Inter-network functional connectivity alterations in chronic Insomnia

Introduction. Chronic insomnia is a common sleep disorder, affecting approximately 10–15% of adults. It is associated with reduced quality of life, cognitive disturbances, and decreased risk of somatic diseases. Functional magnetic resonance imaging (fMRI) allows to assess resting-state neural activity and analyze major brain networks interactions, including sensorimotor network (SMN), visual network (VN), and frontoparietal network (FPN). Previous international studies demonstrated that chronic insomnia involves alterations in both intra- and inter-network connectivity, characterized by increased default mode network activity and reduced frontoparietal integration. However, similar findings in Russian populations are scarce, and associations between functional connectivity measures and objective polysomnographic (PSG) sleep parameters remain insufficiently investigated.
The study aimed to identify major resting-state functional networks in patients with chronic insomnia, assess internetwork connectivity and its correlation with objective sleep parameters.
Materials and methods. The study included 51 patients with clinically confirmed chronic insomnia and 34 healthy volunteers. All participants underwent examination at the Almazov National Medical Research Centre, Ministry of Health of the Russian Federation. Polysomnography was performed using the Embla N7000 system (Natus, USA) and Somnologica Studio software in accordance with the standard protocol. Magnetic resonance imaging was conducted using Magnetom Trio A Tim scanner (Siemens, Germany) with a magnetic field strength of 3.0 T. The protocol comprised a structural T1-MPRAGE sequence and a functional EPI-BOLD sequence (resting state). Data preprocessing included motion correction, slice-timing adjustment, normalization, and spatial smoothing. Independent component analysis (ICA) was performed using SPM12, CONN Toolbox, and DPABI. Statistical analysis was conducted using two-sample t-tests with false discovery rate (FDR) correction for multiple comparisons (p<0.05).
Discussion. Independent component analysis revealed altered functional organization of the sensorimotor, visual, and frontoparietal networks in patients with chronic insomnia. In individuals with disrupted sleep architecture, reduced connectivity between the sensorimotor network and temporal associative regions indicated incomplete deactivation of sensory circuits during the transition to sleep. Decreased connectivity of the visual network with cerebellar and parietotemporal regions suggested impaired sensory inhibition and persistent activation of visual pathways. In patients with reduced sleep quality and prolonged sleep latency, weakened connectivity of the frontoparietal network with frontal and parietotemporal regions reflected impaired cognitive inhibition. Obtained data support the hyperarousal model of chronic insomnia, characterized by sustained activation of executive and sensory networks even during rest.
Conclusion. Patients with chronic insomnia showed altered functional organization of the sensorimotor, visual, and frontoparietal networks, characterized by reduced connectivity with associative and executive brain regions. These changes indicate impaired sensory and cognitive deactivation processes necessary for the transition to sleep and align with the hyperarousal model of insomnia. The findings enhance understanding of neurophysiological mechanisms of sleep disorders and may support the identification of objective MRI markers of sleep-wake regulation disturbances.

1. Zhulev Yu. V., Kulakov S. A., Romanenko A. A. Rasprostranennost’ i struktura narusheniy sna u vzroslogo naseleniya Rossii // Zhurnal nevrologii i psikhiatrii im. S. S. Korsakova. – 2023. – Vol. 123, No. 6. – P. 62–69.

2. Kay D. B., Buysse D. J., Germain A. Evidence for sleep- and wake-related neural activity in insomnia: a meta-analysis of neuroimaging studies // Sleep. – 2016. – Vol. 39, No. 7. – P. 1403–1418.

3. Riemann D., Krone L. B., Wulff K., Nissen C. Sleep, insomnia, and depression // Neuropsychopharmacology. – 2017. – Vol. 42, No. 1. – P. 21–37.

4. Raichle M. E. The brain’s default mode network // Annual Review of Neuroscience. – 2015. – Vol. 38. – P. 433–447.

5. Holub F., Korshoj A. R., Ettrup A. et al. Associations between insomnia symptoms and functional connectivity of the default mode network // Journal of Sleep Research. – 2023. – Vol. 32, No. 6. – e13790.

6. Zheng H., Yu R., Huang X. et al. Altered functional connectivity of the default mode and frontoparietal networks in middle-aged adults with insomnia // Human Brain Mapping. – 2023. – Vol. 44, No. 8. – P. 2941–2954.

7. Sergeev A. V., Trushina L. I., Polyakov A. V. [et al.] Izmeneniya funktsional’noy konnektivnosti pri narusheniyakh sna // Zhurnal nevrologii i psikhiatrii im. S. S. Korsakova. – 2022. – Vol. 122, No. 11. – P. 72–78.

8. Zuo X.-N., Di Martino A., Kelly C., Shehzad Z.-E. et al. Cerebral functional networks during sleep in young and older adults // Scientific Reports. – 2021. – Vol. 11. – Article ID 2307.

9. Liu C.-H., Liu C.-Z., Zhu X.-Q. et al. Increased posterior insula-sensorimotor connectivity is associated with cognitive function in healthy participants with sleep complaints // Frontiers in Human Neuroscience. – 2018. – Vol. 12. – Article 35.

10. Baglioni C., Battagliese G., Feige B. et al. Insomnia as a predictor of depression: a meta-analytic evaluation of longitudinal epidemiological studies // Journal of Affective Disorders. – 2016. – Vol. 186. – P. 10–19.

11. Li C., Dong M., Chen Y. et al. Altered functional connectivity of visual and somatosensory networks in patients with insomnia disorder // Frontiers in Neuroscience. – 2022. – Vol. 16. – 867592.

12. Wang T., Yan J., Li S. et al. Reduced cerebellar functional connectivity with visual and sensorimotor networks in primary insomnia // Brain Imaging and Behavior. – 2020. – Vol. 14, No. 5. – P. 1613–1623.