Traces of EEG-fMRI coupling reveals neurovascular dynamics on sleep inertia.

Upon emergence from sleep, individuals experience temporary hypo-vigilance and grogginess known as sleep inertia. During the transient period of vigilance recovery from prior nocturnal sleep, the neurovascular coupling (NVC) may not be static and constant as assumed by previous neuroimaging studies. Stemming from this viewpoint of sleep inertia, this study aims to probe the NVC changes as awakening time prolongs using simultaneous EEG-fMRI. The time-lagged coupling between EEG features of vigilance and BOLD-fMRI signals, in selected regions of interest, was calculated with one pre-sleep and three consecutive post-awakening resting-state measures. We found marginal changes in EEG theta/beta ratio and spectral slope across post-awakening sessions, demonstrating alterations of vigilance during sleep inertia. Time-varying EEG-fMRI coupling as awakening prolonged was evidenced by the changing time lags of the peak correlation between EEG alpha-vigilance and fMRI-thalamus, as well as EEG spectral slope and fMRI-anterior cingulate cortex. This study provides the first evidence of potential dynamicity of NVC occurred in sleep inertia and opens new avenues for non-invasive neuroimaging investigations into the neurophysiological mechanisms underlying brain state transitions.

Temporal consistency of neurovascular components on awakening: preliminary evidence from electroencephalography, cerebrovascular reactivity, and functional magnetic resonance imaging.

Sleep inertia (SI) is a time period during the transition from sleep to wakefulness wherein individuals perceive low vigilance with cognitive impairments; SI is generally identified by longer reaction times (RTs) in attention tasks immediately after awakening followed by a gradual RT reduction along with waking time. The sluggish recovery of vigilance in SI involves a dynamic process of brain functions, as evidenced in recent functional magnetic resonance imaging (fMRI) studies in within-network and between-network connectivity. However, these fMRI findings were generally based on the presumption of unchanged neurovascular coupling (NVC) before and after sleep, which remains an uncertain factor to be investigated. Therefore, we recruited 12 young participants to perform a psychomotor vigilance task (PVT) and a breath-hold task of cerebrovascular reactivity (CVR) before sleep and thrice after awakening (A1, A2, and A3, with 20 min intervals in between) using simultaneous electroencephalography (EEG)-fMRI recordings. If the NVC were to hold in SI, we hypothesized that time-varying consistencies could be found between the fMRI response and EEG beta power, but not in neuron-irrelevant CVR. Results showed that the reduced accuracy and increased RT in the PVT upon awakening was consistent with the temporal patterns of the PVT-induced fMRI responses (thalamus, insula, and primary motor cortex) and the EEG beta power (Pz and CP1). The neuron-irrelevant CVR did not show the same time-varying pattern among the brain regions associated with PVT. Our findings imply that the temporal dynamics of fMRI indices upon awakening are dominated by neural activities. This is the first study to explore the temporal consistencies of neurovascular components on awakening, and the discovery provides a neurophysiological basis for further neuroimaging studies regarding SI.