Altered insula-prefrontal functional connectivity correlates to decreased vigilant attention after total sleep deprivation

Sleep deprivation can robustly affect vigilant attention. The insula is a key hub of the salience network that mediates shifting attention between endogenous and exogenous states. However, little is known regarding the involvement of insular functional connectivity in impaired vigilant attention after total sleep deprivation (TSD). The purpose of this study is to explore the alterations in insular functional connectivity and its association with vigilant attention performance following TSD. Twenty-six adult men were enrolled in the study. Participants underwent two counterbalanced resting-state functional magnetic resonance imaging (rs-fMRI) scans, once in rested wakefulness (RW) and once after 36 h of TSD. Seed-based functional connectivity analysis was performed using rs-fMRI data for the left and right insula. The vigilant attention was measured using a psychomotor vigilance test (PVT). Furthermore, Pearson correlation analysis was conducted to investigate the relationship between altered insular functional connectivity and PVT performance. Compared to RW, enhanced functional connectivity was observed between the insula and prefrontal cortex and anterior cingulate cortex, while reduced functional connectivity was observed between the insula and temporal, parietal, and occipital regions following TSD. Moreover, altered insular functional connectivity with the prefrontal cortex, ie superior frontal gyrus and middle frontal gyrus, and inferior temporal gyrus was correlated with PVT performance after TSD. Our results suggest that insular coupling with the prefrontal cortex and inferior temporal gyrus may act as neural indicators for vigilant attention impairment, which further reveals the critical role of the salience network in cognitive decline following TSD.