Jorik D Elberse, Amin Saberi, Reihaneh Ahmadi, Monir Changizi, Hanwen Bi, Felix Hoffstaedter, Bryce A Mander, Simon B Eickhoff, Masoud Tahmasian, Alzheimer's Disease Neuroimaging Initiative
{"title":"The interplay between insomnia symptoms and Alzheimer's disease across three main brain networks.","authors":"Jorik D Elberse, Amin Saberi, Reihaneh Ahmadi, Monir Changizi, Hanwen Bi, Felix Hoffstaedter, Bryce A Mander, Simon B Eickhoff, Masoud Tahmasian, Alzheimer's Disease Neuroimaging Initiative","doi":"10.1093/sleep/zsae145","DOIUrl":null,"url":null,"abstract":"<p><strong>Study objectives: </strong>Insomnia symptoms are prevalent along the trajectory of Alzheimer's disease (AD), but the neurobiological underpinning of their interaction is poorly understood. Here, we assessed structural and functional brain measures within and between the default mode network (DMN), salience network, and central executive network (CEN).</p><p><strong>Methods: </strong>We selected 320 participants from the ADNI database and divided them by their diagnosis: cognitively normal (CN), Mild Cognitive Impairment (MCI), and AD, with and without self-reported insomnia symptoms. We measured the gray matter volume (GMV), structural covariance (SC), degrees centrality (DC), and functional connectivity (FC), testing the effect and interaction of insomnia symptoms and diagnosis on each index. Subsequently, we performed a within-group linear regression across each network and ROI. Finally, we correlated observed abnormalities with changes in cognitive and affective scores.</p><p><strong>Results: </strong>Insomnia symptoms were associated with FC alterations across all groups. The AD group also demonstrated an interaction between insomnia and diagnosis. Within-group analyses revealed that in CN and MCI, insomnia symptoms were characterized by within-network hyperconnectivity, while in AD, within- and between-network hypoconnectivity was ubiquitous. SC and GMV alterations were nonsignificant in the presence of insomnia symptoms, and DC indices only showed network-level alterations in the CEN of AD individuals. Abnormal FC within and between DMN and CEN hubs was additionally associated with reduced cognitive function across all groups, and increased depressive symptoms in AD.</p><p><strong>Conclusions: </strong>We conclude that patients with clinical AD present with a unique pattern of insomnia-related functional alterations, highlighting the profound interaction between both conditions.</p>","PeriodicalId":22018,"journal":{"name":"Sleep","volume":" ","pages":""},"PeriodicalIF":5.6000,"publicationDate":"2024-10-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11467060/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Sleep","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1093/sleep/zsae145","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Medicine","Score":null,"Total":0}
引用次数: 0
Abstract
Study objectives: Insomnia symptoms are prevalent along the trajectory of Alzheimer's disease (AD), but the neurobiological underpinning of their interaction is poorly understood. Here, we assessed structural and functional brain measures within and between the default mode network (DMN), salience network, and central executive network (CEN).
Methods: We selected 320 participants from the ADNI database and divided them by their diagnosis: cognitively normal (CN), Mild Cognitive Impairment (MCI), and AD, with and without self-reported insomnia symptoms. We measured the gray matter volume (GMV), structural covariance (SC), degrees centrality (DC), and functional connectivity (FC), testing the effect and interaction of insomnia symptoms and diagnosis on each index. Subsequently, we performed a within-group linear regression across each network and ROI. Finally, we correlated observed abnormalities with changes in cognitive and affective scores.
Results: Insomnia symptoms were associated with FC alterations across all groups. The AD group also demonstrated an interaction between insomnia and diagnosis. Within-group analyses revealed that in CN and MCI, insomnia symptoms were characterized by within-network hyperconnectivity, while in AD, within- and between-network hypoconnectivity was ubiquitous. SC and GMV alterations were nonsignificant in the presence of insomnia symptoms, and DC indices only showed network-level alterations in the CEN of AD individuals. Abnormal FC within and between DMN and CEN hubs was additionally associated with reduced cognitive function across all groups, and increased depressive symptoms in AD.
Conclusions: We conclude that patients with clinical AD present with a unique pattern of insomnia-related functional alterations, highlighting the profound interaction between both conditions.
期刊介绍:
SLEEP® publishes findings from studies conducted at any level of analysis, including:
Genes
Molecules
Cells
Physiology
Neural systems and circuits
Behavior and cognition
Self-report
SLEEP® publishes articles that use a wide variety of scientific approaches and address a broad range of topics. These may include, but are not limited to:
Basic and neuroscience studies of sleep and circadian mechanisms
In vitro and animal models of sleep, circadian rhythms, and human disorders
Pre-clinical human investigations, including the measurement and manipulation of sleep and circadian rhythms
Studies in clinical or population samples. These may address factors influencing sleep and circadian rhythms (e.g., development and aging, and social and environmental influences) and relationships between sleep, circadian rhythms, health, and disease
Clinical trials, epidemiology studies, implementation, and dissemination research.