Cochlear synaptopathy impairs suprathreshold tone-in-noise coding in the cochlear nucleus.

Hearing impairment without threshold elevations can occur when there is damage to high-threshold auditory nerve fiber synapses with cochlear inner hair cells. Instead, cochlear synaptopathy produces suprathreshold deficits, especially in older patients, which affect conversational speech. Since listening in noise at suprathreshold levels presents significant challenges to the ageing population, we examined the effects of synaptopathy on tone-in-noise coding on the central recipients of auditory nerve fibers - the cochlear nucleus neurons. To induce synaptopathy, guinea pigs received a unilateral sound overexposure to the left ears. A separate group received sham exposures. At 4 weeks post-exposure, thresholds had recovered but reduced ABR wave 1 amplitudes and auditory nerve synapse loss remained on the left side. Single unit responses were recorded from several cell types in the ventral cochlear nucleus to puretone and noise stimuli. Receptive fields and rate-level functions in the presence of continuous broadband noise were examined. The synaptopathy-inducing noise exposure did not affect mean unit tone-in-noise thresholds, nor the tone-in-noise thresholds in each animal, demonstrating equivalent tone-in-noise detection thresholds to sham animals. However, synaptopathy reduced single-unit responses to suprathreshold tones in the presence of background noise, particularly in the cochlear nucleus small cells. These data demonstrate that suprathreshold tone-in-noise deficits following cochlear synaptopathy are evident in the first neural station of the auditory brain, the cochlear nucleus neurons, and provide a potential target for assessing and treating listening-in-noise deficits in humans. KEY POINTS: Recording from multiple central auditory neurons can determine any tone-in-noise deficits in animals with quantified cochlear synapse damage. Using this technique, we found that tone-in-noise thresholds are not altered by cochlear synaptopathy, whereas coding of suprathreshold tones-in-noise is disrupted. Suprathreshold deficits occur in small cells and primary-like neurons of the cochlear nucleus. These data provide important insights into the mechanisms underlying difficulties associated with hearing in noisy environments. Abstract figure legend A) Unilateral noise exposure induces synaptopathy and temporary threshold shift (TTS) in guinea pigs. B) Auditory thresholds of single units in the cochlear nucleus are shifted in background noise, and this shift is not affected by synaptopathy. C) Suprathreshold firing rates are decreased by background sound, and this decrease correlates with cochlear synaptopathy. This article is protected by copyright. All rights reserved.