The effects of closed-loop auditory stimulation on sleep oscillatory dynamics in relation to motor procedural memory consolidation

Abstract

Study Objectives Healthy aging and many disorders show reduced sleep-dependent memory consolidation and corresponding alterations in non-rapid eye movement sleep oscillations. Yet sleep physiology remains a relatively neglected target for improving memory. We evaluated the effects of closed-loop auditory stimulation during sleep (CLASS) on slow oscillations (SOs), sleep spindles, and their coupling, all in relation to motor procedural memory consolidation. Methods Twenty healthy young adults had two afternoon naps: one with auditory stimulation during SO upstates and another with no stimulation. Twelve returned for a third nap with stimulation at variable times in relation to SO upstates. In all sessions, participants trained on the Motor Sequence Task prior to napping and were tested afterwards. Results Relative to epochs with no stimulation, upstate stimuli disrupted sleep and evoked SOs, spindles, and SO-coupled spindles. Stimuli that successfully evoked oscillations were delivered closer to the peak of the SO upstate and when spindle power was lower than stimuli that failed to evoke oscillations. Across conditions, participants showed similar significant post-nap performance improvement that correlated with the density of SO-coupled spindles. Conclusions Despite its strong effects on sleep physiology, CLASS failed to enhance motor procedural memory. Our findings suggest methods to overcome this failure, including better sound calibration to preserve sleep continuity and the use of real-time predictive algorithms to more precisely target SO upstates and to avoid disrupting endogenous SO-coupled spindles and their mnemonic function. They motivate continued development of CLASS as an intervention to manipulate sleep oscillatory dynamics and improve memory.

Neurophysiological Correlates of Phase-Specific Enhancement of Motor Memory Consolidation via Slow-Wave Closed-Loop Targeted Memory Reactivation

“…Accordingly, prior research has used experimental interventions to target plasticity processes during this window and, in turn, influence memory consolidation during sleep. In line with our findings, this earlier research has collectively shown that stimulating SO at the up-phase of the slowoscillation enhanced the amplitude of ongoing SOs [17][18][19][20][21][25][26][27]29,33 , sigma oscillation power during the ascending phase of the SO [18][19][20] and memory consolidation [17][18][19][20][21]26,27 . Interestingly, the time-locking of the sigma burst to the up-phase of the SO has been shown to predict a positive outcome of consolidation 14,34 .…”

“…These phase-specific effects are in line with previous studies in which acoustic stimulations delivered in a closed-loop fashion at the up-phase (or during the down-to-up transition) of the SO have been shown to enhance declarative memory consolidation 17,20,21,[25][26][27] (but see 26,28 for null effects). We are only aware of one study using closed-loop acoustic stimulation in the motor memory domain and results showed no benefit of SO upstimulation on motor performance 29 . The discrepancy between this recent research and our findings is unclear but we speculate that methodological differences between studies, such as time afforded in NREM sleep (nap vs. night paradigm) or stimulation phase (380ms post-trough vs. peak), might have contributed to these inconsistencies.…”