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Closed-Loop Auditory Stimulation Reveals Differential Sleep Oscillatory Contributions to Memory in Healthy Older Adults

Saied SabaghypouriD, Lawrence OpreaiD, Arthur S. PowanweiD, Christine N. MoreauiD, Natasha Alfeche, Adrian M. OweniD, Stefan KöhleriD, Lyle MulleriD, Laura J. BatterinkiD

Abstract

Sleep oscillations during non-rapid eye movement (NREM) sleep support memory consolidation but decline with age. Phase-locked auditory stimulation (PLAS) enhances slow-wave activity, yet its effects on distinct oscillatory components and memory in older adults remain unclear. Sixteen healthy older adults (60 years or older; mean age = 65.06 +/- 3.53 years) participated in a randomized, single-blind, sham-controlled crossover study. Participants completed two stimulation nights and two sham nights in a sleep laboratory. Changes in slow oscillations (0.5-1.25 Hz), frontal theta (4-8 Hz), centrofrontal slow spindles (12-14 Hz), and centroparietal fast spindles (14-16 Hz) were compared between stimulation and sham conditions. Declarative memory was assessed using a word-pair recall task that required overnight retention, and broader cognitive performance was evaluated using the Creyos cognitive assessment battery. PLAS enhanced sleep oscillatory activity without altering sleep architecture. Compared with sham, stimulation increased slow oscillation, frontal theta, centrofrontal slow spindle, and centroparietal fast spindle power across both stimulation nights. Although word-pair recall did not improve at the group level, individual differences in stimulation-induced increases in fast spindle power were positively associated with individual differences in overnight memory improvement. Closed-loop auditory stimulation enhances multiple NREM oscillations in healthy older adults while preserving sleep architecture. Moreover, stimulation-induced increases in fast spindle activity track individual differences in overnight memory improvement, suggesting fast spindles as a physiological marker of successful sleep-dependent memory consolidation and a potential target for sleep-based neuromodulation in aging.

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