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

• Published in: Network neuroscience (Cambridge, Mass.) Mass.), 2023-01, Vol.7 (1), p.102-121
• Main Authors: Hilditch, Cassie J., Bansal, Kanika, Chachad, Ravi, Wong, Lily R., Bathurst, Nicholas G., Feick, Nathan H., Santamaria, Amanda, Shattuck, Nita L., Garcia, Javier O., Flynn-Evans, Erin E.
• Format: Article
• Language: English
• Subjects: Alertness; Behavioral Sciences; Brain; Brain research; Clustering; EEG; Frequencies; Graph theoretical framework; Inertia; Network communication; NREM sleep; Performance enhancement; Short-wavelength-enriched light; Sleep; Sleep and wakefulness; Sleep inertia; Wakefulness
• ISSN: 2472-1751; 2472-1751
• DOI: 10.1162/netn_a_00272

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. Using a graphical framework approach, our findings suggest that following awakening from slow wave sleep: (a) a prioritization scheme may underlie recovery rates for different behaviors; (b) long-range neural connections orchestrating local-global operations are uniquely disrupted; and (c) light is able to minimize disruption to long-range connections, revealing the potential mechanism through which light acts as a countermeasure. This research (a) advances the knowledge of neural processes during the transition from sleep to wakefulness; (b) demonstrates a mechanism underlying a brain-behavior relationship that may serve as a target for future countermeasure research; and (c) applies a novel methodological approach to sleep-wake brain states. Further research is needed to apply this analytical method to alternative interventions and sleep-wake transition scenarios.