Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss

BackgroundSensory 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 populatio...

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Main Authors: Tomasz Wolak, Katarzyna Cieśla, Agnieszka Pluta, Elżbieta Włodarczyk, Bharat Biswal, Henryk Skarżyński
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2019.00284/full
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spelling doaj-868bc3f9b531430fa34bea5d72c4514e2020-11-25T02:41:19ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612019-08-011310.3389/fnhum.2019.00284459450Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing LossTomasz Wolak0Katarzyna Cieśla1Agnieszka Pluta2Agnieszka Pluta3Elżbieta Włodarczyk4Bharat Biswal5Henryk Skarżyński6Institute of Physiology and Pathology of Hearing, Bioimaging Research Center, World Hearing Center, Warsaw, PolandInstitute of Physiology and Pathology of Hearing, Bioimaging Research Center, World Hearing Center, Warsaw, PolandInstitute of Physiology and Pathology of Hearing, Bioimaging Research Center, World Hearing Center, Warsaw, PolandFaculty of Psychology, University of Warsaw, Warsaw, PolandInstitute of Physiology and Pathology of Hearing, Bioimaging Research Center, World Hearing Center, Warsaw, PolandDepartment of Biomedical Engineering and Department of Radiology, New Jersey Medical School, NJIT, Newark, NJ, United StatesInstitute of Physiology and Pathology of Hearing, Bioimaging Research Center, World Hearing Center, Warsaw, PolandBackgroundSensory 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 MethodsTwenty 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.ResultsMost 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.ConclusionThe 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.https://www.frontiersin.org/article/10.3389/fnhum.2019.00284/fullfunctional connectivityresting statesensorineural hearing losspartial deafnessneuronal plasticity
collection DOAJ
language English
format Article
sources DOAJ
author Tomasz Wolak
Katarzyna Cieśla
Agnieszka Pluta
Agnieszka Pluta
Elżbieta Włodarczyk
Bharat Biswal
Henryk Skarżyński
spellingShingle Tomasz Wolak
Katarzyna Cieśla
Agnieszka Pluta
Agnieszka Pluta
Elżbieta Włodarczyk
Bharat Biswal
Henryk Skarżyński
Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
Frontiers in Human Neuroscience
functional connectivity
resting state
sensorineural hearing loss
partial deafness
neuronal plasticity
author_facet Tomasz Wolak
Katarzyna Cieśla
Agnieszka Pluta
Agnieszka Pluta
Elżbieta Włodarczyk
Bharat Biswal
Henryk Skarżyński
author_sort Tomasz Wolak
title Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss
title_short 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_sort altered functional connectivity in patients with sloping sensorineural hearing loss
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2019-08-01
description BackgroundSensory 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 MethodsTwenty 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.ResultsMost 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.ConclusionThe 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.
topic functional connectivity
resting state
sensorineural hearing loss
partial deafness
neuronal plasticity
url https://www.frontiersin.org/article/10.3389/fnhum.2019.00284/full
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