Exploration of Dynamic Neurovascular Coupling in Sleep Inertia from Simultaneous EEG-fMRI Recordings

Emergence from sleep to wake is underpinned by arousal transitions from low to high levels as sleep inertia dissipates. Previous neuroimaging studies have found both electrophysiological and hemodynamic alterations in the brain during sleep inertia. However, the electrophysiological studies mostly explore canonical frequency band changes, while the fMRI studies largely assumed constant neurovascular coupling (NVC) during sleep inertia, despite recent evidence demonstrating NVC variability depending on brain states. Moreover, past experiments mainly focused on comparing between pre-sleep and post-sleep, without measuring multiple stages of sleep inertia. To characterize the transient neurophysiological changes in human brain during sleep inertia, we utilized simultaneous EEG-fMRI and acquired four resting-state scans – one session before sleep, and three consecutive sessions after awakening – in an attempt to capture the initiation, maintenance, and dissipation of sleep inertia. Specifically, we calculated EEG frequency band power, EEG brain-state metrics (EEG-vigilance, spectral slope, theta/beta ratio, and occipital alpha power), and then conducted a time-lag analysis between EEG metrics and BOLD activities of three brain areas – thalamus, anterior cingulate cortex (ACC), and sensorimotor (SM) cortex. We found that delta power progressively increased upon awakening alongside weak fluctuations of theta/beta ratio and EEG spectral slope. Peak-correlation timing between thalamus and EEG-vigilance as well as ACC and EEG spectral slope were found to significantly alter as awakening time prolonged. The changes in temporal coupling between EEG metrics and ROI BOLD activities suggest potential dynamic NVC mechanisms during sleep inertia that are regionally specific. Our approach and findings should open new avenues for non-invasive neuroimaging investigations into the neurophysiological mechanisms underlying brain state transitions.