Dynamic neural activity and vigilance impairment during prolonged wakefulness: A resting-state EEG study

The homeostatic regulation of sleep is thought to underlie the temporal progressive decline in vigilance. However, accumulating evidence indicated that the decline in vigilance does not follow a simple linear trajectory in sleep loss. Therefore, it is necessary to investigate how vigilance degradation progressively evolves during prolonged wakefulness and to capture the temporal progression of cortical neural activities associated with this variation. Forty-five healthy young adults underwent a prolonged period of wakefulness for one night at their habitual bedtime. Participants completed a 10-minute psychomotor vigilance task and resting-state electroencephalography recording from 22:00 (baseline) to 06:00 at 2-hour intervals. Power spectral and phase-amplitude coupling analyses were conducted. Vigilance during prolonged wakefulness exhibited a gradient deterioration that remained stable until 02:00, then sharply declined at 04:00. At 02:00, the coupling between the frontal delta phase and occipital gamma amplitude significantly increased and showed a significant negative correlation with lapses, potentially indicating a top-down compensatory mechanism. Additionally, increased delta activity in parietal areas was significantly correlated with increased mean reaction time and lapses at 04:00. These findings reveal the dynamic fluctuations of neural activity during prolonged wakefulness and suggest that the disconnection between anterior and posterior brain regions may be one of the critical factors contributing to deterioration in vigilance performance.