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Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss

BACKGROUND: Sensory deprivation, such as hearing loss, has been demonstrated to change the intrinsic functional connectivity (FC) of the brain, as measured with resting-state functional magnetic resonance imaging (rs-fMRI). Patients with sloping sensorineural hearing loss (SNHL) are a unique populat...

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Autores principales: Wolak, Tomasz, Cieśla, Katarzyna, Pluta, Agnieszka, Włodarczyk, Elżbieta, Biswal, Bharat, Skarżyński, Henryk
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6713935/
https://www.ncbi.nlm.nih.gov/pubmed/31507391
http://dx.doi.org/10.3389/fnhum.2019.00284
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author Wolak, Tomasz
Cieśla, Katarzyna
Pluta, Agnieszka
Włodarczyk, Elżbieta
Biswal, Bharat
Skarżyński, Henryk
author_facet Wolak, Tomasz
Cieśla, Katarzyna
Pluta, Agnieszka
Włodarczyk, Elżbieta
Biswal, Bharat
Skarżyński, Henryk
author_sort Wolak, Tomasz
collection PubMed
description BACKGROUND: Sensory deprivation, such as hearing loss, has been demonstrated to change the intrinsic functional connectivity (FC) of the brain, as measured with resting-state functional magnetic resonance imaging (rs-fMRI). Patients with sloping sensorineural hearing loss (SNHL) are a unique population among the hearing impaired, as they have all been exposed to some auditory input throughout their lifespan and all use spoken language. MATERIALS AND METHODS: Twenty patients with SNHL and 21 control subjects participated in a rs-fMRI study. Whole-brain seed-driven FC maps were obtained, with audiological scores of patients, including hearing loss severity and speech performance, used as covariates. RESULTS: Most profound differences in FC were found between patients with prelingual (before language development, PRE) vs. postlingual onset (after language development, POST) of SNHL. An early onset was related to enhancement in long-range network connections, including the default-mode network, the dorsal-attention network and the fronto-parietal network, as well as in local sensory networks, the visual and the sensorimotor. A number of multisensory brain regions in frontal and parietal cortices, as well as the cerebellum, were also more internally connected. We interpret these effects as top-down mechanisms serving optimization of multisensory experience in SNHL with a prelingual onset. At the same time, POST patients showed enhanced FC between the salience network and multisensory parietal areas, as well as with the hippocampus, when they were compared to those with PRE hearing loss. Signal in several cortex regions subserving visual processing was also more intra-correlated in POST vs. PRE patients. This outcome might point to more attention resources directed to multisensory as well as memory experience. Finally, audiological scores correlated with FC in several sensory and high-order brain regions in all patients. CONCLUSION: The results show that a sloping hearing loss is related to altered resting-state brain organization. Effects were shown in attention and cognitive control networks, as well as visual and sensorimotor regions. Specifically, we found that even in a partial hearing deficit (affecting only some of the hearing frequency ranges), the age at the onset affects the brain function differently, pointing to the role of sensitive periods in brain development.
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spelling pubmed-67139352019-09-10 Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss Wolak, Tomasz Cieśla, Katarzyna Pluta, Agnieszka Włodarczyk, Elżbieta Biswal, Bharat Skarżyński, Henryk Front Hum Neurosci Neuroscience BACKGROUND: Sensory deprivation, such as hearing loss, has been demonstrated to change the intrinsic functional connectivity (FC) of the brain, as measured with resting-state functional magnetic resonance imaging (rs-fMRI). Patients with sloping sensorineural hearing loss (SNHL) are a unique population among the hearing impaired, as they have all been exposed to some auditory input throughout their lifespan and all use spoken language. MATERIALS AND METHODS: Twenty patients with SNHL and 21 control subjects participated in a rs-fMRI study. Whole-brain seed-driven FC maps were obtained, with audiological scores of patients, including hearing loss severity and speech performance, used as covariates. RESULTS: Most profound differences in FC were found between patients with prelingual (before language development, PRE) vs. postlingual onset (after language development, POST) of SNHL. An early onset was related to enhancement in long-range network connections, including the default-mode network, the dorsal-attention network and the fronto-parietal network, as well as in local sensory networks, the visual and the sensorimotor. A number of multisensory brain regions in frontal and parietal cortices, as well as the cerebellum, were also more internally connected. We interpret these effects as top-down mechanisms serving optimization of multisensory experience in SNHL with a prelingual onset. At the same time, POST patients showed enhanced FC between the salience network and multisensory parietal areas, as well as with the hippocampus, when they were compared to those with PRE hearing loss. Signal in several cortex regions subserving visual processing was also more intra-correlated in POST vs. PRE patients. This outcome might point to more attention resources directed to multisensory as well as memory experience. Finally, audiological scores correlated with FC in several sensory and high-order brain regions in all patients. CONCLUSION: The results show that a sloping hearing loss is related to altered resting-state brain organization. Effects were shown in attention and cognitive control networks, as well as visual and sensorimotor regions. Specifically, we found that even in a partial hearing deficit (affecting only some of the hearing frequency ranges), the age at the onset affects the brain function differently, pointing to the role of sensitive periods in brain development. Frontiers Media S.A. 2019-08-22 /pmc/articles/PMC6713935/ /pubmed/31507391 http://dx.doi.org/10.3389/fnhum.2019.00284 Text en Copyright © 2019 Wolak, Cieśla, Pluta, Włodarczyk, Biswal and Skarżyński. 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
Wolak, Tomasz
Cieśla, Katarzyna
Pluta, Agnieszka
Włodarczyk, Elżbieta
Biswal, Bharat
Skarżyński, Henryk
Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_full Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_fullStr Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_full_unstemmed Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_short Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_sort altered functional connectivity in patients with sloping sensorineural hearing loss
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6713935/
https://www.ncbi.nlm.nih.gov/pubmed/31507391
http://dx.doi.org/10.3389/fnhum.2019.00284
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