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

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.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.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.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.