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...
Main Authors: | , , , , , |
---|---|
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 |
id |
doaj-a09c991ca5714299960e8f7635c94109 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT xiaominxu inefficientinvolvementofinsulainsensorineuralhearingloss AT yunjiao inefficientinvolvementofinsulainsensorineuralhearingloss AT tianyutang inefficientinvolvementofinsulainsensorineuralhearingloss AT jianzhang inefficientinvolvementofinsulainsensorineuralhearingloss AT richardsalvi inefficientinvolvementofinsulainsensorineuralhearingloss AT gaojunteng inefficientinvolvementofinsulainsensorineuralhearingloss |
_version_ |
1725850626920808448 |