Sleep is crucial for survival, but sleep loss commonly occurs in modern society. Individuals experience acute or chronic sleep deprivation due to work pressure, shift work or sleep disorders (Killgore, 2010), and insufficient sleep leads to various dysfunctions of health and cognitive performance (Lim & Dinges, 2010). Acute sleep deprivation can strongly impair various human cognitive functions, including attention, working memory, executive function, and decision making (Chee
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.
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.
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