Persistent Auditory Nerve Damage Following Kainic Acid Excitotoxicity in the Budgerigar (Melopsittacus undulatus)

Permanent loss of auditory nerve (AN) fibers occurs with increasing age and sound overexposure, sometimes without hair cell damage or associated audiometric threshold elevation. Rodent studies suggest effects of AN damage on central processing and behavior, but these species have limited capacity to discriminate low-frequency speech-like sounds. Here, we introduce a new animal model of AN damage in an avian communication specialist, the budgerigar (Melopsittacus undulatus). The budgerigar is a vocal learner and speech mimic with sensitive low-frequency hearing and human-like behavioral sensitivity to many complex signals including speech components. Excitotoxic AN damage was induced through bilateral cochlear infusions of kainic acid (KA). Acute KA effects on cochlear function were assessed using AN compound action potentials (CAPs) and hair cell cochlear microphonics (CMs). Long-term KA effects were assessed using auditory brainstem response (ABR) measurements for up to 31 weeks post-KA exposure. KA infusion immediately abolished AN CAPs while having mild impact on the CM. ABR wave I, the far-field AN response, showed a pronounced 40-75 % amplitude reduction at moderate-to-high sound levels that persisted for the duration of the study. In contrast, wave I latency and the amplitude of wave V were nearly unaffected by KA, and waves II-IV were less reduced than wave I. ABR thresholds, calculated based on complete response waveforms, showed no impairment following KA. These results demonstrate that KA exposure in the budgerigar causes irreversible AN damage, most likely through excitotoxic injury to afferent fibers or synapses as in other species, while sparing ABR thresholds. Normal wave V amplitude, assumed to originate centrally, may persist through compensatory mechanisms that restore central response amplitude by downregulating inhibition. Future studies in this new animal model of AN damage can explore effects of this neural lesion, in isolation from hair cell trauma and threshold elevation, on central processing and perception of complex sounds.