Abnormal Rich Club Organization of Structural Network as a Neuroimaging Feature in Relation With the Severity of Primary Insomnia

Abstract

Purpose: Insomnia is the most prevalent sleep complaint in the general population but is often intractable due to uncertainty regarding the underlying pathomechanisms. Sleep is regulated by a network of neural structures interconnected with the core nodes of the brain connectome referred to as the "rich club". We examined alterations in brain rich-club organization as revealed by diffusion tensor imaging (DTI) and the statistical relationships between abnormalities in rich-club metrics and the clinical features of primary insomnia (PI). Methods: This study recruited 43 primary insomnia (PI) patients and 42 age-, sex-, and education level-matched healthy controls (HCs). Differences in global and regional network parameters between PI and healthy control groups were compared by nonparametric tests, and Spearman's correlations were calculated to assess associations of these network metrics with PI-related clinical features, including disease duration and scores on the Pittsburgh Sleep Quality Index, Insomnia Severity Index, Self-Rating Anxiety Scale, and Self-Rating Depression Scale. Results: Weighted white matter networks exhibited weaker rich-club organization in PI patients than HCs across different thresholds (50%, 75%, and 90%) and parcellation schemes [automated anatomical labeling (AAL)-90 and AAL-1024]. Aberrant rich-club organization was found mainly in limbic-cortical-basal ganglia circuits and the defaultmode network. Conclusions: Abnormal rich-club metrics are a characteristic feature of PI-related to disease severity. These metrics provide potential clues to PI pathogenesis and may be useful as diagnostic markers and for assessment of treatment response.

Rich-club reorganization of functional brain networks in acute mild traumatic brain injury with cognitive impairment

“…The rich-club organization described in the human connectome is a high-capacity central core that comprises a set of regions (22) which are suggested to form an information backbone; it is crucial for brain function and vulnerable to pathogenic agents of disease (23). Consequently, rich-club organization has been studied in several brain disorders, including Alzheimer's disease (24,25), schizophrenia (26), insomnia (27), and stroke (28). Antonakakis et al (18) identified with magnetoencephalography (MEG) that patients with mTBI demonstrate hyper-synchronization among rich-club regions compared with healthy controls (HCs) in the δ band and the δ-γ1, θ-γ1, and β-γ2 frequency pairs.…”

Altered functional connectivity strength in chronic insomnia associated with gut microbiota composition and sleep efficiency

“…Finally, the FCS method calculated by degree centrality was used to explore the abnormal brain areas in CI patients without combining this method with brain structural methods based on 3D-T1WI, DTI, etc. However, our team has explored brain structural alterations and the mechanism of CI in the past ( 53 , 76 , 77 ). In the future, we will further explore the complex mechanism of the interaction between brain functional and structural alterations and the GM in CI patients to screen for more accurate imaging biomarkers for MGBA interaction mechanisms.…”

Disrupted rich club organization of white matter networks in de novo Parkinson's disease with REM sleep behavior disorder

“…It probably revealed that the rich-club connections among central hubs, which worked as high-cost and high-capacity backbone of global brain communication (Power et al 2013; van den Heuvel et al 2012), had higher tendency to be impaired in PD-pRBD patients. Structural networks in primary insomnia DTI studies have suggested that abnormal rich club connections, mainly in the limbic cortices and basal ganglia circuit network, were associated with primary insomnia severity (Wu et al 2020). However, rich club organization in PD-pRBD has not been reported previously.…”