Reconfigurations in brain networks upon awakening from slow wave sleep: Interventions and implications in neural communication

Abstract

Sleep inertia is the brief period of impaired alertness and performance experienced immediately after waking. Little is known about the neural mechanisms underlying this phenomenon. A better understanding of the neural processes during sleep inertia may offer insight into the awakening process. We observed brain activity every 15 min for 1 hr following abrupt awakening from slow wave sleep during the biological night. Using 32-channel electroencephalography, a network science approach, and a within-subject design, we evaluated power, clustering coefficient, and path length across frequency bands under both a control and a polychromatic short-wavelength-enriched light intervention condition. We found that under control conditions, the awakening brain is typified by an immediate reduction in global theta, alpha, and beta power. Simultaneously, we observed a decrease in the clustering coefficient and an increase in path length within the delta band. Exposure to light immediately after awakening ameliorated changes in clustering. Our results suggest that long-range network communication within the brain is crucial to the awakening process and that the brain may prioritize these long-range connections during this transitional state. Our study highlights a novel neurophysiological signature of the awakening brain and provides a potential mechanism by which light improves performance after waking.

Keywords: Graph theoretical framework; Network communication; Short-wavelength-enriched light; Sleep inertia.

Figure 1.

Comparison for (A) power and (B), (C) brain network properties across test bouts for each frequency band in the control condition (dim red light). BL = baseline, T#_C = Test bout # during the control condition. Asterisks represent significant difference on a paired t test without any further correction applied such that *p < 0.05, **p < 0.01, ***p < 0.001. Dashed line denotes marginally significant difference (p = 0.053).

Figure 2.

Brain network properties comparing pre-sleep baseline (BL), control at T1 (T1_C), and light at T1 (T1_L) for (A), (B) the delta frequency band and (C) delta power. Colored lines represent individual participants. Here, p represents the p value on a paired t test without any further correction applied.

Figure 3.

Change in clustering between (A) baseline (BL) and control at T1 (T1_C), (B) baseline and light at T1 (T1_L), and (C) control and light at T1 across scalp regions in the delta band. Asterisks represent electrodes with significant difference on a paired t test (p < 0.05). Electrodes that survived an additional correction for multiple comparisons are highlighted in white (q < 0.05). (See Figures S6–S8 in the Supporting Information for an additional analysis across the metrics and frequency bands shown within the main text.)

Figure 4.

Protocol schematic. Light gray shading indicates wakefulness during the at-home portion of study. Dark gray shading indicates in-laboratory pre-sleep activities including baseline testing (•). Black shading indicates sleep opportunities (<0.3 lux). Blue and red shading indicate intervention and control sleep inertia testing periods, respectively. Inset shows electrode montage and post-awakening test bouts. Clock times shown are approximate and varied depending on habitual sleep-wake times and appearance of slow wave sleep periods.