Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology

BackgroundStructural network alterations in Alzheimer’s disease (AD) are related to worse cognitive impairment. The aim of this study was to quantify the alterations in gray matter associated with impaired cognition and their pathological biomarkers in AD-spectrum patients.MethodsWe extracted gray m...

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Main Authors: Xiaoning Sheng, Haifeng Chen, Pengfei Shao, Ruomeng Qin, Hui Zhao, Yun Xu, Feng Bai, the Alzheimer’s Disease Neuroimaging Initiative
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2021.630278/full
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language English
format Article
sources DOAJ
author Xiaoning Sheng
Haifeng Chen
Haifeng Chen
Haifeng Chen
Pengfei Shao
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Hui Zhao
Hui Zhao
Hui Zhao
Yun Xu
Yun Xu
Yun Xu
Feng Bai
Feng Bai
Feng Bai
the Alzheimer’s Disease Neuroimaging Initiative
spellingShingle Xiaoning Sheng
Haifeng Chen
Haifeng Chen
Haifeng Chen
Pengfei Shao
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Hui Zhao
Hui Zhao
Hui Zhao
Yun Xu
Yun Xu
Yun Xu
Feng Bai
Feng Bai
Feng Bai
the Alzheimer’s Disease Neuroimaging Initiative
Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
Frontiers in Neuroscience
cognitive impairment
pathological biomarkers
Alzheimer’s disease
structural compensation ability
gray matter (GM) atrophy
author_facet Xiaoning Sheng
Haifeng Chen
Haifeng Chen
Haifeng Chen
Pengfei Shao
Ruomeng Qin
Ruomeng Qin
Ruomeng Qin
Hui Zhao
Hui Zhao
Hui Zhao
Yun Xu
Yun Xu
Yun Xu
Feng Bai
Feng Bai
Feng Bai
the Alzheimer’s Disease Neuroimaging Initiative
author_sort Xiaoning Sheng
title Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
title_short Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
title_full Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
title_fullStr Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
title_full_unstemmed Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease Pathology
title_sort brain structural network compensation is associated with cognitive impairment and alzheimer’s disease pathology
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2021-02-01
description BackgroundStructural network alterations in Alzheimer’s disease (AD) are related to worse cognitive impairment. The aim of this study was to quantify the alterations in gray matter associated with impaired cognition and their pathological biomarkers in AD-spectrum patients.MethodsWe extracted gray matter networks from 3D-T1 magnetic resonance imaging scans, and a graph theory analysis was used to explore alterations in the network metrics in 34 healthy controls, 70 mild cognitive impairment (MCI) patients, and 40 AD patients. Spearman correlation analysis was computed to investigate the relationships among network properties, neuropsychological performance, and cerebrospinal fluid pathological biomarkers (i.e., Aβ, t-tau, and p-tau) in these subjects.ResultsAD-spectrum individuals demonstrated higher nodal properties and edge properties associated with impaired memory function, and lower amyloid-β or higher tau levels than the controls. Furthermore, these compensations at the brain regional level in AD-spectrum patients were mainly in the medial temporal lobe; however, the compensation at the whole-brain network level gradually extended from the frontal lobe to become widely distributed throughout the cortex with the progression of AD.ConclusionThe findings provide insight into the alterations in the gray matter network related to impaired cognition and pathological biomarkers in the progression of AD. The possibility of compensation was detected in the structural networks in AD-spectrum patients; the compensatory patterns at regional and whole-brain levels were different and the clinical significance was highlighted.
topic cognitive impairment
pathological biomarkers
Alzheimer’s disease
structural compensation ability
gray matter (GM) atrophy
url https://www.frontiersin.org/articles/10.3389/fnins.2021.630278/full
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spelling doaj-c369ff0aa2c448908b4ea093006978612021-02-25T09:23:26ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-02-011510.3389/fnins.2021.630278630278Brain Structural Network Compensation Is Associated With Cognitive Impairment and Alzheimer’s Disease PathologyXiaoning Sheng0Haifeng Chen1Haifeng Chen2Haifeng Chen3Pengfei Shao4Ruomeng Qin5Ruomeng Qin6Ruomeng Qin7Hui Zhao8Hui Zhao9Hui Zhao10Yun Xu11Yun Xu12Yun Xu13Feng Bai14Feng Bai15Feng Bai16the Alzheimer’s Disease Neuroimaging InitiativeDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaDepartment of Neurology, Affiliated Drum Tower Hospital of Medical School and The State Key Laboratory of Pharmaceutical Biotechnology, Institute of Brain Science, Nanjing University, Nanjing, ChinaJiangsu Province Stroke Center for Diagnosis and Therapy, Nanjing, ChinaNanjing Neuropsychiatry Clinic Medical Center, Nanjing, ChinaBackgroundStructural network alterations in Alzheimer’s disease (AD) are related to worse cognitive impairment. The aim of this study was to quantify the alterations in gray matter associated with impaired cognition and their pathological biomarkers in AD-spectrum patients.MethodsWe extracted gray matter networks from 3D-T1 magnetic resonance imaging scans, and a graph theory analysis was used to explore alterations in the network metrics in 34 healthy controls, 70 mild cognitive impairment (MCI) patients, and 40 AD patients. Spearman correlation analysis was computed to investigate the relationships among network properties, neuropsychological performance, and cerebrospinal fluid pathological biomarkers (i.e., Aβ, t-tau, and p-tau) in these subjects.ResultsAD-spectrum individuals demonstrated higher nodal properties and edge properties associated with impaired memory function, and lower amyloid-β or higher tau levels than the controls. Furthermore, these compensations at the brain regional level in AD-spectrum patients were mainly in the medial temporal lobe; however, the compensation at the whole-brain network level gradually extended from the frontal lobe to become widely distributed throughout the cortex with the progression of AD.ConclusionThe findings provide insight into the alterations in the gray matter network related to impaired cognition and pathological biomarkers in the progression of AD. The possibility of compensation was detected in the structural networks in AD-spectrum patients; the compensatory patterns at regional and whole-brain levels were different and the clinical significance was highlighted.https://www.frontiersin.org/articles/10.3389/fnins.2021.630278/fullcognitive impairmentpathological biomarkersAlzheimer’s diseasestructural compensation abilitygray matter (GM) atrophy