Dissociable brainstem functional connectivity changes correlate with objective and subjective vigilance decline after total sleep deprivation in healthy male subjects

Abstract The maintenance of vigilance relies on the activation of the cerebral cortex by the arousal system centered on the brainstem. Previous studies have suggested that both objective and subjective vigilance are susceptible to sleep deprivation. This study aims to explore the alterations in brainstem arousal system functional connectivity (FC) and its involvement in these two types of vigilance decline following total sleep deprivation (TSD). Thirty‐seven healthy male subjects underwent two counterbalanced resting‐state fMRI scans, once in rested wakefulness (RW) and once after 36 h of TSD. The pontine tegmental area and caudal midbrain (PTA‐cMidbrain), the core regions of the brainstem arousal system, were chosen as the seeds for FC analysis. The difference in PTA‐cMidbrain FC between RW and TSD conditions was then investigated, as well as its associations with objective vigilance measured by psychomotor vigilance task (PVT) and subjective vigilance measured by Stanford Sleepiness Scale. The sleep‐deprived subjects showed increased PTA‐cMidbrain FC with the thalamus and cerebellum and decreased PTA‐cMidbrain FC with the occipital, parietal, and sensorimotor regions. TSD‐induced increases in PVT reaction time were negatively correlated with altered PTA‐cMidbrain FC in the dorsolateral prefrontal cortex, extrastriate visual cortex, and precuneus. TSD‐induced increases in subjective sleepiness were positively correlated with altered PTA‐cMidbrain FC in default mode regions including the medial prefrontal cortex and precuneus. Our results suggest that different brainstem FC patterns underlie the objective and subjective vigilance declines induced by TSD.