Changes in slow oscillations and sleep spindles by auditory stimulation positively correlate with memory consolidation in children with epilepsy and controls

Kwon, H.; Chinappen, D. M.; Wodeyar, A.; Kinard, E. A.; Goodman, S. K.; Shi, W.; Baxter, B. S.; Manoach, D. S.; Kramer, M. A.; Chu, C. J.

doi:10.1101/2025.05.12.653459

bioRxiv · 10.1101/2025.05.12.653459

Changes in slow oscillations and sleep spindles by auditory stimulation positively correlate with memory consolidation in children with epilepsy and controls

Kwon, H.·Chinappen, D. M.·Wodeyar, A.·Kinard, E. A.·Goodman, S. K.·Shi, W.·Baxter, B. S.·Manoach, D. S.·Kramer, M. A.·Chu, C. J.

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Abstract

BackgroundSleep-dependent memory consolidation is supported by sleep spindles during stages 2 and 3 non-rapid eye movement sleep. Sleep spindles and sleep-dependent memory consolidation are both decreased in Rolandic epilepsy (RE). Non-invasive auditory stimulation evokes SOs and SO-spindle complexes in healthy adults but the impact on memory consolidation has been inconsistent. ObjectiveWe investigated the effects of auditory stimulation during sleep on SOs, SO-spindle complexes, and sleep-dependent memory consolidation in children with RE and controls. MethodsA prospective cross-over study was conducted in children with RE and control. Children completed two nap visits with auditory or sham stimulation. SOs and SO-spindle complexes rates were measured offline using validated detectors. Sleep-dependent memory consolidation was assessed using the motor sequence typing task. ResultsAuditory stimulation evoked SOs and SO-spindle complexes broadly with maximal effect over frontal electrodes. Compared to sham, stimulation delivered during background activity evoked SOs (29.8% increase, p<0.001) and SO-spindle complexes (16.8% increase, p<0.001) and stimulations delivered near the peak of an ongoing SO upstate maximally evoked SOs (51.3% increase, p<0.001) and SO-spindle complexes (32.3% increase, p<0.001). Changes in frontal SO (1.9% improvement per increase in SO/min; p<0.001) and SO-spindle complexes (9.5% improvement per increase in SO-spindle/min) event rates due to auditory stimulation positively predicted changes in sleep-dependent memory consolidation. ConclusionAuditory stimulation reliably modulates sleep oscillations when delivered on background activity and during the upstate of SOs. As increased event rates improve memory consolidation, stimulation paradigms to increase SO and SO-spindle complex rates are required to enhance memory.

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Kwon, H., Chinappen, D. M., Wodeyar, A., Kinard, E. A., Goodman, S. K., Shi, W., Baxter, B. S., Manoach, D. S., Kramer, M. A., Chu, C. J.. 2025-05-13. Changes in slow oscillations and sleep spindles by auditory stimulation positively correlate with memory consolidation in children with epilepsy and controls. https://doi.org/10.1101/2025.05.12.653459

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