Altered Functional Connectivity in Patients With Sloping Sensorineural Hearing Loss

Abstract

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.

Keywords: functional connectivity; neuronal plasticity; partial deafness; resting state; sensorineural hearing loss.

FIGURE 1

Pure Tone Audiometry results for (A) the whole patient group, (B) the patient group with prelingual onset of SNHL, (C) the patient group with postlingual onset of SNHL.

FIGURE 2

Between-group effects. Increased functional connectivity in normal hearing subjects, compared to the group of patients as a whole. Networks and seed regions are indicated below each slice. The target regions of altered FC are outlined in red for better visualization. The number of voxels is the size of the whole target region, and the name indicates the anatomical area the majority of the voxels belonged to. If the brain side of the target region is not stated, it was in both hemispheres.

FIGURE 3

Between-group effects. Increased functional connectivity in the group of patients as a whole, compared to normal hearing subjects. Networks and seed regions are indicated below each slice. The target regions of altered FC are outlined in red for better visualization. The number of voxels is the size of the whole target region, and the name indicates the anatomical area the majority of the voxels belonged to. If the brain side of the target region is not stated, it was found in both hemispheres.

FIGURE 4

Between-group effects. Increased functional connectivity in patients with Prelingual SNHL vs. Postlingual SNHL. Networks and seed regions are indicated below each slice. The target regions of altered FC are outlined in red for better visualization. The number of voxels is the size of the whole target region, and the name indicates the anatomical area that the majority of the voxels belonged to. If the brain side of the target region is not stated, it was found in both hemispheres.

FIGURE 5

Between-group effects. Increased functional connectivity in patients with Postlingual SNHL vs. Prelingual SNHL. Networks and seed regions are indicated below each slice. The target regions of altered FC are outlined in red for better visualization. The number of voxels is the size of the whole target region, and the name indicates the anatomical area the majority of the voxels belonged to. If the brain side of the target region is not stated, it was in found both hemispheres.