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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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Autores principales: Xu, Xiao-Min, Jiao, Yun, Tang, Tian-Yu, Zhang, Jian, Salvi, Richard, Teng, Gao-Jun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6391342/
https://www.ncbi.nlm.nih.gov/pubmed/30842724
http://dx.doi.org/10.3389/fnins.2019.00133
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author Xu, Xiao-Min
Jiao, Yun
Tang, Tian-Yu
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
author_facet Xu, Xiao-Min
Jiao, Yun
Tang, Tian-Yu
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
author_sort Xu, Xiao-Min
collection PubMed
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.
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spelling pubmed-63913422019-03-06 Inefficient Involvement of Insula in Sensorineural Hearing Loss Xu, Xiao-Min Jiao, Yun Tang, Tian-Yu Zhang, Jian Salvi, Richard Teng, Gao-Jun Front Neurosci Neuroscience 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. Frontiers Media S.A. 2019-02-20 /pmc/articles/PMC6391342/ /pubmed/30842724 http://dx.doi.org/10.3389/fnins.2019.00133 Text en Copyright © 2019 Xu, Jiao, Tang, Zhang, Salvi and Teng. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Xu, Xiao-Min
Jiao, Yun
Tang, Tian-Yu
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
Inefficient Involvement of Insula in Sensorineural Hearing Loss
title 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_short Inefficient Involvement of Insula in Sensorineural Hearing Loss
title_sort inefficient involvement of insula in sensorineural hearing loss
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6391342/
https://www.ncbi.nlm.nih.gov/pubmed/30842724
http://dx.doi.org/10.3389/fnins.2019.00133
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