Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study

Presbycusis (PC) is characterized by bilateral sensorineural hearing loss at high frequencies and speech-perception difficulties in noisy environments and has a strikingly detrimental impact on cognitive function. As the neural consequences of PC may involve the whole brain, we hypothesized that pat...

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Main Authors: Fuxin Ren, Wen Ma, Muwei Li, Huaiqiang Sun, Qian Xin, Wei Zong, Weibo Chen, Guangbin Wang, Fei Gao, Bin Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-10-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2018.00744/full
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author Fuxin Ren
Wen Ma
Muwei Li
Huaiqiang Sun
Qian Xin
Wei Zong
Weibo Chen
Guangbin Wang
Fei Gao
Bin Zhao
author_facet Fuxin Ren
Wen Ma
Muwei Li
Huaiqiang Sun
Qian Xin
Wei Zong
Weibo Chen
Guangbin Wang
Fei Gao
Bin Zhao
author_sort Fuxin Ren
collection DOAJ
description Presbycusis (PC) is characterized by bilateral sensorineural hearing loss at high frequencies and speech-perception difficulties in noisy environments and has a strikingly detrimental impact on cognitive function. As the neural consequences of PC may involve the whole brain, we hypothesized that patients with PC would show structural alterations not only in the auditory cortex but also in the cortexes involved in cognitive function. The purpose of this study was to use surface-based morphometry (SBM) analysis to elucidate whole-brain structural differences between patients with PC and age-matched normal hearing controls. Three-dimensional T1-weighted MR images of 26 patients with mild PC and 26 age-, sex- and education-matched healthy controls (HCs) were acquired. All participants underwent a battery of neuropsychological tests. Our results revealed gray matter atrophy in several auditory cortical areas, nodes of the default mode network (DMN), including the bilateral precuneus and inferior parietal lobule, the right posterior cingulate cortex (PCC), and the right insula of patients with PC compared to that in the HCs. Our findings also revealed that hearing loss was associated with reduced gray matter volume in the right primary auditory cortex of patients with PC. Moreover, structural alterations in the nodes of the DMN were associated with cognitive impairments in PC patients. Additionally, this study provides evidence that a thicker right insula is associated with better speech perception in patients with PC. Based on these findings, we argue that the onset of PC seems to trigger its own cascade of conditions, including a need for increased cognitive resources during speech comprehension, which might lead to auditory and cognition-related cortical reorganization.
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spelling doaj.art-c28abaefefbd4eca83ae8e8ef262be3b2022-12-22T01:18:11ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2018-10-011210.3389/fnins.2018.00744410387Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric StudyFuxin Ren0Wen Ma1Muwei Li2Huaiqiang Sun3Qian Xin4Wei Zong5Weibo Chen6Guangbin Wang7Fei Gao8Bin Zhao9Shandong Medical Imaging Research Institute, Shandong University, Jinan, ChinaDepartment of Otolaryngology, Jinan Central Hospital, Shandong University, Jinan, ChinaVanderbilt University Institute of Imaging Science, Vanderbilt University, Nashville, TN, United StatesHuaxi MR Research Center, Department of Radiology, West China Hospital of Sichuan University, Chengdu, ChinaCentral Laboratory, The Second Hospital of Shandong University, Jinan, ChinaShandong Medical Imaging Research Institute, Shandong University, Jinan, ChinaPhilips Healthcare, Shanghai, ChinaShandong Medical Imaging Research Institute, Shandong University, Jinan, ChinaShandong Medical Imaging Research Institute, Shandong University, Jinan, ChinaShandong Medical Imaging Research Institute, Shandong University, Jinan, ChinaPresbycusis (PC) is characterized by bilateral sensorineural hearing loss at high frequencies and speech-perception difficulties in noisy environments and has a strikingly detrimental impact on cognitive function. As the neural consequences of PC may involve the whole brain, we hypothesized that patients with PC would show structural alterations not only in the auditory cortex but also in the cortexes involved in cognitive function. The purpose of this study was to use surface-based morphometry (SBM) analysis to elucidate whole-brain structural differences between patients with PC and age-matched normal hearing controls. Three-dimensional T1-weighted MR images of 26 patients with mild PC and 26 age-, sex- and education-matched healthy controls (HCs) were acquired. All participants underwent a battery of neuropsychological tests. Our results revealed gray matter atrophy in several auditory cortical areas, nodes of the default mode network (DMN), including the bilateral precuneus and inferior parietal lobule, the right posterior cingulate cortex (PCC), and the right insula of patients with PC compared to that in the HCs. Our findings also revealed that hearing loss was associated with reduced gray matter volume in the right primary auditory cortex of patients with PC. Moreover, structural alterations in the nodes of the DMN were associated with cognitive impairments in PC patients. Additionally, this study provides evidence that a thicker right insula is associated with better speech perception in patients with PC. Based on these findings, we argue that the onset of PC seems to trigger its own cascade of conditions, including a need for increased cognitive resources during speech comprehension, which might lead to auditory and cognition-related cortical reorganization.https://www.frontiersin.org/article/10.3389/fnins.2018.00744/fullpresbycusiscognitive impairmenthearing lossGM atrophysurface-based morphometry
spellingShingle Fuxin Ren
Wen Ma
Muwei Li
Huaiqiang Sun
Qian Xin
Wei Zong
Weibo Chen
Guangbin Wang
Fei Gao
Bin Zhao
Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
Frontiers in Neuroscience
presbycusis
cognitive impairment
hearing loss
GM atrophy
surface-based morphometry
title Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
title_full Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
title_fullStr Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
title_full_unstemmed Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
title_short Gray Matter Atrophy Is Associated With Cognitive Impairment in Patients With Presbycusis: A Comprehensive Morphometric Study
title_sort gray matter atrophy is associated with cognitive impairment in patients with presbycusis a comprehensive morphometric study
topic presbycusis
cognitive impairment
hearing loss
GM atrophy
surface-based morphometry
url https://www.frontiersin.org/article/10.3389/fnins.2018.00744/full
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