Otoacoustic emissions but not behavioral measurements predict cochlear-nerve frequency tuning in an avian vocal-communication specialist

Abstract

Frequency analysis by the cochlea forms a key foundation for all subsequent auditory processing. Stimulus-frequency otoacoustic emissions (SFOAEs) are a potentially powerful alternative to traditional behavioral experiments for estimating cochlear tuning without invasive testing, as is necessary in humans. Which methods accurately predict cochlear tuning remains controversial due to only a single animal study comparing SFOAE-based, behavioral, and cochlear frequency tuning in the same species. The budgerigar (Melopsittacus undulatus) is a parakeet species with human-like behavioral sensitivity to many sounds and the capacity to mimic speech. Multiple studies show that budgerigars exhibit a perceptual auditory fovea with sharpest behavioral frequency tuning at mid frequencies from 3.5-4 kHz, in contrast to the typical pattern of monotonically increasing tuning sharpness for higher characteristic frequencies. We measured SFOAE-based and cochlear-afferent tuning in budgerigars, for comparison to previously reported behavioral results. SFOAE-based and cochlear-afferent tuning sharpness both increased monotonically for higher frequencies, in contrast to the behavioral pattern. Thus, SFOAE-based tuning in budgerigars accurately predicted cochlear frequency tuning, and both measures aligned with typical patterns of cochlear tuning in other species. Given divergent behavioral tuning in budgerigars, which could reflect specializations for central processing of masked signals, these results highlight the value of SFOAEs for estimating cochlear tuning and caution against direct inference of cochlear tuning from behavioral results.