Sleep Inertia:Evidence From Electroencephalogram And Functional Magnetic Resonance Imaging

Sleep inertia is a phenomenon of temporary hypo-vigilance,confusion,disorientation of behavior,and impaired cognitive and behavioral performance right after awakening.Previous studies have confirmed various cognitive impairments during sleep inertia,such as response latency,error-monitoring function,working memory,and decision-making.Basic research on sleep inertia suggests that the transition from sleep to the waking state is not an all-or-none basis,but rather according to a slow and progressive mechanism.Despite the increasing attention paid to the effect of sleep inertia on cognitive performance,the neurophysiological mechanisms of awakening from sleep remains largely understudied.This study further explores the cognitive neural mechanisms of sleep inertia through two experiments.There are three purposes for this study.First of all,we examine whether sleep-specific features intrude into the sleep inertia phase.Secondly,we investigate the change of both electroencephalogram(EEG)network and large-scale network between pre-sleep and sleep inertia phases.Finally,the dynamic interactions of neuroelectric and hemodynamic responses are revealed by a time-course analysis with high temporal resolution.In the first study,we explored whether a 90-minute nap could induce sleep inertia and investigate the changes of EEG network between pre-sleep and sleep inertia phases using minimum spanning tree analysis.Specifically,we collected 5-min eyes-open EEG resting data from 27 healthy college students at pre-sleep,5 minutes after waking,and 25 minutes after waking,and these participants completed the psychomotor vigilance test and the positive-negative mood scale.Among the 15 participants who have 5 min slow-wave sleep,eight participants' vigilance impaired upon awakening.Compared to the pre-sleep resting state,the diameter and average eccentricity of the delta frequency band significantly increased during sleep inertia,which means the degree of integration of the delta EEG network decreased.Besides,we explored the emotional state of the participants during sleep inertia,and we found neither the score on the positive-negative emotional scale nor the EEG frontal alpha asymmetry was no significant changes among pre-sleep,5 min after awakening and 25min after awakening.In the second study,we gathered resting-state brain functional data with simultaneous EEG-fMRI during pre-sleep and sleep inertia phases from 43 healthy college students.We focused on electrophysiology,hemodynamics,and the coupling between them during sleep inertia and provided fundamental insight into the nature of sleep inertia from a multimodal perspective.The results showed that compared to the pre-sleep resting-state,1)delta band increased significantly and EEG vigilance decreased upon awakening,2)the low-frequency amplitude of the default network decreased significantly,3)the functional connectivity between the default network and the dorsal attention network decreased significantly;the functional connectivity between the frontal control network and the dorsal attention network decreased significantly,4)the correlation between the frontoparietal network(FPN)and EEG vigilance disappeared during sleep inertia.Overall,the present study further explored cognitive neural mechanisms during sleep inertia and identified some unique manifestations of the sleep-to-wake transition process.Both spectral power and connectivity features of the delta band showed a unique pattern that is significantly different from that in the fully awake state,reflecting the intrusion of sleep-like elements into sleep inertia.For functional Magnetic Resonance Imaging(fMRI),both brain activity and functional connectivity decreased for the three large-scale networks.More importantly,the FPN lost its regulation of EEG vigilance upon awakening;the neural substrate underpinning this phenomenon was the impaired dynamic interaction revealed by simultaneous EEG-fMRI.Our data provide new multimodal neurophysiological evidence of sleep inertia and may facilitate the development of potential treatments for sleep disorders related to jet lag and shift work.