Interaural time difference sensitivity under binaural cochlear implant stimulation persists at high pulse rates up to 900 pps

Abstract

Spatial hearing remains one of the major challenges for bilateral cochlear implant (biCI) users, and early deaf patients in particular are often completely insensitive to interaural time differences (ITDs) delivered through biCIs. One popular theory held is that this may be due to a lack of early binaural experience. However, previously we have shown that neonatally deafened rats fitted with biCIs in adulthood quickly learn to discriminate ITDs as well as their normal hearing litter mates (Rosskothen-Kuhl et al. 2021), and perform orders of magnitude better than human biCI users. Our unique behaving biCI rat model allows us to investigate other possible limiting factors of prosthetic binaural hearing, such as the effect of stimulus pulse rate and envelope shape. Previous work has indicated that ITD sensitivity may decline substantially at the high pulse rates often used in clinical practice. We therefore measured behavioral ITD thresholds in neonatally deafened, adult implanted biCI rats to pulse trains of 50, 300, 900 and 1800 pulses per second (pps), with either rectangular or Hanning window envelopes. Our rats exhibited very high sensitivity to ITDs at pulse rates up to 900 pps for both envelope shapes, a pulse rate commonly used in clinical practice. However, ITD sensitivity declined to near zero at 1800 pps, for both Hanning and rectangular windowed pulse trains. Current clinical cochlear implant (CI) processors are often set to pulse rates ≥900 pps, but ITD sensitivity in human CI listeners is often reported to decline sharply above ~300 pps. Our results suggest that the relatively poor ITD sensitivity seen at >300 pps in human CI users may not reflect the hard upper limit of biCI ITD performance in the mammalian auditory pathway. Perhaps with training or better CI strategies good binaural hearing may be achievable at pulse rates high enough to allow good sampling of speech envelopes while delivering usable ITDs.

Interaural level difference sensitivity in neonatally deafened rats fitted with bilateral cochlear implants

“…In this study, we set out to measure and describe the behavioral sensitivity of ND rats to ILDs in pulsatile electric stimuli delivered binaurally via neuroprosthetic intracochlear electrodes. As explained in the introduction, rats have turned out to be a very useful model species for investigating ITD sensitivity under biCI stimulation, as they exhibit remarkably low behavioral [23][24][25] and physiological [20; 24] ITD thresholds even after neonatal deafening and over a wide range of pulse rates. The use of this animal model allows us to circumvent the many confounds that patient needs and clinical practice issues introduce into studies on human volunteers, making it easier to investigate factors that determine binaural hearing outcomes following bilateral cochlear implantation.…”

“…A total of 24 female Wistar rats were used in this study. All rats underwent neonatal deafening, acoustic and electric auditory brainstem response (aABR/eABR) recordings, bilateral cochlear implantation and [ [23][24][25] and briefly below.…”

“…After implantation, the rats were trained in a 2AFC stimulus lateralization task in a custom-made behavioral setup [23][24][25]. The setup is illustrated schematically in Figure 1A.…”

“…Rats already turned out to be a promising choice given that they are easy to train in behavioral binaural cue lateralization tasks [6] and highly suitable for electrophysiological investigations of binaural cue sensitivity [17][18][19][20][21][22]. In addition, the extremely encouraging results from Buck et al [23] and Rosskohten-Kuhl et al [24] showed, that neonatally deafened (ND), young adult cochlear implanted rats were able to learn with only minimal training to lateralize CI pulse timing ITDs as small as ~50 μs for pulse rates up to 900 pps, exhibiting an ITD discrimination performance that is comparable to normally hearing peers and substantially better than that observed in comparable human patient cohorts [6]. These results are exciting because they open up avenues for further research into improved CI stimulation strategies or treatment regimes that should lead to substantially better outcomes for biCI patients.…”

Does age protect against loss of tonotopy after acute deafness in adulthood?

“…ABRs were recorded by averaging scalp potentials measured with subcutaneous needle electrodes between mastoids and the vertex of the rat's head over 300 click presentations. While normal hearing rats typically exhibited click ABR thresholds near 0 dB SL, deafened rats showed increased hearing thresholds ≥95 dB SL to broadband click stimuli as well as pure tones (Rosskothen-Kuhl et al, 2021;Buck et al, 2023). Figures 1 A and B show ABRs of an adult-deafened rat before and after deafening by EA and KM injection.…”