Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease

As a central hub in the interconnected brain network, the precuneus has been reported showing disrupted functional connectivity and hypometabolism in Alzheimer’s disease (AD). However, as a highly heterogeneous cortical structure, little is known whether individual subregion of the precuneus is unif...

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Main Authors: Miao Zhang, Wanqing Sun, Ziyun Guan, Jialin Hu, Binyin Li, Guanyu Ye, Hongping Meng, Xinyun Huang, Xiaozhu Lin, Jin Wang, Jun Liu, Biao Li, Yaoyu Zhang, Yao Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Aging Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnagi.2021.737002/full
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language English
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author Miao Zhang
Wanqing Sun
Ziyun Guan
Jialin Hu
Binyin Li
Guanyu Ye
Hongping Meng
Xinyun Huang
Xiaozhu Lin
Jin Wang
Jun Liu
Biao Li
Biao Li
Yaoyu Zhang
Yao Li
spellingShingle Miao Zhang
Wanqing Sun
Ziyun Guan
Jialin Hu
Binyin Li
Guanyu Ye
Hongping Meng
Xinyun Huang
Xiaozhu Lin
Jin Wang
Jun Liu
Biao Li
Biao Li
Yaoyu Zhang
Yao Li
Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
Frontiers in Aging Neuroscience
Alzheimer’s disease
mild cognitive impairment
hybrid PET/MRI
glucose metabolism
functional connectivity
precuneus
author_facet Miao Zhang
Wanqing Sun
Ziyun Guan
Jialin Hu
Binyin Li
Guanyu Ye
Hongping Meng
Xinyun Huang
Xiaozhu Lin
Jin Wang
Jun Liu
Biao Li
Biao Li
Yaoyu Zhang
Yao Li
author_sort Miao Zhang
title Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
title_short Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
title_full Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
title_fullStr Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
title_full_unstemmed Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s Disease
title_sort simultaneous pet/fmri detects distinctive alterations in functional connectivity and glucose metabolism of precuneus subregions in alzheimer’s disease
publisher Frontiers Media S.A.
series Frontiers in Aging Neuroscience
issn 1663-4365
publishDate 2021-09-01
description As a central hub in the interconnected brain network, the precuneus has been reported showing disrupted functional connectivity and hypometabolism in Alzheimer’s disease (AD). However, as a highly heterogeneous cortical structure, little is known whether individual subregion of the precuneus is uniformly or differentially involved in the progression of AD. To this end, using a hybrid PET/fMRI technique, we compared resting-state functional connectivity strength (FCS) and glucose metabolism in dorsal anterior (DA_pcu), dorsal posterior (DP_pcu) and ventral (V_pcu) subregions of the precuneus among 20 AD patients, 23 mild cognitive impairment (MCI) patients, and 27 matched cognitively normal (CN) subjects. The sub-parcellation of precuneus was performed using a K-means clustering algorithm based on its intra-regional functional connectivity. For the whole precuneus, decreased FCS (p = 0.047) and glucose hypometabolism (p = 0.006) were observed in AD patients compared to CN subjects. For the subregions of the precuneus, decreased FCS was found in DP_pcu of AD patients compared to MCI patients (p = 0.011) and in V_pcu for both MCI (p = 0.006) and AD (p = 0.008) patients compared to CN subjects. Reduced glucose metabolism was found in DP_pcu of AD patients compared to CN subjects (p = 0.038) and in V_pcu of AD patients compared to both MCI patients (p = 0.045) and CN subjects (p < 0.001). For both FCS and glucose metabolism, DA_pcu remained relatively unaffected by AD. Moreover, only in V_pcu, disruptions in FCS (r = 0.498, p = 0.042) and hypometabolism (r = 0.566, p = 0.018) were significantly correlated with the cognitive decline of AD patients. Our results demonstrated a distinctively disrupted functional and metabolic pattern from ventral to dorsal precuneus affected by AD, with V_pcu and DA_pcu being the most vulnerable and conservative subregion, respectively. Findings of this study extend our knowledge on the differential roles of precuneus subregions in AD.
topic Alzheimer’s disease
mild cognitive impairment
hybrid PET/MRI
glucose metabolism
functional connectivity
precuneus
url https://www.frontiersin.org/articles/10.3389/fnagi.2021.737002/full
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spelling doaj-98082857e36047e8ba7c9d8328b8ebc22021-09-24T07:12:57ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652021-09-011310.3389/fnagi.2021.737002737002Simultaneous PET/fMRI Detects Distinctive Alterations in Functional Connectivity and Glucose Metabolism of Precuneus Subregions in Alzheimer’s DiseaseMiao Zhang0Wanqing Sun1Ziyun Guan2Jialin Hu3Binyin Li4Guanyu Ye5Hongping Meng6Xinyun Huang7Xiaozhu Lin8Jin Wang9Jun Liu10Biao Li11Biao Li12Yaoyu Zhang13Yao Li14Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaCollaborative Innovation Center for Molecular Imaging of Precision Medicine, Ruijin Center, Shanghai, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, ChinaAs a central hub in the interconnected brain network, the precuneus has been reported showing disrupted functional connectivity and hypometabolism in Alzheimer’s disease (AD). However, as a highly heterogeneous cortical structure, little is known whether individual subregion of the precuneus is uniformly or differentially involved in the progression of AD. To this end, using a hybrid PET/fMRI technique, we compared resting-state functional connectivity strength (FCS) and glucose metabolism in dorsal anterior (DA_pcu), dorsal posterior (DP_pcu) and ventral (V_pcu) subregions of the precuneus among 20 AD patients, 23 mild cognitive impairment (MCI) patients, and 27 matched cognitively normal (CN) subjects. The sub-parcellation of precuneus was performed using a K-means clustering algorithm based on its intra-regional functional connectivity. For the whole precuneus, decreased FCS (p = 0.047) and glucose hypometabolism (p = 0.006) were observed in AD patients compared to CN subjects. For the subregions of the precuneus, decreased FCS was found in DP_pcu of AD patients compared to MCI patients (p = 0.011) and in V_pcu for both MCI (p = 0.006) and AD (p = 0.008) patients compared to CN subjects. Reduced glucose metabolism was found in DP_pcu of AD patients compared to CN subjects (p = 0.038) and in V_pcu of AD patients compared to both MCI patients (p = 0.045) and CN subjects (p < 0.001). For both FCS and glucose metabolism, DA_pcu remained relatively unaffected by AD. Moreover, only in V_pcu, disruptions in FCS (r = 0.498, p = 0.042) and hypometabolism (r = 0.566, p = 0.018) were significantly correlated with the cognitive decline of AD patients. Our results demonstrated a distinctively disrupted functional and metabolic pattern from ventral to dorsal precuneus affected by AD, with V_pcu and DA_pcu being the most vulnerable and conservative subregion, respectively. Findings of this study extend our knowledge on the differential roles of precuneus subregions in AD.https://www.frontiersin.org/articles/10.3389/fnagi.2021.737002/fullAlzheimer’s diseasemild cognitive impairmenthybrid PET/MRIglucose metabolismfunctional connectivityprecuneus