Neural ITD Sensitivity and Temporal Coding with Cochlear Implants in an Animal Model of Early-Onset Deafness

Abstract

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.

Chronic Bilateral Cochlear Implant Stimulation in Early-Deaf Rabbits Restores Neural Binaural Sensitivity

“…The ITD sensitivity of IC neurons to bilateral CI stimulation degrades with increasing pulse rates, consistent with limitations in perceptual ITD sensitivity in human CI listeners (Chung et al, 2016b). This rate-dependent degradation of ITD sensitivity is more severe in early- deafened and unstimulated animals than in adult-deafened rabbits (Chung et al, 2019). We compared the dependence of ITD sensitivity on pulse rates to investigate whether bilateral CI stimulation during develop can restore ITD sensitivity over a wide range of pulse rates.…”

“…The difference in relative fractions of excitatory/suppressive response might be driven by differences in spontaneous activity of the IC neurons. We have previously shown that there was no significant difference in spontaneous firing rates in AD, ED-US and normal hearing animals (Chung et al, 2019). Figure 7C compares the distribution of SR in three deafness groups and normal hearing rabbits.…”

“…We used an experimental "Fundamental Asynchronous Stimulus Timing" (FAST) strategy specifically designed to deliver ITD cues (Smith, 2010(Smith, , 2014. Neural ITD sensitivity and temporal coding metrics were compared to previous reported data from 117 neurons in three neonatally deafened and unstimulated rabbits (early-deaf, unstimulated, ED-US) (Chung et al 2019) and 180 neurons in four rabbits that were deafened as adults (adult-deaf, AD) (Chung et al 2016) (Figure 1). Detailed history of age at implantation and recording sessions for all groups of rabbits is given in adult deafened rabbits, the onset of deafness is the same as the age at implantation (i.e., all adultdeafened rabbits were deafened during the CI surgery).…”

“…We defined the excitatory/suppressive (E/S) ratio for each unit to characterize the relative prevalence of excitatory vs. suppressive responses across the pulse rates tested in the three animals groups (Chung et al 2019) ( Figure 7B). The E/S index ranges from −1 for purely suppressive response to +1 for purely excitatory response at all rates.…”

“…Single neurons in the central auditory pathway show similar limitations in how they encode bilateral CI stimulation. Degraded neural ITD sensitivity with bilateral CI stimulation has been observed in the auditory midbrain (Hancock, Noel, Ryugo, & Delgutte, 2010) and auditory cortex (Tillein et al, 2010) of congenitally deaf cats under anesthesia, and auditory midbrain of neonatally-deafened rabbits in an unanesthetized preparation (Chung, Buechel, Sunwoo, Wagner, & Delgutte, 2019).…”