Using Oscillating Sounds to Manipulate Sleep Spindles

Abstract

Introduction: EEG oscillations known as sleep spindles have been linked with various aspects of cognition, but the specific functions they signal remain controversial. Two types of EEG sleep spindles have been distinguished: slow spindles at 11-13.5 Hz and fast spindles at 13.5-16 Hz. Slow spindles exhibit a frontal scalp topography, whereas fast spindles exhibit a posterior scalp topography and have been preferentially linked with memory consolidation during sleep. To advance understanding beyond that provided from correlative studies of spindles, we aimed to develop a new method to systematically manipulate spindles.

Aims and methods: We presented repeating bursts of oscillating white noise to people during a 90-min afternoon nap. During stage 2 and slow-wave sleep, oscillations were embedded within contiguous 10-s stimulation intervals, each comprising 2 s of white noise amplitude modulated at 12 Hz (targeting slow spindles), 15 Hz (targeting fast spindles), or 50 Hz followed by 8 s of constant white noise.

Results: During oscillating stimulation compared to constant stimulation, parietal EEG recordings showed more slow spindles in the 12-Hz condition, more fast spindles in the 15-Hz condition, and no change in the 50-Hz control condition. These effects were topographically selective, and were absent in frontopolar EEG recordings, where slow spindle density was highest. Spindles during stimulation were similar to spontaneous spindles in standard physiological features, including duration and scalp distribution.

Conclusions: These results define a new method to selectively and noninvasively manipulate spindles through acoustic resonance, while also providing new evidence for functional distinctions between the 2 types of EEG spindles.

Keywords: memory consolidation.; oscillations; sleep spindles.

Figure 1

Stimulation parameters and spindle analysis approach. Participants took a 90-min nap amidst a background of white noise. While they slept, 2-s periods of oscillating white noise (OWN) alternated with 8-s periods of constant white noise (CWN). An expanded, 1-s example of 15-Hz OWN is shown.

Figure 2

Oscillating white noise (OWN) increased spindles relative to constant white noise (CWN) in a frequency-specific manner. For the parietal electrode cluster (right column), 12 and 15 Hz stimulation enhanced slow and fast spindles, respectively. For both electrode clusters, 50 Hz stimulation showed no significant changes in spindle density. Error bars denote SEM. **p < .01, ***p < .001.

Figure 3

Frequency-specific spindle increases occurred most strongly between 1 and 2 s of oscillating white noise (OWN) onset. (A) Method for calculating instantaneous spindle density relative to OWN onset. Three sample traces are shown with spindles occurring at different times relative to OWN onset at time 0. For each 100-ms interval during a given 10-s period, the number of spindles counted in the interval (spindles either starting during the interval or continuing into the interval) was converted into an instantaneous spindle density measure. (B) Significant frequency-specific increases manifested during 1–2 s post-OWN onset. Fast and slow spindle counts are presented in light and dark gray, respectively. Color-coded horizontal significance bars signify times during which spindle counts deviated from baseline (average count during 3–9 s post-cue).

Figure 4

Auditory steady-state response (ASSR) analyses revealed no stimulus-evoked power differences for corresponding frequencies. (Top) Plotted are ASSR differences for 2-s segments of OWN − CWN without spindles. No electrodes showed significant differences between OWN and CWN. (Bottom) Spindle boost topographies are presented as a comparison to ASSR results. No cross-electrode topographical correlations were found between the ASSR and spindle boost effect for either condition.