Acoustic enhancement of slow wave sleep improves memory retention by coordinating brain oscillatory rhythms and autonomic activity.

Abstract

The interplay between sleep slow oscillations (SOs), spindles, and autonomic activity is thought to be crucial for sleep-dependent memory consolidation, yet the precise mechanisms remain unclear. In this randomized, single-blind, crossover study of 20 healthy young adults (25 ± 4 years, 75% female), we investigated whether one night of closed-loop acoustic stimulation of sleep slow waves during non-rapid eye movement sleep stages 2 and 3 enhanced memory retention at a paired word-associates task by modulating these neural and autonomic processes, compared to a sham condition. We found that memory enhancement was associated with two tightly coupled mechanisms: increased spindle nesting with SOs (0.5 - 1.5 Hz) relative to delta waves (δ, >1.5 - 4 Hz), and elevated parasympathetic activity measured by heart rate variability during SWS. Critically, the SO/δ-spindle nesting ratio, not absolute SO-spindle nesting, predicted memory performance, suggesting that an optimized relative balance between SO and δ wave influences on spindle activity drives consolidation. Both the SO/δ-spindle nesting ratio and parasympathetic activity predicted memory retention and were strongly correlated, pointing to a potential mechanistic link. Findings suggest that acoustic stimulation may enhance memory consolidation by optimizing the coordination between sleep oscillatory networks and autonomic activity.