Disrupted coupling between salience network segregation and glucose metabolism is associated with cognitive decline in Alzheimer's disease – A simultaneous resting-state FDG-PET/fMRI study

Miao Zhang; Ziyun Guan; Yaoyu Zhang; Wanqing Sun; Wenli Li; Jialin Hu; Binyin Li; Guanyu Ye; Hongping Meng; Xinyun Huang; Xiaozhu Lin; Jin Wang; Jun Liu; Biao Li; Yao Li

NeuroImage: Clinical (Jan 2022)

Disrupted coupling between salience network segregation and glucose metabolism is associated with cognitive decline in Alzheimer's disease – A simultaneous resting-state FDG-PET/fMRI study

Miao Zhang,
Ziyun Guan,
Yaoyu Zhang,
Wanqing Sun,
Wenli Li,
Jialin Hu,
Binyin Li,
Guanyu Ye,
Hongping Meng,
Xinyun Huang,
Xiaozhu Lin,
Jin Wang,
Jun Liu,
Biao Li,
Yao Li

Affiliations

Miao Zhang: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Ziyun Guan: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China
Yaoyu Zhang: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China
Wanqing Sun: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China
Wenli Li: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China
Jialin Hu: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China
Binyin Li: Department of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Guanyu Ye: Department of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Hongping Meng: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Xinyun Huang: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Xiaozhu Lin: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Jin Wang: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Jun Liu: Department of Neurology & Institute of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
Biao Li: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; Collaborative Innovation Center for Molecular Imaging of Precision Medicine, Ruijin Center, Shanghai 200025, China; Corresponding authors at: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China (B. Li). School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China (Y. Li).
Yao Li: School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China; Corresponding authors at: Department of Nuclear Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China (B. Li). School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai 200030, China (Y. Li).

Journal volume & issue: Vol. 34
p. 102977

Abstract

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The aberrant organization and functioning of three core neurocognitive networks (NCNs), i.e., default-mode network (DMN), central executive network (CEN), and salience network (SN), are among the prominent features in Alzheimer’s disease (AD). The dysregulation of both intra- and inter-network functional connectivities (FCs) of the three NCNs contributed to AD-related cognitive and behavioral abnormalities. Brain functional network segregation, integrating intra- and inter-network FCs, is essential for maintaining the energetic efficiency of brain metabolism. The association of brain functional network segregation, together with glucose metabolism, with age-related cognitive decline was recently shown. Yet how these joint functional-metabolic biomarkers relate to cognitive decline along with mild cognitive impairment (MCI) and AD remains to be elucidated. In this study, under the framework of the triple-network model, we performed a hybrid FDG-PET/fMRI study to evaluate the concurrent changes of resting-state brain intrinsic FCs and glucose metabolism of the three NCNs across cognitively normal (CN) (N = 24), MCI (N = 21), and AD (N = 21) groups. Lower network segregation and glucose metabolism were observed in all three NCNs in patients with AD. More interestingly, in the SN, the coupled relationship between network segregation and glucose metabolism existed in the CN group (r = 0.523, p = 0.013) and diminished in patients with MCI (r = 0.431, p = 0.065) and AD (r = 0.079, p = 0.748). Finally, the glucose metabolism of the DMN (r = 0.380, p = 0.017) and the network segregation of the SN (r = 0.363, p = 0.023) were significantly correlated with the general cognitive status of the patients. Our findings suggest that the impaired SN segregation and its uncoupled relationship with glucose metabolism contribute to the cognitive decline in AD.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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