Normal tone-in-noise sensitivity in trained budgerigars despite substantial auditory-nerve injury: no evidence of hidden hearing loss.

2020 
Loss of auditory-nerve (AN) afferent cochlear innervation is a prevalent human condition that does not affect audiometric thresholds and therefore remains largely undetectable with standard clinical tests. AN loss is widely expected to cause hearing difficulties in noise, known as ‘hidden hearing loss’, but support for this hypothesis is controversial. Here, we used operant conditioning procedures to examine the perceptual impact of AN loss on behavioral tone-in-noise sensitivity in the budgerigar (Melopsittacus undulatus; of either sex), an avian animal model with complex hearing abilities similar to humans. Bilateral kainic-acid infusions depressed compound AN responses by 40-70% without impacting otoacoustic emissions or behavioral tone sensitivity in quiet. Surprisingly, animals with AN damage showed normal thresholds for tone detection in noise (0.1 ±1.0 dB re. control animals; mean difference ±standard error), even under a challenging roving-level condition with random stimulus variation across trials. Furthermore, decision-variable correlations showed no difference for AN-damaged animals in their use of energy and envelope cues to perform the task. These results show that AN damage has less impact on tone-in-noise detection than generally expected, even under a difficult roving-level condition known to impact TIN detection in individuals with sensorineural hearing loss. Perceptual deficits could emerge for different perceptual tasks or with greater AN loss, but are potentially minor compared to those caused by sensorineural hearing loss. Significance Statement Loss of auditory-nerve cochlear innervation is a common problem in humans that does not affect audiometric thresholds on a clinical hearing test. Auditory-nerve loss is widely expected to cause hearing problems in noise, known as ‘hidden hearing loss’, but existing studies are controversial. Here, using an avian animal model with complex hearing abilities similar to humans, we examined for the first time the impact of an experimentally induced auditory-nerve lesion on behavioral tone sensitivity in noise. Surprisingly, auditory-nerve lesioned animals showed no difference in hearing performance in noise or detection strategy compared to controls. These results show that perceptual deficits from auditory-nerve damage are smaller than generally expected, and potentially minor compared to those caused by sensorineural hearing loss.
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