Sleep spindles predict neural and behavioral changes in motor sequence consolidation

Abstract

The purpose of this study was to investigate the predictive function of sleep spindles in motor sequence consolidation. BOLD responses were acquired in 10 young healthy subjects who were trained on an explicitly known 5-item sequence using their left nondominant hand, scanned at 9:00 pm while performing that same task and then were retested and scanned 12 h later after a night of sleep during which polysomnographic measures were recorded. An automatic algorithm was used to detect sleep spindles and to quantify their characteristics (i.e., density, amplitude, and duration). Analyses revealed significant positive correlations between gains in performance and the amplitude of spindles. Moreover, significant increases in BOLD signal were observed in several motor-related areas, most of which were localized in the right hemisphere, particularly in the right cortico-striatal system. Such increases in BOLD signal also correlated positively with the amplitude of spindles at several derivations. Taken together, our results show that sleep spindles predict neural and behavioral changes in overnight motor sequence consolidation.

Keywords: EEG; cortico-striatal system; fMRI; motor sequence consolidation; sleep spindles.

Figure 1

Experimental design used in the present experiment.

Figure 2

Behavioral Results: Comparison of the time per sequence in seconds (TpS) on the last block of practice during the immediate test and the first block of practice during the delayed retest.

Figure 3

Statistical parametric maps revealing brain regions that showed significant changes in BOLD activity following a night of sleep. A: Right Putamen/Globus Pallidus, B: Right Primary Motor Cortex. On the right: graph depicting strength of BOLD signal in the Putamen/Globus Pallidus and Right Primary Motor Cortex during both the Immediate test (S1) and the Delayed Retest (S2) sessions.

Figure 4

Correlation between the amplitude of spindles at F4 and percentage of performance gains (r[10] = 0.73, P = 0.025).

Figure 5

Brain regions showing a significant correlation between spindles amplitude on F4 and BOLD activity changes after the experimental night in the (A) Right Putamen /Globus Pallidus (r[10] = 0.70, P = 0.024), and (B) Right Primary Motor Cortex (r[10] = 0.65, P = 0.041). On the right: plot graph depicting a positive correlation between the strength of the BOLD signal (x axis) and the spindle amplitude on F4 (y axis).