Functional and Structural Brain Plasticity in Adult Onset Single-Sided Deafness.

Yingying Shang,Karuna Subramaniam,Srikantan S Nagarajan,Yi-Shin Chang,Steven W Cheung,Coleman Garrett,Chang Cai,Pratik Mukherjee,Leighton B Hinkley,Danielle Mizuiri,Julia P Owen

doi:10.3389/fnhum.2018.00474

Abstract

Single-sided deafness (SSD) or profound unilateral hearing loss obligates the only serviceable ear to capture all acoustic information. This loss of binaural function taxes cognitive resources for accurate listening performance, especially under adverse environments or challenging tasks. We hypothesized that adults with SSD would manifest both functional and structural brain plasticity compared to controls with normal binaural hearing. We evaluated functional alterations using magnetoencephalographic imaging (MEGI) of brain activation during performance of a moderately difficult auditory syllable sequence reproduction task and assessed structural integrity using diffusion tensor imaging (DTI). MEGI showed the SSD cohort to have increased induced oscillations in the theta band over the left superior temporal cortex and decreased induced gamma band oscillations over the frontal and parietal cortices between 175 and 475 ms following stimulus onset. DTI showed the SSD cohort to have extensive fractional anisotropy (FA) reduction in both auditory and non-auditory tracts and regions. Overlaying functional and structural changes revealed by the two imaging techniques demonstrated close registration of cortical areas and white matter tracts that expressed brain plasticity. Hence, complete loss of input from one ear in adulthood triggers both functional and structural alterations to dorsal temporal and frontal-parietal areas.

Highlights

Bilateral deafness or anacusis enforces undesirable auditory isolation and triggers widespread central network plasticity
After data quality assessments and exclusions were applied, magnetoencephalographic imaging (MEGI) data was analyzable in 24 single-sided deafness (SSD) patients and 14 normal hearing (NH) controls and diffusion tensor imaging (DTI) data was analyzable in 20 SSD patients and 12 NH controls
Based on comparable psychoacoustic performance in the two cohorts, we interpret functional and structural imaging differences between SSD and NH as whole brain changes attributable to SSD not confounded by task performance differences

Summary

Introduction

Bilateral deafness or anacusis enforces undesirable auditory isolation and triggers widespread central network plasticity. Some behavioral adaptations to single sensor hearing are deployment of cognitive and attentional resources to monitor the acoustic scene, readiness to orient to sounds of interest by making head or body adjustments, and use of visually guided lip-reading strategies to bolster accuracy. Despite those steps to mitigate challenges imposed by SSD, troublesome clinical consequences include greater difficulty with sound localization, higher signal-to-noise ratio requirement for speech discrimination, and reduced ease of listening (Rigby et al, 1997; Noble and Gatehouse, 2004; Tufarelli et al, 2006; Douglas et al, 2007). While the latter intervention reintroduces auditory information through the deaf ear, with promise for restoration of binaural hearing, treatment outcomes remain highly variable (van Zon et al, 2015; Cabral Junior et al, 2016)

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