Indication of dynamic neurovascular coupling from inconsistency between EEG and fMRI indices across sleep-wake states

Neurovascular coupling (NVC), the transient regional hyperemia following the evoked neuronal responses, is the basis of blood oxygenation level-dependent techniques and is generally adopted across physiological conditions, including the intrinsic resting state. However, the possibility of neurovascular dissociations across physiological alterations is indicated in the literature. To examine the NVC stability across sleep-wake states, we used electroencephalography (EEG) as the index of neural activity and functional magnetic resonance imaging (fMRI) as the measure of cerebrovascular response. Eight healthy adults were recruited for simultaneous EEG-fMRI recordings in nocturnal sleep. We compared the cross-modality (EEG vs. fMRI) consistency of functional indices (spectral amplitude and functional connectivity) among five states of wakefulness and sleep (state effect). We also segregated the brain into three main partitions (anterior, middle and posterior) for spatial assessments (regional effect). Significant state effects were found on delta, alpha and fMRI indices and regional effects on the alpha and fMRI indices. However, the cross-state EEG changes in spectral amplitude and functional connectivity did not consistently match the changes in the fMRI indices across sleep-wake states. In spectral amplitude, the delta band peaked at the N3 stage for all brain regions, while the fMRI fluctuation amplitude peaked at the N2 stage in the central and posterior regions. In regional connectivity, the inter-hemispheric connectivity of the delta band peaked at the N3 stage for all regions, but the bilateral fMRI connectivity showed the state changes in the anterior and central regions. The cross-modality inconsistencies across sleep-wake states provided preliminary evidence that the neurovascular relationship may not change in a linear consistency during NREM sleep. Thus, caution shall be exercised when applying the NVC presumption to investigating sleep/wake transitions, even among healthy young adults.