Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment

Background: Mild cognitive impairment (MCI) is the prodromal phase of Alzheimer’s disease (AD) and has a high risk of progression to AD. Cigarette smoking is one of the important modifiable risk factors in AD progression. Cholinergic dysfunction, especially the nucleus basalis of Meynert (NBM), is t...

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Autores principales: Tiantian Qiu, Qingze Zeng, Xiao Luo, Tongcheng Xu, Zhujing Shen, Xiaopei Xu, Chao Wang, Kaicheng Li, Peiyu Huang, Xiaodong Li, Fei Xie, Shouping Dai, Minming Zhang
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Publicado: Frontiers Media S.A. 2021
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Acceso en línea:https://doaj.org/article/c39da36991484a72b5e09bed88231b55
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spelling oai:doaj.org-article:c39da36991484a72b5e09bed88231b552021-11-18T16:14:44ZEffects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment1663-436510.3389/fnagi.2021.755630https://doaj.org/article/c39da36991484a72b5e09bed88231b552021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fnagi.2021.755630/fullhttps://doaj.org/toc/1663-4365Background: Mild cognitive impairment (MCI) is the prodromal phase of Alzheimer’s disease (AD) and has a high risk of progression to AD. Cigarette smoking is one of the important modifiable risk factors in AD progression. Cholinergic dysfunction, especially the nucleus basalis of Meynert (NBM), is the converging target connecting smoking and AD. However, how cigarette smoking affects NBM connectivity in MCI remains unclear.Objective: This study aimed to evaluate the interaction effects of condition (non-smoking vs. smoking) and diagnosis [cognitively normal (CN) vs. MCI] based on the resting-state functional connectivity (rsFC) of the NBM.Methods: After propensity score matching, we included 86 non-smoking CN, 44 smoking CN, 62 non-smoking MCI, and 32 smoking MCI. All subjects underwent structural and functional magnetic resonance imaging scans and neuropsychological tests. The seed-based rsFC of the NBM with the whole-brain voxel was calculated. Furthermore, the mixed effect analysis was performed to explore the interaction effects between condition and diagnosis on rsFC of the NBM.Results: The interaction effects of condition × diagnosis on rsFC of the NBM were observed in the bilateral prefrontal cortex (PFC), bilateral supplementary motor area (SMA), and right precuneus/middle occipital gyrus (MOG). Specifically, the smoking CN showed decreased rsFC between left NBM and PFC and increased rsFC between left NBM and SMA compared with non-smoking CN and smoking MCI. The smoking MCI showed reduced rsFC between right NBM and precuneus/MOG compared with non-smoking MCI. Additionally, rsFC between the NBM and SMA showed a significant negative correlation with Wechsler Memory Scale-Logical Memory (WMS-LM) immediate recall in smoking CN (r = −0.321, p = 0.041).Conclusion: Our findings indicate that chronic nicotine exposure through smoking may lead to functional connectivity disruption between the NBM and precuneus in MCI patients. The distinct alteration patterns on NBM connectivity in CN smokers and MCI smokers suggest that cigarette smoking has different influences on normal and impaired cognition.Tiantian QiuQingze ZengXiao LuoTongcheng XuZhujing ShenXiaopei XuChao WangKaicheng LiPeiyu HuangXiaodong LiFei XieShouping DaiMinming ZhangFrontiers Media S.A.articlemild cognitive impairmentsmokingcholinergic dysfunctionnucleus basalis of Meynertresting-state functional connectivityNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENFrontiers in Aging Neuroscience, Vol 13 (2021)
institution DOAJ
collection DOAJ
language EN
topic mild cognitive impairment
smoking
cholinergic dysfunction
nucleus basalis of Meynert
resting-state functional connectivity
Neurosciences. Biological psychiatry. Neuropsychiatry
RC321-571
spellingShingle mild cognitive impairment
smoking
cholinergic dysfunction
nucleus basalis of Meynert
resting-state functional connectivity
Neurosciences. Biological psychiatry. Neuropsychiatry
RC321-571
Tiantian Qiu
Qingze Zeng
Xiao Luo
Tongcheng Xu
Zhujing Shen
Xiaopei Xu
Chao Wang
Kaicheng Li
Peiyu Huang
Xiaodong Li
Fei Xie
Shouping Dai
Minming Zhang
Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
description Background: Mild cognitive impairment (MCI) is the prodromal phase of Alzheimer’s disease (AD) and has a high risk of progression to AD. Cigarette smoking is one of the important modifiable risk factors in AD progression. Cholinergic dysfunction, especially the nucleus basalis of Meynert (NBM), is the converging target connecting smoking and AD. However, how cigarette smoking affects NBM connectivity in MCI remains unclear.Objective: This study aimed to evaluate the interaction effects of condition (non-smoking vs. smoking) and diagnosis [cognitively normal (CN) vs. MCI] based on the resting-state functional connectivity (rsFC) of the NBM.Methods: After propensity score matching, we included 86 non-smoking CN, 44 smoking CN, 62 non-smoking MCI, and 32 smoking MCI. All subjects underwent structural and functional magnetic resonance imaging scans and neuropsychological tests. The seed-based rsFC of the NBM with the whole-brain voxel was calculated. Furthermore, the mixed effect analysis was performed to explore the interaction effects between condition and diagnosis on rsFC of the NBM.Results: The interaction effects of condition × diagnosis on rsFC of the NBM were observed in the bilateral prefrontal cortex (PFC), bilateral supplementary motor area (SMA), and right precuneus/middle occipital gyrus (MOG). Specifically, the smoking CN showed decreased rsFC between left NBM and PFC and increased rsFC between left NBM and SMA compared with non-smoking CN and smoking MCI. The smoking MCI showed reduced rsFC between right NBM and precuneus/MOG compared with non-smoking MCI. Additionally, rsFC between the NBM and SMA showed a significant negative correlation with Wechsler Memory Scale-Logical Memory (WMS-LM) immediate recall in smoking CN (r = −0.321, p = 0.041).Conclusion: Our findings indicate that chronic nicotine exposure through smoking may lead to functional connectivity disruption between the NBM and precuneus in MCI patients. The distinct alteration patterns on NBM connectivity in CN smokers and MCI smokers suggest that cigarette smoking has different influences on normal and impaired cognition.
format article
author Tiantian Qiu
Qingze Zeng
Xiao Luo
Tongcheng Xu
Zhujing Shen
Xiaopei Xu
Chao Wang
Kaicheng Li
Peiyu Huang
Xiaodong Li
Fei Xie
Shouping Dai
Minming Zhang
author_facet Tiantian Qiu
Qingze Zeng
Xiao Luo
Tongcheng Xu
Zhujing Shen
Xiaopei Xu
Chao Wang
Kaicheng Li
Peiyu Huang
Xiaodong Li
Fei Xie
Shouping Dai
Minming Zhang
author_sort Tiantian Qiu
title Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
title_short Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
title_full Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
title_fullStr Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
title_full_unstemmed Effects of Cigarette Smoking on Resting-State Functional Connectivity of the Nucleus Basalis of Meynert in Mild Cognitive Impairment
title_sort effects of cigarette smoking on resting-state functional connectivity of the nucleus basalis of meynert in mild cognitive impairment
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/c39da36991484a72b5e09bed88231b55
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