Abstract
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.
Highlights
The brain develops the capability of a complex form based on its genetic makeup, that is modified by its sensory experience (Kral and Eggermont, 2007; Ballantyne et al, 2008)
One MRI technique, which may serve as a window into experience-related brain development and plasticity, is resting state functional magnetic resonance imaging
We suggest that the demonstrated enhanced collaboration between the multisensory and “unisensory” brain areas in this specific hearing impaired population reflects, (a) processing of vibrotactile and spatial aspects of acoustic signal, such as people’s gestures or music-induced vibration, (b) experience with lip-reading and face feature analysis, (c) enhanced sensory-motor-visual integration (Verger et al, 2017; Xie et al, 2019)
Summary
The brain develops the capability of a complex form based on its genetic makeup, that is modified by its sensory experience (Kral and Eggermont, 2007; Ballantyne et al, 2008). One MRI technique, which may serve as a window into experience-related brain development and plasticity, is resting state functional magnetic resonance imaging (rs-fMRI). It measures low-frequency spontaneous fluctuations of blood oxygen level-dependent (BOLD) signals across the whole brain. Rs-fMRI benefits from the fact that the brain at rest retains its inherent functional organization ( termed, functional connectivity, FC) and temporal correlations between various brain regions are hypothesized to reflect prior coincidental neural firing 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
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