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Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus

Sensorineural hearing loss (SNHL), sometimes accompanied with tinnitus, is associated with dysfunctions within and outside the classical auditory pathway. The salience network, which is anchored in bilateral anterior insula and dorsal anterior cingulate cortex, has been implicated in sensory integra...

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Autores principales: Xu, Xiao-Min, Jiao, Yun, Tang, Tian-Yu, Lu, Chun-Qiang, 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/PMC6433888/
https://www.ncbi.nlm.nih.gov/pubmed/30941010
http://dx.doi.org/10.3389/fnins.2019.00246
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author Xu, Xiao-Min
Jiao, Yun
Tang, Tian-Yu
Lu, Chun-Qiang
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
author_facet Xu, Xiao-Min
Jiao, Yun
Tang, Tian-Yu
Lu, Chun-Qiang
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
author_sort Xu, Xiao-Min
collection PubMed
description Sensorineural hearing loss (SNHL), sometimes accompanied with tinnitus, is associated with dysfunctions within and outside the classical auditory pathway. The salience network, which is anchored in bilateral anterior insula and dorsal anterior cingulate cortex, has been implicated in sensory integration. Partial auditory deprivation could alter the characteristics of the salience network and other related brain areas, thereby contributing to hearing impairments-induced neuropsychiatric symptoms. To test this hypothesis, we performed fMRI scanning and neuropsychological tests on 32 subjects with long-term bilateral hearing impairment and 30 well-matched Controls. Non-directional functional connectivity and directional Granger causality analysis were used to identify aberrant spatial and temporal patterns of connections targeting bilateral anterior insula and dorsal anterior cingulate cortex. We found that the left anterior insula showed decreased connectivity with right precentral gyrus and superior frontal gyrus. The connections between the dorsal anterior cingulate cortex and middle frontal gyrus, superior parietal gyrus and supplementary motor area (SMA) were also reduced. Relative to Controls, SNHL patients showed abnormal effective connectivity of the salience network, including inferior temporal gyrus, cerebellum lobule VI, lobule VIII, precentral gyrus, middle frontal gyrus and SMA. Furthermore, correlation analysis demonstrated that some of these atypical connectivity measures were correlated with performance of neuropsychiatric tests. These findings suggest that the inefficient modulation of the salience network might contribute to the neural basis of SNHL and tinnitus, as well as associated cognition and emotion deficits.
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spelling pubmed-64338882019-04-02 Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus Xu, Xiao-Min Jiao, Yun Tang, Tian-Yu Lu, Chun-Qiang Zhang, Jian Salvi, Richard Teng, Gao-Jun Front Neurosci Neuroscience Sensorineural hearing loss (SNHL), sometimes accompanied with tinnitus, is associated with dysfunctions within and outside the classical auditory pathway. The salience network, which is anchored in bilateral anterior insula and dorsal anterior cingulate cortex, has been implicated in sensory integration. Partial auditory deprivation could alter the characteristics of the salience network and other related brain areas, thereby contributing to hearing impairments-induced neuropsychiatric symptoms. To test this hypothesis, we performed fMRI scanning and neuropsychological tests on 32 subjects with long-term bilateral hearing impairment and 30 well-matched Controls. Non-directional functional connectivity and directional Granger causality analysis were used to identify aberrant spatial and temporal patterns of connections targeting bilateral anterior insula and dorsal anterior cingulate cortex. We found that the left anterior insula showed decreased connectivity with right precentral gyrus and superior frontal gyrus. The connections between the dorsal anterior cingulate cortex and middle frontal gyrus, superior parietal gyrus and supplementary motor area (SMA) were also reduced. Relative to Controls, SNHL patients showed abnormal effective connectivity of the salience network, including inferior temporal gyrus, cerebellum lobule VI, lobule VIII, precentral gyrus, middle frontal gyrus and SMA. Furthermore, correlation analysis demonstrated that some of these atypical connectivity measures were correlated with performance of neuropsychiatric tests. These findings suggest that the inefficient modulation of the salience network might contribute to the neural basis of SNHL and tinnitus, as well as associated cognition and emotion deficits. Frontiers Media S.A. 2019-03-19 /pmc/articles/PMC6433888/ /pubmed/30941010 http://dx.doi.org/10.3389/fnins.2019.00246 Text en Copyright © 2019 Xu, Jiao, Tang, Lu, 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
Lu, Chun-Qiang
Zhang, Jian
Salvi, Richard
Teng, Gao-Jun
Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title_full Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title_fullStr Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title_full_unstemmed Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title_short Altered Spatial and Temporal Brain Connectivity in the Salience Network of Sensorineural Hearing Loss and Tinnitus
title_sort altered spatial and temporal brain connectivity in the salience network of sensorineural hearing loss and tinnitus
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6433888/
https://www.ncbi.nlm.nih.gov/pubmed/30941010
http://dx.doi.org/10.3389/fnins.2019.00246
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