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. 2020 Oct 15;41(15):4288-4298.
doi: 10.1002/hbm.25125. Epub 2020 Jul 11.

Loss of frontal regulator of vigilance during sleep inertia: A simultaneous EEG-fMRI study

Xinyuan Chen  1   2 , Ching-Fen Hsu  3 , Dan Xu  1   2 , Jing Yu  1   2 , Xu Lei  1   2
Affiliations

Loss of frontal regulator of vigilance during sleep inertia: A simultaneous EEG-fMRI study

Xinyuan Chen et al. Hum Brain Mapp. .

Abstract

Sleep inertia refers to a distinct physiological state of waking up from sleep accompanied by performance impairments and sleepiness. The neural substrates of sleep inertia are unknown, but growing evidence suggests that this inertia state maintains certain sleep features. To investigate the neurophysiological mechanisms of sleep inertia, a comparison of pre-sleep and post-sleep wakefulness with eyes-open resting-state was performed using simultaneous EEG-fMRI, which has the potential to reveal the dynamic details of neuroelectric and hemodynamic responses with high temporal resolution. Our data suggested sleep-like features of slow EEG power and decreased BOLD activity were persistent during sleep inertia. In the pre-sleep phase, participants with stronger EEG vigilance showed stronger activity in the fronto-parietal network (FPN), but this phenomenon disappeared during sleep inertia. A time course analysis confirmed a decreased correlation between EEG vigilance and the FPN activity during sleep inertia. This simultaneous EEG-fMRI study advanced our understanding of sleep inertia and revealed the importance of the FPN in maintaining awareness. This is the first study to reveal the dynamic brain network changes from multi-modalities perspective during sleep inertia.

Keywords: EEG vigilance; fronto-parietal network; resting-state; simultaneous EEG-fMRI; sleep inertia.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIGURE 1
FIGURE 1
The spatial distribution of the DMN, DAN, and FPN. Brain areas with intensities of two SD greater than the mean are shown. DMN, default mode network (green); DAN, dorsal attention network (blue); FPN, fronto‐parietal network (red)
FIGURE 2
FIGURE 2
A flow diagram of correlation analyses between EEG vigilance and fMRI time courses. EEG and fMRI signals were processed with the model‐specific methods and were correlated in the temporary domain. Original EEG data were correlated with the fMRI gradients and ballistocardiographic artifacts. Then, frequencies of delta, theta, and alpha band powers were calculated, and the EEG vigilance was estimated. For fMRI signals, group ICA was conducted. Brain networks, including the DMN, DAN, and FPN, were selected. The correlations were calculated between fMRI time courses of brain networks and EEG vigilance, which was convoluted with the hemodynamic response function to obtain the predictor of BOLD responses. DMN, default mode network; DAN, dorsal attention network; FPN, fronto‐parietal network
FIGURE 3
FIGURE 3
Comparisons of EEG rhythms and fMRI brain networks during pre‐sleep (red) and sleep inertia phases (green). (a). EEG rhythms and EEG vigilance during pre‐sleep and sleep inertia phases. (b). The low‐frequency fluctuation (ALFF) of the DMN, DAN, and FPN. (c). The functional connectivity among the three brain networks. DMN, default mode network; DAN, dorsal attention network; FPN, fronto‐parietal network*p < .05, **p < .01
FIGURE 4
FIGURE 4
Correlation between EEG vigilance and time course of resting‐state networks. (a). The mean and SE of the correlation between EEG vigilance and three networks during pre‐sleep (red) and sleep inertia (green) phase. Each dot represents one participant. (b). Relationship between EEG vigilance and time course of the FPN in one participant during pre‐sleep resting‐state. (c). Relationship between EEG vigilance and time course of the FPN in the same participant during sleep inertia. Blue line: time course of fMRI brain network; green line: EEG vigilance. Note that the EEG vigilance was inverse plotted (i.e., multiply with −1) for ease of visualization. DMN, default mode network; DAN, dorsal attention network; FPN, fronto‐parietal network* p<0.01
FIGURE 5
FIGURE 5
Correlation between the EEG vigilance and ALFF of the three brain networks at a group level. All values indicate the differences between pre‐sleep and sleep inertia phases. (a). Correlation between the EEG vigilance and ALFF of the FPN. (b). Correlation between the EEG vigilance and ALFF of the DAN. (c). Correlation between the EEG vigilance and ALFF of the DMN. DMN, default mode network; DAN, dorsal attention network; FPN, fronto‐parietal network
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