Hidden Hearing Loss Impacts the Neural Representation of Speech in Background Noise

Jessica J.M Monaghan,Jose A Garcia-Lazaro,David Mcalpine,Roland Schaette

doi:10.1016/j.cub.2020.09.046

Jessica J.M Monaghan, Jose A Garcia-Lazaro + Show 2 more

Open Access

https://doi.org/10.1016/j.cub.2020.09.046

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Abstract

SummaryMany individuals with seemingly normal hearing abilities struggle to understand speech in noisy backgrounds. To understand why this might be the case, we investigated the neural representation of speech in the auditory midbrain of gerbils with “hidden hearing loss” through noise exposure that increased hearing thresholds only temporarily. In noise-exposed animals, we observed significantly increased neural responses to speech stimuli, with a more pronounced increase at moderate than at high sound intensities. Noise exposure reduced discriminability of neural responses to speech in background noise at high sound intensities, with impairment most severe for tokens with relatively greater spectral energy in the noise-exposure frequency range (2–4 kHz). At moderate sound intensities, discriminability was surprisingly improved, which was unrelated to spectral content. A model combining damage to high-threshold auditory nerve fibers with increased response gain of central auditory neurons reproduced these effects, demonstrating that a specific combination of peripheral damage and central compensation could explain listening difficulties despite normal hearing thresholds.

Highlights

Understanding speech is one of the most important roles of the human auditory system
A simple phenomenological model of cochlear synaptopathy and enhanced central gain could reproduce this pattern of improved discrimination performance at moderate levels and decreased performance at high sound intensities, linking the effects of peripheral pathology and central plasticity. These results show that noise exposure designed to elicit hidden hearing loss (HHL) causes a selective deficit in neural encoding at high sound intensities in the frequency range affected by the noise exposure, which could explain listening difficulties in background noise despite normal hearing thresholds
Neural responses were recorded from the IC to a range of sounds from 4 animals exposed to 2 h of 105 dB SPL octave-band (2–4 kHz) noise 4 weeks prior to recording and from 4 control animals subjected to a sham noise exposure

Summary

Introduction

Understanding speech is one of the most important roles of the human auditory system In quiet environments, this task is relatively straightforward, even for individuals whose peripheral auditory system is severely impaired, such as users of cochlear implants [1]. Recent findings suggest that some of these difficulties might arise from exposure to loud sounds [8], which in animal studies has been shown to cause permanent damage to synaptic contacts between auditory-nerve fibers (ANFs) and the sensory hair cells of the cochlea [9, 10] This ‘‘cochlear synaptopathy’’ precedes the more commonly considered form of sensorineural deafness associated with damage to, or loss of, the hair cells themselves [11] and leads to a form of hidden hearing loss (HHL)—hidden because it is undetected by conventional tests such as audiometry, which measures the quietest sounds that can be heard. Investigations of controlled noise exposure on neural responses in experimental animal models have not assessed processing of complex sounds such as speech, being confined largely to relatively simple acoustic signals such as tones ( see [17])

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