Sleep Consolidation Potentiates Sensorimotor Adaptation

Abstract

Contrary to its well-established role in declarative learning, the impact of sleep on motor memory consolidation remains a subject of debate. Current literature suggests that while motor skill learning benefits from sleep, consolidation of sensorimotor adaptation (SMA) depends solely on the passage of time. This has led to the proposal that SMA may be an exception to other types of memories. Here, we addressed this ongoing controversy in humans through three comprehensive experiments using the visuomotor adaptation paradigm (N = 290, 150 females). In Experiment 1, we investigated the impact of sleep on memory retention when the temporal gap between training and sleep was not controlled. In line with the previous literature, we found that memory consolidates with the passage of time. In Experiment 2, we used an anterograde interference protocol to determine the time window during which SMA memory is most fragile and, thus, potentially most sensitive to sleep intervention. Our results show that memory is most vulnerable during the initial hour post-training. Building on this insight, in Experiment 3, we investigated the impact of sleep when it coincided with the critical first hour of memory consolidation. This manipulation unveiled a benefit of sleep (30% memory enhancement) alongside an increase in spindle density and spindle-SO coupling during NREM sleep, two well-established neural markers of sleep consolidation. Our findings reconcile seemingly conflicting perspectives on the active role of sleep in motor learning and point to common mechanisms at the basis of memory formation.

Keywords: EEG; consolidation; human; motor learning; sleep.

Figure 1.

Experimental paradigm and experimental design. a, VMA experimental paradigm. Subjects sat on a chair and performed center-out movements to one of eight visual targets displayed concentrically around the start point, using a cursor controlled with a joystick operated with their right dominant hand. One cycle was composed of eight trials (one per target), and one block was composed of 11 cycles. The vision of the hand was occluded. The inset depicts the visual display of the computer screen, illustrating the relationship between the hand manipulating the joystick (unseen) and the trajectory of the cursor (seen) during null trials (Baseline) and during early and late phases of adaptation to an optical CW rotation (α). b, Experimental design. Three experiments were conducted to address the aims of the study in which different sets of subjects trained on the VMA paradigm, and adapted to a CCW (A) and/or a CW (B) rotation. In Experiment 1, we assessed the effect of sleep when the temporal gap between training and bedtime was not controlled. Six different groups of participants trained on A (one block of null trials followed by six blocks of A) at different time points throughout the daytime (between 7 A.M. and 6 P.M.), and their memory retention was tested after a variable time interval post-learning: 15 min, 1 h, 3 h, 5.5 h, 9 h, or 24 h (note that only the 24 h group underwent a full night of sleep). In Experiment 2, we determined the optimal time window for sleep intervention in a controlled experimental setting. Four groups of participants underwent an anterograde interference protocol to determine the time course of memory consolidation and, thus, the time point at which the motor memory was most fragile. Subjects adapted sequentially to A and B, separated by either 5 min, 1 h, 6 h, or 24 h, and memory retention was assessed 24 h after training on B. A control group trained only on B. In Experiment 3, we assessed the effect of sleep when the temporal gap between training and bedtime was controlled based on the results of Experiment 2. Two groups of volunteers trained on B and polysomnographic EEG recordings were performed overnight. One group trained in the morning and thus slept outside the optimal time window (AM/AM), while the other group trained at night and went to sleep during the optimal time window (PM/PM). Memory retention in both groups was assessed 24 h after training. To control for a possible circadian effect due to the time of test, two additional groups were tested at the opposite circadian time (AM/PM and PM/AM).

Figure 2.

Experiment 1. Sleep does not benefit SMA when the temporal gap between training and bedtime is not controlled. a, Learning curves. Shown are the median ± SEM of the normalized pointing angle (in arbitrary units) during visuomotor adaptation for all six groups. b, Time course of memory retention. Memory retention was evaluated during the test session and expressed as % of learning. Shown are the mean ± SEM for each group and the individual data superimposed as dots. ***p < 0.001 indicates the result of the one-way ANOVA test across groups. c, Characterization of VMA memory decay. Shown is the individual level of memory retention displayed on b, where the abscissa scale represents the true time interval elapsed between the end of training and test (15 min through 9 h). Superimposed is the curve resulting from fitting a single exponential function: y(t) = a * exp(−b * t)+c, with a = 42.30%, b = 0.44 h⁻¹, and c = 40.97%. The dotted line represents the asymptote c. Memory decay stabilized ∼6 h after training. *p < 0.05; n.s., nonsignificance indicates the result of the t test between the 3 h and 5.5 h groups versus c adjusted for multiple comparisons based on Bonferroni. d, Effect of sleep on VMA memory retention. Shown is the mean ± SEM of memory retention for the group that underwent a full night of sleep (24 h group). The dashed line represents the asymptote of memory decay during wakefulness (c). No significant difference was observed between the level of retention attained after a night of sleep and c.

Figure 3.

Experiment 2. Time course of SMA memory consolidates during wake. a, Learning curves. Shown are the median ± SEM of the normalized pointing angle (in arbitrary units) for all groups as a function of the training session in which participants adapted sequentially to two opposing optical rotations (A followed by B) separated by one of four possible time intervals. In addition, a control group only adapted to B. b, Time course of memory retention. Memory retention was evaluated during the test session by quantifying the pointing angle through two error-clamp cycles, expressed as a percentage of the asymptotic performance on B. Shown are the mean ± SEM of memory retention for each group, with individual data superimposed as dots. ***p < 0.001 indicates those groups that differed significantly from the control group according to Dunnett's test.

Figure 4.

Experiment 3. Sleep potentiates SMA when it overlaps with the time window during which memory remains fragile. a, Learning curves. Shown are the median ± SEM of the normalized pointing angle (in arbitrary units) corresponding to the AM/AM and PM/PM groups and their circadian controls (AM/PM and PM/AM). b, Memory retention. Memory retention was evaluated during the test session by quantifying the pointing angle through two error-clamp cycles, which was expressed as a percentage of the asymptotic performance level. Shown are the mean ± SEM of the memory retention attained by each group; individual data are superimposed as dots. ***p < 0.001 indicates the result of the two-way ANOVA for the main effect of time of training on memory retention.

Figure 5.

Sleep benefits SMA through an active mechanism. Shown are the topographic plots depicting the spatial distribution of the interhemispheric percent change of the density of fast spindles (a) and the fast spindle–SO couplings (b) during NREM of the first cycle of sleep for the PM/PM and the AM/AM groups. The interhemispheric change in these metrics was computed according to the function (left hemisphere − right hemisphere) / right hemisphere * 100, applied across corresponding EEG electrodes. Barplots on the right depict the statistical quantification of these metrics across groups obtained based on LMMs. Superimposed on the bar plots is the estimated grand average for each subject (illustrated as dots). *p < 0.05 indicates the result of the F test across groups.

Figure 6.

The time course of SMA memory retention is not explained by the time spent training at the asymptote. Shown are the mean ± SEM of the number of cycles training at the asymptote (a) and the level of memory retention (b) corresponding to the 5 min, 1 h, and control groups from Experiment 2 and to the overlearning group. *p < 0.05, **p < 0.01, ***p < 0.001; n.s., nonsignificance, indicates the result of the Dunnett's test for each group compared against the control.