Neural Coding of Interaural Time Differences with Bilateral Cochlear Implants: Effects of Congenital Deafness

Abstract

Human bilateral cochlear implant users do poorly on tasks involving interaural time differences (ITD), a cue that provides important benefits to the normal hearing, especially in challenging acoustic environments, yet the precision of neural ITD coding in acutely deafened, bilaterally implanted cats is essentially normal (Smith and Delgutte, 2007a). One explanation for this discrepancy is that the extended periods of binaural deprivation typically experienced by cochlear implant users degrades neural ITD sensitivity, by either impeding normal maturation of the neural circuitry or altering it later in life. To test this hypothesis, we recorded from single units in inferior colliculus of two groups of bilaterally implanted, anesthetized cats that contrast maximally in binaural experience: acutely deafened cats, which had normal binaural hearing until experimentation, and congenitally deaf white cats, which received no auditory inputs until the experiment. Rate responses of only half as many neurons showed significant ITD sensitivity to low-rate pulse trains in congenitally deaf cats compared with acutely deafened cats. For neurons that were ITD sensitive, ITD tuning was broader and best ITDs were more variable in congenitally deaf cats, leading to poorer ITD coding within the naturally occurring range. A signal detection model constrained by the observed physiology supports the idea that the degraded neural ITD coding resulting from deprivation of binaural experience contributes to poor ITD discrimination by human implantees.

Modeling Binaural Responses in the Auditory Brainstem to Electric Stimulation of the Auditory Nerve

“…The ITD signal-to-total variance ratio (STVR) is a metric based on analysis of variance that has been used to characterize ITD sensitivity of neural data (Hancock et al 2010). ITD STVR represents the fraction of the variance in neural spike counts due to variation in stimulus ITD, as opposed to random The second metric, the signed ITD modulation depth (sMD), was used to characterize the shapes of ITD tuning curves, specifically to distinguish peakshaped from trough-shaped curves.…”

“…While many IC neurons show an upper rate limit near 200-300 pps beyond which they only give an onset response to electric pulse trains (Snyder et al 1995;Hancock et al 2012;Chung et al 2014b), ITD sensitivity for low-rate pulse trains appears to be largely independent of tonotopic position (Smith and Delgutte 2007;Hancock et al 2010). Moreover, there is no evidence that higher CF IC neurons show better ITD tuning to higher rate pulse trains, at least in anesthetized preparations Hancock et al 2010). Overall, there is little physiological evidence for a tonotopic dependence in the range of electric pulse rates over which neurons show ITD sensitivity as predicted by our modeling results.…”

“…This hypothesis is most relevant to cases of adult-onset deafness of relatively short duration to minimize developmental abnormalities and degenerative changes in the binaural pathways resulting from prolonged deafness (Hancock et al 2010(Hancock et al , 2013Tillein et al 2010). Specifically, we hypothesize that the limitations on ITD sensitivity in single cells in acutely deafened animals and postlingually deaf human subjects could be mainly due to the abnormal properties of auditory nerve fiber (ANF) responses to electric stimulation.…”

Congenital and Prolonged Adult-Onset Deafness Cause Distinct Degradations in Neural ITD Coding with Bilateral Cochlear Implants

“…Bilaterally implanted cats acutely deafened as adults show a high incidence of IC neurons sensitive to ITDs of electric pulse trains, and the ITD tuning of these neurons is as precise as in normal-hearing, acoustically stimulated cats (Smith and Delgutte 2007). In contrast, neural ITD coding with bilateral CI is severely degraded in congenitally deaf white cats, where fewer neurons are ITD sensitive (Hancock et al 2010). Furthermore, in both IC and auditory cortex of congenitally deaf cats, best ITDs of sensitive neurons are broadly distributed around the midline, lacking the bias for contralateral-leading ITDs observed in normal-hearing and acutely deafened cats (Tillein et al 2009;Hancock et al 2010).…”

“…Most congenitally deaf children who use their implants daily do not learn to lateralize based on ITD, even though they do lateralize based on ILD (Salloum et al 2010). Animal models of bilateral CI show parallel deficits in ITD coding by inferior colliculus (IC) and auditory cortex neurons (Tillein et al 2009;Hancock et al 2010). Bilaterally implanted cats acutely deafened as adults show a high incidence of IC neurons sensitive to ITDs of electric pulse trains, and the ITD tuning of these neurons is as precise as in normal-hearing, acoustically stimulated cats (Smith and Delgutte 2007).…”