Users of cochlear implant (CI) face challenges in everyday situations such as understanding conversations in noise, even with CIs in both ears. These challenges are related to difficulties with tasks that require fine temporal processing such as discrimination of pulse rates or interaural time differences (ITD), a major cue for sound localization. The degradation in temporal processing and ITD sensitivity are especially acute in those who lost hearing in early childhood. Here, we characterized temporal coding and ITD sensitivity of single neurons in a novel animal model of early-onset deafness. Rabbits were deafened as neonates and deprived of auditory stimulation until they reached adult age when singleunit recordings from the auditory midbrain were made chronically using an unanesthetized preparation. The results are compared to measurements from adult-deafened rabbits with normal auditory development to understand the effect of early-onset deafness on neural temporal coding and ITD sensitivity. Neurons in the inferior colliculus (IC) of earlydeafened rabbits were less likely to show sustained, excitatory responses to pulse train stimulation and more likely to show suppressive responses compared to neurons in adult-deaf animals. Fewer neurons showed synchronized responses to pulse trains at any rate in the early-deaf group. In addition, fewer neurons showed significant ITD sensitivity in their overall firing rate in the early-deaf group compared to adult-deaf animals. Neural ITD discrimination thresholds in the early-deaf group were poorer than thresholds in adult-deaf group, especially at high pulse rates. The overall degradation in neural ITD sensitivity is consistent with the difficulties encountered by human CI users with early-onset hearing loss. These results lay the groundwork for investigating whether the degradations in temporal coding and ITD sensitivity observed in early-deaf animals can be reversed by appropriate CI stimulation during development.
The pitch of harmonic complex tones (HCT) common in speech, music and animal vocalizations plays a key role in the perceptual organization of sound. Unraveling the neural mechanisms of pitch perception requires animal models but little is known about complex pitch perception by animals, and some species appear to use different pitch mechanisms than humans. Here, we tested rabbits' ability to discriminate the fundamental frequency (F0) of HCTs with missing fundamentals using a behavioral paradigm inspired by foraging behavior in which rabbits learned to harness a spatial gradient in F0 to find the location of a virtual target within a room for a food reward. Rabbits were initially trained to discriminate HCTs with F0s in the range 400-800 Hz and with harmonics covering a wide frequency range (800-16,000 Hz), and then tested with stimuli differing either in spectral composition to test the role of harmonic resolvability (Experiment 1), or in F0 range (Experiment 2), or both F0 and spectral content (Experiment 3). Together, these experiments show that rabbits can discriminate HCTs over a wide F0 range (200-1600 Hz) encompassing the range of conspecific vocalizations, and can use either the spectral pattern of harmonics resolved by the cochlea for higher F0s or temporal envelope cues resulting from interaction between unresolved harmonics for lower F0s. The qualitative similarity of these results to human performance supports using rabbits as an animal model for studies of pitch mechanisms providing species differences in cochlear frequency selectivity and F0 range of vocalizations are taken into account.
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