Cochlear deafferentation impairs perception of acoustic onset cues in kainate-exposed budgerigars

Synaptopathy is a common cochlear pathology involving damage, dysfunction, and loss of auditory-nerve synapses with sensory hair cells. Cochlear synaptopathy can occur following sound overexposure due to glutamate excitotoxicity. Synaptopathy is undetectable with the clinical audiogram and is widely hypothesized to cause "hidden hearing loss," i.e., impaired perception of speech and other complex sounds under challenging listening conditions. However, evidence that cochlear synaptopathy causes hidden hearing loss is mixed, and the specific aspects of auditory perception impacted by synaptopathy remain unknown. We quantified the effects of excitotoxic cochlear synaptopathy/deafferentation on behavioral tone-in-noise detection in trained budgerigars (Melopsittacus undulatus). The budgerigar is a parakeet species with the capacity to mimic speech and highly developed complex-sound discrimination abilities. Synaptopathy was induced through excitotoxicity with intracochlear kainic-acid infusions. Tone signals varied in duration and onset time relative to the start of the noise. Animals with cochlear synaptopathy showed normal detection of 200-ms tones regardless of whether tones were delayed by 100 ms relative to the start of the noise or had the same onset time as the noise. In contrast, detection of shorter 20-ms tones was normal for delayed tones but significantly impaired for tones sharing the same onset time as the noise. These results provide the first evidence to our knowledge that synaptopathy selectively impairs perception of acoustic onset cues. In humans, impaired perception of onset cues by cochlear synaptopathy would represent a major challenge to real-world communication due to the extensive information carried by acoustic onset cues in speech.