Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers

Background: Deficient sleep is implicated in nicotine dependence as well as depressive and anxiety disorders. The hypothalamus regulates the sleep-wake cycle and supports motivated behavior, and hypothalamic dysfunction may underpin comorbid nicotine dependence, depression and anxiety. We aimed to i...

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Main Authors: Yu Chen, Shefali Chaudhary, Guangfei Li, Lisa M. Fucito, Jinbo Bi, Chiang-Shan R. Li
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Neuroimage: Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2666956024000060
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author Yu Chen
Shefali Chaudhary
Guangfei Li
Lisa M. Fucito
Jinbo Bi
Chiang-Shan R. Li
author_facet Yu Chen
Shefali Chaudhary
Guangfei Li
Lisa M. Fucito
Jinbo Bi
Chiang-Shan R. Li
author_sort Yu Chen
collection DOAJ
description Background: Deficient sleep is implicated in nicotine dependence as well as depressive and anxiety disorders. The hypothalamus regulates the sleep-wake cycle and supports motivated behavior, and hypothalamic dysfunction may underpin comorbid nicotine dependence, depression and anxiety. We aimed to investigate whether and how the resting state functional connectivities (rsFCs) of the hypothalamus relate to cigarette smoking, deficient sleep, depression and anxiety. Methods: We used the data of 64 smokers and 198 age- and sex-matched adults who never smoked, curated from the Human Connectome Project. Deficient sleep and psychiatric problems were each assessed with Pittsburgh Sleep Quality Index (PSQI) and Achenbach Adult Self-Report. We processed the imaging data with published routines and evaluated the results at a corrected threshold, all with age, sex, and the severity of alcohol use as covariates. Results: Smokers vs. never smokers showed poorer sleep quality and greater severity of depression and anxiety. In smokers only, the total PSQI score, indicating more sleep deficits, was positively associated with hypothalamic rsFCs with the right inferior frontal/insula/superior temporal and postcentral (rPoCG) gyri. Stronger hypothalamus-rPoCG rsFCs were also associated with greater severity of depression and anxiety in smokers but not never smokers. Additionally, in smokers, the PSQI score completely mediated the relationships of hypothalamus-rPoCG rsFCs with depression and anxiety severity. Conclusions: These findings associate hypothalamic circuit dysfunction to sleep deficiency and severity of depression and anxiety symptoms in adults who smoke. Future studies may investigate the roles of the hypothalamic circuit in motivated behaviors to better characterize the inter-related neural markers of smoking, deficient sleep, depression and anxiety.
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spelling doaj.art-2c964be7e9c14e7da22ce442148c509c2024-03-17T07:59:12ZengElsevierNeuroimage: Reports2666-95602024-03-0141100200Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokersYu Chen0Shefali Chaudhary1Guangfei Li2Lisa M. Fucito3Jinbo Bi4Chiang-Shan R. Li5Department of Psychiatry, Yale University School of Medicine, New Haven, CT, 06520, USA; Corresponding author. Connecticut Mental Health Center S110, 34 Park Street, New Haven, CT, 06519, USA.Department of Psychiatry, Yale University School of Medicine, New Haven, CT, 06520, USADepartment of Biomedical Engineering, College of Chemistry and Life Science, Beijing University of Technology, Beijing, China; Beijing International Science and Technology Cooperation Base for Intelligent Physiological Measurement and Clinical Transformation, Beijing, ChinaDepartment of Psychiatry, Yale University School of Medicine, New Haven, CT, 06520, USADepartment of Computer Science and Engineering, School of Engineering, University of Connecticut, Storrs, CT, USADepartment of Psychiatry, Yale University School of Medicine, New Haven, CT, 06520, USA; Department of Neuroscience, Yale University School of Medicine, New Haven, CT, 06520, USA; Wu Tsai Institute, Yale University, New Haven, CT, 06520, USABackground: Deficient sleep is implicated in nicotine dependence as well as depressive and anxiety disorders. The hypothalamus regulates the sleep-wake cycle and supports motivated behavior, and hypothalamic dysfunction may underpin comorbid nicotine dependence, depression and anxiety. We aimed to investigate whether and how the resting state functional connectivities (rsFCs) of the hypothalamus relate to cigarette smoking, deficient sleep, depression and anxiety. Methods: We used the data of 64 smokers and 198 age- and sex-matched adults who never smoked, curated from the Human Connectome Project. Deficient sleep and psychiatric problems were each assessed with Pittsburgh Sleep Quality Index (PSQI) and Achenbach Adult Self-Report. We processed the imaging data with published routines and evaluated the results at a corrected threshold, all with age, sex, and the severity of alcohol use as covariates. Results: Smokers vs. never smokers showed poorer sleep quality and greater severity of depression and anxiety. In smokers only, the total PSQI score, indicating more sleep deficits, was positively associated with hypothalamic rsFCs with the right inferior frontal/insula/superior temporal and postcentral (rPoCG) gyri. Stronger hypothalamus-rPoCG rsFCs were also associated with greater severity of depression and anxiety in smokers but not never smokers. Additionally, in smokers, the PSQI score completely mediated the relationships of hypothalamus-rPoCG rsFCs with depression and anxiety severity. Conclusions: These findings associate hypothalamic circuit dysfunction to sleep deficiency and severity of depression and anxiety symptoms in adults who smoke. Future studies may investigate the roles of the hypothalamic circuit in motivated behaviors to better characterize the inter-related neural markers of smoking, deficient sleep, depression and anxiety.http://www.sciencedirect.com/science/article/pii/S2666956024000060SmokingfMRIHypothalamic functional connectivityDeficient sleepDepressionAnxiety
spellingShingle Yu Chen
Shefali Chaudhary
Guangfei Li
Lisa M. Fucito
Jinbo Bi
Chiang-Shan R. Li
Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
Neuroimage: Reports
Smoking
fMRI
Hypothalamic functional connectivity
Deficient sleep
Depression
Anxiety
title Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
title_full Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
title_fullStr Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
title_full_unstemmed Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
title_short Deficient sleep, altered hypothalamic functional connectivity, depression and anxiety in cigarette smokers
title_sort deficient sleep altered hypothalamic functional connectivity depression and anxiety in cigarette smokers
topic Smoking
fMRI
Hypothalamic functional connectivity
Deficient sleep
Depression
Anxiety
url http://www.sciencedirect.com/science/article/pii/S2666956024000060
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