Inefficient Involvement of Insula in Sensorineural Hearing Loss

The insular cortex plays an important role in multimodal sensory processing, audio-visual integration and emotion; however, little is known about how the insula is affected by auditory deprivation due to sensorineural hearing loss (SNHL). To address this issue, we used structural and functional magn...

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Main Authors: Xiao-Min Xu, Yun Jiao, Tian-Yu Tang, Jian Zhang, Richard Salvi, Gao-Jun Teng
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.00133/full
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spelling doaj-a09c991ca5714299960e8f7635c941092020-11-24T21:58:42ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-02-011310.3389/fnins.2019.00133434999Inefficient Involvement of Insula in Sensorineural Hearing LossXiao-Min Xu0Yun Jiao1Tian-Yu Tang2Jian Zhang3Richard Salvi4Gao-Jun Teng5Jiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, ChinaJiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, ChinaJiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, ChinaJiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, ChinaCenter for Hearing and Deafness, University at Buffalo, Buffalo, NY, United StatesJiangsu Key Laboratory of Molecular and Functional Imaging, Department of Radiology, Zhongda Hospital, Medical School of Southeast University, Nanjing, ChinaThe insular cortex plays an important role in multimodal sensory processing, audio-visual integration and emotion; however, little is known about how the insula is affected by auditory deprivation due to sensorineural hearing loss (SNHL). To address this issue, we used structural and functional magnetic resonance imaging to determine if the neural activity within the insula and its interregional functional connectivity (FC) was disrupted by SNHL and if these alterations were correlated clinical measures of emotion and cognition. Thirty-five SNHL subjects and 54 Controls enrolled in our study underwent auditory evaluation, neuropsychological assessments, functional and structure MRI, respectively. Twenty five patients and 20 Controls underwent arterial spin labeling scanning. FC of six insula subdivisions were assessed and the FC results were compared to the neuropsychological tests. Interregional connections were also compared among insula-associated networks, including salience network (SN), default mode network (DMN), and central executive network (CEN). Compared to Controls, SNHL subjects demonstrated hyperperfusion in the insula and significantly decreased FC between some insula subdivisions and other brain regions, including thalamus, putamen, precentral gyrus, postcentral gyrus, mid-cingulate cortex, dorsolateral prefrontal cortex, rolandic operculum. Anxiety, depression and cognitive impairments were correlated with FC values. Abnormal interactions among SN, DMN, and CEN were observed in SNHL group. Our result provides support for the “inefficient high-order control” theory of the insula in which the auditory deprivation caused by SNHL contributes to impaired sensory integration and central deficits in emotional and cognitive processing.https://www.frontiersin.org/article/10.3389/fnins.2019.00133/fullsensorineural hearing lossinsulahyperperfusionfunctional connectivitycognitionemotion
collection DOAJ
language English
format Article
sources DOAJ
author Xiao-Min Xu
Yun Jiao
Tian-Yu Tang
Jian Zhang
Richard Salvi
Gao-Jun Teng
spellingShingle Xiao-Min Xu
Yun Jiao
Tian-Yu Tang
Jian Zhang
Richard Salvi
Gao-Jun Teng
Inefficient Involvement of Insula in Sensorineural Hearing Loss
Frontiers in Neuroscience
sensorineural hearing loss
insula
hyperperfusion
functional connectivity
cognition
emotion
author_facet Xiao-Min Xu
Yun Jiao
Tian-Yu Tang
Jian Zhang
Richard Salvi
Gao-Jun Teng
author_sort Xiao-Min Xu
title Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_short Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_full Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_fullStr Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_full_unstemmed Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_sort inefficient involvement of insula in sensorineural hearing loss
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2019-02-01
description The insular cortex plays an important role in multimodal sensory processing, audio-visual integration and emotion; however, little is known about how the insula is affected by auditory deprivation due to sensorineural hearing loss (SNHL). To address this issue, we used structural and functional magnetic resonance imaging to determine if the neural activity within the insula and its interregional functional connectivity (FC) was disrupted by SNHL and if these alterations were correlated clinical measures of emotion and cognition. Thirty-five SNHL subjects and 54 Controls enrolled in our study underwent auditory evaluation, neuropsychological assessments, functional and structure MRI, respectively. Twenty five patients and 20 Controls underwent arterial spin labeling scanning. FC of six insula subdivisions were assessed and the FC results were compared to the neuropsychological tests. Interregional connections were also compared among insula-associated networks, including salience network (SN), default mode network (DMN), and central executive network (CEN). Compared to Controls, SNHL subjects demonstrated hyperperfusion in the insula and significantly decreased FC between some insula subdivisions and other brain regions, including thalamus, putamen, precentral gyrus, postcentral gyrus, mid-cingulate cortex, dorsolateral prefrontal cortex, rolandic operculum. Anxiety, depression and cognitive impairments were correlated with FC values. Abnormal interactions among SN, DMN, and CEN were observed in SNHL group. Our result provides support for the “inefficient high-order control” theory of the insula in which the auditory deprivation caused by SNHL contributes to impaired sensory integration and central deficits in emotional and cognitive processing.
topic sensorineural hearing loss
insula
hyperperfusion
functional connectivity
cognition
emotion
url https://www.frontiersin.org/article/10.3389/fnins.2019.00133/full
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AT richardsalvi inefficientinvolvementofinsulainsensorineuralhearingloss
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