Sleep discrepancy is associated with alterations in the salience network in patients with insomnia disorder: An EEG-fMRI study

Abstract

BackgroundPositron emission tomography – computed tomography (PET-CT) research has shown that sleep discrepancy recorded by self-report and polysomnography (PSG) may be related to the altered metabolic rate of the anterior insula (aINS) during non-rapid eye movement (NREM) sleep in patients with insomnia disorder. We aim to explore the functional connectivity of aINS across wake and NREM sleep in the patients and to reveal the association between aINS connectivity and sleep discrepancy. MethodsPatients with insomnia disorder (n = 33) and healthy controls (n = 31) underwent simultaneous electroencephalography and functional magnetic resonance imaging (EEG-fMRI) during nighttime sleep, and aINS-based connectivity was calculated across wake and NREM sleep. A linear mixed-effects model was used to assess the main effect of group and group-by-stage (wake, NREM stages 1–3) interaction effect on aINS connectivity. Similar mixed models were used to assess the potential correlation between aINS connectivity and the sleep misperception index (MI). ResultsA significant group-by-stage interaction effect on aINS-based connectivity was observed in the bilateral frontal gyrus, right inferior temporal gyrus, bilateral middle occipital gyrus and right postcentral gyrus (p < 0.05, corrected). There was also a significant group-by-MI interaction effect on aINS connectivity with the putamen and thalamus during wakefulness (p < 0.05 corrected); MI was significantly associated with aINS–putamen/thalamus connectivity in the control group, whereas the association was weak or even nonsignificant in the patient group. There was no significant main effect of group. ConclusionThe waking activity of a neural pathway containing the aINS, putamen, and thalamus may underlie sleep perception, potentially providing important perspectives to reveal complex mechanisms of sleep discrepancy between self-report and PSG.