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

Abstract

Bilateral cochlear implant (CI) users perform poorly on tasks involving interaural time differences (ITD), which are critical for sound localization and speech reception in noise by normal-hearing listeners. ITD perception with bilateral CI is influenced by age at onset of deafness and duration of deafness. We previously showed that ITD coding in the auditory midbrain is degraded in congenitally deaf white cats (DWC) compared to acutely deafened cats (ADC) with normal auditory development (Hancock et al., J. Neurosci, 30:14068). To determine the relative importance of early onset of deafness and prolonged duration of deafness for abnormal ITD coding in DWC, we recorded from single units in the inferior colliculus of cats deafened as adults 6 months prior to experimentation (long-term deafened cats, LTDC) and compared neural ITD coding between the three deafness models. The incidence of ITD-sensitive neurons was similar in both groups with normal auditory development (LTDC and ADC), but significantly diminished in DWC. In contrast, both groups that experienced prolonged deafness (LTDC and DWC) had broad distributions of best ITDs around the midline, unlike the more focused distributions biased toward contralateral-leading ITDs present in both ADC and normalhearing animals. The lack of contralateral bias in LTDC and DWC results in reduced sensitivity to changes in ITD within the natural range. The finding that early onset of deafness more severely degrades neural ITD coding than prolonged duration of deafness argues for the importance of fitting deaf children with sound processors that provide reliable ITD cues at an early age.

Delayed cochlear implantation in post-meningitic deafness and hereditary complement C2 deficiency

“…This is a well-known phenomenon, related with the reduced survival rate of spiral ganglion cells in postmeningitic cochleas. [28][29][30] The personal experience with CIs after long-term deprivation was also quite disappointing: in agreement with the literature [31][32][33], none of our pre-verbal children receiving a CI after 10 years of age ever equalled the speech perception performances of earlier CI recipients (below 3 years of age at surgery).…”

Multisensory Training Improves Auditory Spatial Processing following Bilateral Cochlear Implantation

“…For example, ultrastructural studies in congenitally deaf cats have shown that neurons in the medial superior olive, a brainstem nucleus involved in processing interaural time differences, exhibit abnormalities in the number and size of their synaptic inputs, which can be partially reversed after prolonged intracochlear electrical stimulation (Tirko and Ryugo, 2012). Recordings from neurons in the inferior colliculus of bilaterally implanted adult animals have demonstrated that ITD sensitivity in congenitally deaf cats is degraded compared with that seen in acutely deafened animals (Hancock et al, 2010(Hancock et al, , 2013. Because neural ITD coding was less severely altered in cats that were deafened as adults 6 months before recording (Hancock et al, 2013), it appears that early auditory experience is critical for the development of neural sensitivity to this localization cue.…”

“…Recordings from neurons in the inferior colliculus of bilaterally implanted adult animals have demonstrated that ITD sensitivity in congenitally deaf cats is degraded compared with that seen in acutely deafened animals (Hancock et al, 2010(Hancock et al, , 2013. Because neural ITD coding was less severely altered in cats that were deafened as adults 6 months before recording (Hancock et al, 2013), it appears that early auditory experience is critical for the development of neural sensitivity to this localization cue.…”

“…To determine whether there were also group differences in spatial resolution that might account for the behavioral results, we obtained a discriminability index (d ILD Ј ) of neuronal populations based on the range of firing rates in response to repeat presentations of each unique stimulus (Hancock et al, 2010). This was calculated as follows:…”

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

“…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.…”