{"title":"Impact of sleep disruptions on gray matter structural covariance networks across the Alzheimer's disease continuum.","authors":"Xiao Luo, Kaicheng Li, Qingze Zeng, Xiaocao Liu, Jixuan Li, Xinyi Zhang, Siyan Zhong, Lingyun Liu, Shuyue Wang, Chao Wang, Yanxing Chen, Minming Zhang, Peiyu Huang","doi":"10.1002/dad2.70077","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>This study explores the impact of sleep disturbances on gray matter structural covariance networks (SCNs) across the Alzheimer's disease (AD) continuum.</p><p><strong>Methods: </strong>Amyloid-negative participants served as controls, whereas amyloid positive (A+) individuals were categorized into six groups based on cognitive status and sleep quality. SCNs for the default mode network (DMN), salience network (SN), and executive control network (ECN) were derived from T1-weighted magnetic resonance images.</p><p><strong>Results: </strong>In the DMN, increased structural associations were observed in cognitive unimpaired (CU) A+ and mild cognitive impairment (MCI) groups regardless of sleep quality, whereas AD with poor sleep (PS) showed a decrease and AD with normal sleep (NS) an increase. For the ECN, AD-NS showed increased and AD-PS showed reduced associations. In the SN, reduced associations were observed in CU A+ NS and MCI-NS, whereas AD-NS displayed increased associations; only AD-PS had decreased associations.</p><p><strong>Conclusion: </strong>Distinct SCN damage patterns between normal and poor sleepers provide insights into sleep disturbances in AD.</p><p><strong>Highlights: </strong>We delineated distinct patterns of structural covariance networks (SCN) impairment across the Alzheimer's disease (AD) continuum, uncovering significant disparities between individuals with normal sleep architecture and those afflicted by sleep disturbances.These observations underscore the pivotal importance of addressing sleep disruptions in AD therapeutics, providing a refined understanding of their detrimental impact on brain networks implicated in the disease.Our investigation epitomizes methodological precision by constructing an AD continuum using amyloid positron emission tomography (PET) and cerebrospinal fluid (CSF) biomarkers to minimize diagnostic heterogeneity, further enhanced by a substantial cohort size that bolsters the robustness and generalizability of our findings.</p>","PeriodicalId":53226,"journal":{"name":"Alzheimer''s and Dementia: Diagnosis, Assessment and Disease Monitoring","volume":"17 1","pages":"e70077"},"PeriodicalIF":4.0000,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11780114/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Alzheimer''s and Dementia: Diagnosis, Assessment and Disease Monitoring","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1002/dad2.70077","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: This study explores the impact of sleep disturbances on gray matter structural covariance networks (SCNs) across the Alzheimer's disease (AD) continuum.
Methods: Amyloid-negative participants served as controls, whereas amyloid positive (A+) individuals were categorized into six groups based on cognitive status and sleep quality. SCNs for the default mode network (DMN), salience network (SN), and executive control network (ECN) were derived from T1-weighted magnetic resonance images.
Results: In the DMN, increased structural associations were observed in cognitive unimpaired (CU) A+ and mild cognitive impairment (MCI) groups regardless of sleep quality, whereas AD with poor sleep (PS) showed a decrease and AD with normal sleep (NS) an increase. For the ECN, AD-NS showed increased and AD-PS showed reduced associations. In the SN, reduced associations were observed in CU A+ NS and MCI-NS, whereas AD-NS displayed increased associations; only AD-PS had decreased associations.
Conclusion: Distinct SCN damage patterns between normal and poor sleepers provide insights into sleep disturbances in AD.
Highlights: We delineated distinct patterns of structural covariance networks (SCN) impairment across the Alzheimer's disease (AD) continuum, uncovering significant disparities between individuals with normal sleep architecture and those afflicted by sleep disturbances.These observations underscore the pivotal importance of addressing sleep disruptions in AD therapeutics, providing a refined understanding of their detrimental impact on brain networks implicated in the disease.Our investigation epitomizes methodological precision by constructing an AD continuum using amyloid positron emission tomography (PET) and cerebrospinal fluid (CSF) biomarkers to minimize diagnostic heterogeneity, further enhanced by a substantial cohort size that bolsters the robustness and generalizability of our findings.
期刊介绍:
Alzheimer''s & Dementia: Diagnosis, Assessment & Disease Monitoring (DADM) is an open access, peer-reviewed, journal from the Alzheimer''s Association® that will publish new research that reports the discovery, development and validation of instruments, technologies, algorithms, and innovative processes. Papers will cover a range of topics interested in the early and accurate detection of individuals with memory complaints and/or among asymptomatic individuals at elevated risk for various forms of memory disorders. The expectation for published papers will be to translate fundamental knowledge about the neurobiology of the disease into practical reports that describe both the conceptual and methodological aspects of the submitted scientific inquiry. Published topics will explore the development of biomarkers, surrogate markers, and conceptual/methodological challenges. Publication priority will be given to papers that 1) describe putative surrogate markers that accurately track disease progression, 2) biomarkers that fulfill international regulatory requirements, 3) reports from large, well-characterized population-based cohorts that comprise the heterogeneity and diversity of asymptomatic individuals and 4) algorithmic development that considers multi-marker arrays (e.g., integrated-omics, genetics, biofluids, imaging, etc.) and advanced computational analytics and technologies.