Altered vigilant maintenance and reorganization of rich-clubs in functional brain networks after total sleep deprivation.

BACKGROUND: Sleep deprivation strongly deteriorates the stability of vigilant maintenance. In previous neuroimaging studies of large-scale networks, neural variations in the resting state after sleep deprivation have been well documented, highlighting that large-scale networks implement efficient cognitive functions and attention regulation in a spatially hierarchical organization. However, alterations of neural networks during cognitive tasks have rarely been investigated. METHODS AND PURPOSES: The present study used a within-participant design of 35 healthy right-handed adults and used task-based functional magnetic resonance imaging to examine the neural mechanism of attentional decline after sleep deprivation from the perspective of rich-club architecture during a psychomotor vigilance task. RESULTS: We found that a significant decline in the hub disruption index was related to impaired vigilance due to sleep loss. The hierarchical rich-club architectures were reconstructed after sleep deprivation, especially in the default mode network and sensorimotor network. Notably, the relatively fast alert response compensation was correlated with the feeder organizational hierarchy that connects core (rich-club) and peripheral nodes. SIGNIFICANCES: Our findings provide novel insights into understanding the relationship of alterations in vigilance and the hierarchical architectures of the human brain after sleep deprivation, emphasizing the significance of optimal collaboration between different functional hierarchies for regular attention maintenance.

Altered effective connectivity of thalamus with vigilance impairments after sleep deprivation.

The thalamus is an essential gating hub to relay brainstem ascending arousal signals to attention-related networks, including the frontal-parietal attention network and default mode network, which plays an important role in attentional maintenance. Research has proved that sleep loss leads to impairment of attentional performance by affecting neural connectivity between thalamic and attention-related cortical regions. However, the effective connectivity between thalamic and cortical areas in the resting state remains unclear after sleep deprivation. The present study aimed to investigate the effect of sleep deprivation on the effective connectivity between thalamic and cortical areas, and explored whether the alteration of the effective connectivity can predict vigilance impairment after sleep deprivation. We implemented resting-state functional magnetic resonance imaging with 31 participants under both normally-rested and sleep-deprivation conditions. The Granger causality analysis was used to investigate the alteration of effective connectivity between thalamic and cortical areas, and the psychomotor vigilance task was used to measure vigilance. Correlation analysis investigated the relationship between the alteration in effective connectivity and vigilance performance. Sleep deprivation significantly decreased the effective connectivity from the thalamus to the nodes in the default mode network, and significantly increased in the effective connectivity from the thalamus to the nodes in the frontal-parietal attention network. Critically, increased thalamus-parietal effective connectivity was correlated with decreased lapses. The findings indicated sleep deprivation induced a robust alteration of the communication from the sub-cortical to cortical regions. The alteration of thalamus-parietal effective connectivity was anti-correlated with sustained attentional impairment after sleep deprivation.

Temporal fluctuations in vigilance and neural networks after sleep deprivation.

Vigilance instability in the sleep-deprived state was deemed to result from the imbalance in thalamic-FPN-DMN circuits (FPN: frontoparietal network; DMN: default mode network), but the behavioural correlation of this neural hypothesis is still unclear. To address this issue, we applied dynamic functional connectivity (DFC) analysis on the task-based fMRI data and detected high arousal state (HAS) and low arousal state (LAS). Relative to HAS, LAS demonstrated higher positive connectivity within task-positive networks (TPN), attenuated TPN-DMN anti-correlation, and greater anti-correlation between cerebral and subcortico-cerebellar networks. Critically, DFC differences between HAS and LAS were correlated with the ongoing vigilance performance in the sleep-deprived state. The current findings confirmed a direct link between vigilance instability and DFC in the thalamic-FPN-DMN circuits. In particular, we postulated that the integration within task-related system and segregation between task-related system and the subcortico-cerebellar system might be the critical neural markers underlying vigilance instability in the sleep-deprived state.