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. 2022:35:103111.
doi: 10.1016/j.nicl.2022.103111. Epub 2022 Jul 14.

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

Yuezhen Li  1 , Guangyuan Zou  2 , Yan Shao  3 , Ping Yao  4 , Jiayi Liu  2 , Shuqin Zhou  5 , Sifan Hu  3 , Jing Xu  6 , Yupeng Guo  3 , Jia-Hong Gao  7 , Qihong Zou  8 , Hongqiang Sun  9
Affiliations

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

Yuezhen Li et al. Neuroimage Clin. 2022.

Abstract

Background: Positron 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.

Methods: Patients 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).

Results: A 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.

Conclusion: The 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.

Keywords: Anterior insula; EEG-fMRI; Insomnia disorder; Salience network; Sleep discrepancy.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1
Group-by-stage interaction effect on the connectivity of the left aINS. (N=33 for the patients, N=31 for the controls. p < 0.001 and clusterwise corrected p < 0.05). Average Fisher-transformed z scores (mean ± SEM) in the clusters for the interaction (post hoc two-sample t tests between the two groups, **p < 0.01). Region 1, left middle occipital gyrus/right inferior temporal gyrus; Region 2, right middle occipital gyrus; Region 3, bilateral superior frontal gyrus; Region 4, right inferior temporal gyrus; Region 5, right postcentral gyrus.
Fig. 2
Fig. 2
Group-by-stage interaction effect on the connectivity of the right aINS.(N=33 for the patients, N=31 for the controls. p < 0.001 and clusterwise corrected p < 0.05). Average Fisher-transformed z scores (mean ± SEM) in the clusters for the interaction (post hoc two-sample t tests between the two groups, **p < 0.01). Region 1, left middle occipital gyrus; Region 2, superior medial frontal gyrus.
Fig. 3
Fig. 3
MI-by-group interaction effect on the connectivity of the left aINS during wakefulness.(N=17 for the patients, N=10 for the controls). Colored brain region: left putamen/ thalamus. TSTMI, total sleep time misperception index ((sleep diary TST - PSG TST) ⁄ PSG TST); laINS, left anterior insula.
Fig. 4
Fig. 4
MI-by-group interaction effect on the connectivity of the right aINS during wakefulness. (N=17 for the patients, N=10 for the controls). Colored brain region: right putamen/ thalamus. TSTMI, total sleep time misperception index ((sleep diary TST - PSG TST) ⁄ PSG TST); raINS, right anterior insula.
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