Animal models of hidden hearing loss: Does auditory-nerve-fiber loss cause real-world listening difficulties?

Afferent innervation of the cochlea by the auditory nerve declines during aging and potentially after sound overexposure, producing the common pathology known as cochlear synaptopathy. Auditory-nerve-fiber loss is difficult to detect with the clinical audiogram and has been proposed to cause 'hidden hearing loss' including impaired speech-in-noise perception. While evidence that auditory-nerve-fiber loss causes hidden hearing loss in humans is controversial, behavioral animal models hold promise to rigorously test this hypothesis because neural lesions can be induced and histologically validated. Here, we review recent animal behavioral studies on the impact of auditory-nerve-fiber loss on perception in a range of species. We first consider studies of tinnitus and hyperacusis inferred from acoustic startle reflexes, followed by a review of operant-conditioning studies of the audiogram, temporal integration for tones of varying duration, temporal resolution of gaps in noise, and tone-in-noise detection. Studies quantifying the audiogram show that tone-in-quiet sensitivity is unaffected by auditory-nerve-fiber loss unless neural lesions exceed 80%, at which point large deficits are possible. Changes in other aspects of perception, which were typically investigated for moderate-to-severe auditory-nerve-fiber loss of 50-70%, appear heterogeneous across studies and might be small compared to impairment caused by hair-cell pathologies. Future studies should pursue recent findings that behavioral sensitivity to brief tones and silent gaps in noise may be particularly vulnerable to auditory-nerve-fiber loss. Furthermore, aspects of auditory perception linked to central inhibition and fine neural response timing, such as modulation masking release and spatial hearing, may be productive directions for further animal behavioral research.