Participants (n = 45) were trained on a 5-element finger movement sequence either by physical practice (PP), motor imagery (MI) or action observation (AO). Sleep EEG recordings were acquired during a 90-min daytime nap following training. Participants were subsequently tested on the same motor sequence during retention and inter-manual transfer tests. During the pre-test, post-test, retention and transfer tests, all participants were required to physically performed the motor sequence. EEG: Electroencephalography.

Figure 2

Behavioral results Performance changes (in percentages) on the motor sequence task during acquisition (from the pre-test to the post-test), sleep-related skill consolidation (from the post-test to the retention test), and inter-manual skill transfer (from the retention test to the transfer test) for each of the physical practice (PP; n = 15), motor imagery (MI; n = 15) and action observation (AO; n = 15) groups. The curved lines indicate the distribution of data, the dark bars represent the mean of the distribution, and the lighter area surrounding the mean represent the standard error of the means. Individual data points are displayed as colored circles. ∗p < 0.05, ∗∗p < 0.01 in a one-way ANOVA test.

Figure 3

Sleep spindles in relation with motor skill consolidation and transfer (A) Relationship between skill consolidation (percentage of performance changes across the sleep retention interval, from the post-test to the retention test) and the total number of NREM2 spindles for each of the physical practice (PP; n = 15), motor imagery (MI; n = 15) and action observation (AO; n = 15) groups. (B) Relationship between skill transfer (percentage of performance changes from the retention test to the inter-manual transfer test) and the total number of NREM2 spindles for each practice group. Scatterplots and linear trend-lines are provided. Pearson correlation coefficients (r) and associated p values are reported for each correlation.

Figure 4

Sleep-related motor skill consolidation and transfer following physical practice, motor imagery and action observation Upper row. Graphical illustration of the relationship between the magnitude of skill consolidation (percentage of performance changes across the sleep retention interval, from the post-test to the retention test) and the total number of grouped (lighter points) or isolated spindles (darker points) in the (A) physical practice (red; n = 15), (B) motor imagery (blue; n = 15), and (C) action observation (green; n = 15) groups. Lower row. Graphical illustration of the relationship between the magnitude of skill transfer (percentage of performance changes from the retention to the inter-manual transfer test) and the total number of grouped (lighter points) or isolated spindles (darker points) in the (D) physical practice (red; n = 15), (E) motor imagery (blue; n = 15), and (F) action observation (green; n = 15) groups. Scatterplots and linear trend-lines are provided. Pearson correlation coefficients (r) and associated p values are reported for each correlation.

Figure 5

Time-frequency decomposition of NREM2 sleep spindles following physical practice, motor imagery and action observation Grand average time-frequency maps across participants for spindle events occurring at scalp electrode Pz, using epoch windows ranging from −6 s to +6 s around spindle onsets, and illustrating the 0.2–0.3 Hz spindle rhythmicity within trains during NREM2 sleep periods following (A) physical practice (left panel; n = 15), (B) motor imagery (middle panel; n = 15) and (C) action observation (right panel; n = 15). The color bar reflects normalized (1/f compensation) spectral power values (μV²). Contour lines indicate regions where power is significantly higher than the baseline (−2 s to −0.5 s) for each frequency bin after two-tailed Student’s t test corrected for multiple comparisons using the Benjamini-Hochberg procedure to control the false discovery rate (Ntest = 60020). NREM: Non-Rapid Eye Movement.