Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar

Abstract

Auditory-nerve fibers are lost steadily with age and as a possible consequence of noise-induced glutamate excitotoxicity. Auditory-nerve loss in the absence of other cochlear pathologies is thought to be undetectable with a pure-tone audiogram while degrading real-world speech perception (hidden hearing loss). Perceptual deficits remain unclear, however, due in part to the limited behavioral capacity of existing rodent models to discriminate complex sounds. The budgerigar is an avian vocal learner with human-like behavioral sensitivity to many simple and complex sounds and the capacity to mimic speech. Previous studies in this species show that intracochlear kainic-acid infusion reduces wave 1 of the auditory brainstem response by 40-70%, consistent with substantial excitotoxic auditory-nerve damage. The present study used operantconditioning procedures in trained budgerigars to quantify kainic-acid effects on tone detection across frequency (0.25-8 kHz; the audiogram) and as a function of duration (20-160 ms; temporal integration). Tone thresholds in control animals were lowest from 1-4 kHz and decreased with increasing duration as in previous studies of the budgerigar. Behavioral results in kainic-acidexposed animals were as sensitive as in controls, suggesting preservation of the audiogram and temporal integration despite auditory-nerve loss associated with up to 70% wave 1 reduction. Distortion-product otoacoustic emissions were also preserved in kainic-acid exposed animals, consistent with normal hair-cell function. These results highlight considerable perceptual resistance of tone-detection performance with selective auditory-nerve loss. Future behavioral studies in budgerigars with auditory-nerve damage can use complex speech-like stimuli to help clarify aspects of auditory perception impacted by this common cochlear pathology.

The search for noise-induced cochlear synaptopathy in humans: Mission impossible?

“…Theoretical reasoning by Lopez-Poveda and Barrios (2013) and perceptual model simulations by Marmel et al (2015) suggest that synaptopathy involves a substantial loss of low-threshold AN fibers in addition to the larger loss of high-threshold fibers, which is predicted to elevate the detection threshold for brief tones, without significantly elevating the thresholds for longer sounds. The results of Wong et al (2019) in the budgerigar undermine this approach and the experimental data currently available are not adequate to allow a recommended protocol for this test.…”

Normal Tone-In-Noise Sensitivity in Trained Budgerigars despite Substantial Auditory-Nerve Injury: No Evidence of Hidden Hearing Loss

“…Similarly, most mice with .95% AN loss because of ouabain exposure show normal tone sensitivity in quiet (Chambers et al, 2016). Finally, a recent study in budgerigars found no impact of 40-70% AN damage from kainic acid (KA), even for tone durations as short as 20 ms (Wong et al, 2019). Other studies based on acoustic-startle responses have found diverse changes in behavioral reflex strength that vary with the magnitude of AN loss and specific test paradigm (Hickox and Liberman, 2014;Chambers et al, 2016;Lobarinas et al, 2017), but translation of startle results to auditory perception remains controversial Klump, 2015, 2016).…”

Effects of tone duration on three psychophysical measures of temporal integration in rhesus macaques

“…This speaks to the importance of using measures in addition to threshold when attempting to elucidate the effects of noise on auditory processing. Considering slope may become increasingly important in understanding the effects of hearing impairment, as recent hidden hearing loss studies have demonstrated a lack of effect on threshold measures of temporal integration (Marmel et al, 2020;Wong et al, 2019), but did not asses psychometric slope.…”