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Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness.

ABSTRACT: Spatial hearing in cochlear implant (CI) patients remains a major challenge, with many early deaf users reported to have no measurable sensitivity to interaural time differences (ITDs). Deprivation of binaural experience during an early critical period is often hypothesized to be the cause of this shortcoming. However, we show that neonatally deafened (ND) rats provided with precisely synchronized CI stimulation in adulthood can be trained to lateralize ITDs with essentially normal behavioral thresholds near 50 ?s. Furthermore, comparable ND rats show high physiological sensitivity to ITDs immediately after binaural implantation in adulthood. Our result that ND-CI rats achieved very good behavioral ITD thresholds, while prelingually deaf human CI patients often fail to develop a useful sensitivity to ITD raises urgent questions concerning the possibility that shortcomings in technology or treatment, rather than missing input during early development, may be behind the usually poor binaural outcomes for current CI patients.

SUBMITTER: Rosskothen-Kuhl N

PROVIDER: S-EPMC7815311 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness.

Rosskothen-Kuhl Nicole N Buck Alexa N AN Li Kongyan K Schnupp Jan Wh JW

eLife 20210111

Spatial hearing in cochlear implant (CI) patients remains a major challenge, with many early deaf users reported to have no measurable sensitivity to interaural time differences (ITDs). Deprivation of binaural experience during an early critical period is often hypothesized to be the cause of this shortcoming. However, we show that neonatally deafened (ND) rats provided with precisely synchronized CI stimulation in adulthood can be trained to lateralize ITDs with essentially normal behavioral th ...[more]

PMID: 33427644

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Project description:While cochlear implantation has benefitted many patients with single-sided deafness (SSD), there is great variability in cochlear implant (CI) outcomes and binaural performance remains poorer than that of normal-hearing (NH) listeners. Differences in sound quality across ears-temporal fine structure (TFS) information with acoustic hearing vs. coarse spectro-temporal envelope information with electric hearing-may limit integration of acoustic and electric patterns. Binaural performance may also be limited by inter-aural mismatch between the acoustic input frequency and the place of stimulation in the cochlea. SSD CI patients must learn to accommodate these differences between acoustic and electric stimulation to maximize binaural performance. It is possible that training may increase and/or accelerate accommodation and further improve binaural performance. In this study, we evaluated lateralization training in NH subjects listening to broad simulations of SSD CI signal processing. A 16-channel vocoder was used to simulate the coarse spectro-temporal cues available with electric hearing; the degree of inter-aural mismatch was varied by adjusting the simulated insertion depth (SID) to be 25 mm (SID25), 22 mm (SID22) and 19 mm (SID19) from the base of the cochlea. Lateralization was measured using headphones and head-related transfer functions (HRTFs). Baseline lateralization was measured for unprocessed speech (UN) delivered to the left ear to simulate SSD and for binaural performance with the acoustic ear combined with the 16-channel vocoders (UN+SID25, UN+SID22 and UN+SID19). After completing baseline measurements, subjects completed six lateralization training exercises with the UN+SID22 condition, after which performance was re-measured for all baseline conditions. Post-training performance was significantly better than baseline for all conditions (p < 0.05 in all cases), with no significant difference in training benefits among conditions. Given that there was no significant difference between the SSD and the SSD CI conditions before or after training, the results suggest that NH listeners were unable to integrate TFS and coarse spectro-temporal cues across ears for lateralization, and that inter-aural mismatch played a secondary role at best. While lateralization training may benefit SSD CI patients, the training may largely improve spectral analysis with the acoustic ear alone, rather than improve integration of acoustic and electric hearing.

Project description:BackgroundA major cue for the position of a high-frequency sound source in azimuth is the difference in sound pressure levels in the two ears, Interaural Level Differences (ILDs), as a sound is presented from different positions around the head. This study aims to use data classification techniques to build a descriptive model of electro-physiologically determined neuronal sensitivity functions for ILDs. The ILDs were recorded from neurons in the central nucleus of the Inferior Colliculus (ICc), an obligatory midbrain auditory relay nucleus. The majority of ICc neurons (~ 85%) show sensitivity to ILDs but with a variety of different forms that are often difficult to unambiguously separate into different information-bearing types. Thus, this division is often based on laboratory-specific and relatively subjective criteria. Given the subjectivity and non-uniformity of ILD classification methods in use, we examined if objective data classification techniques for this purpose. Our key objectives were to determine if we could find an analytical method (A) to validate the presence of four typical ILD sensitivity functions as is commonly assumed in the field, and (B) whether this method produced classifications that mapped on to the physiologically observed results.MethodsThe three-step data classification procedure forms the basic methodology of this manuscript. In this three-step procedure, several data normalization techniques were first tested to select a suitable normalization technique to our data. This was then followed by PCA to reduce data dimensionality without losing the core characteristics of the data. Finally Cluster Analysis technique was applied to determine the number of clustered data with the aid of the CCC and Inconsistency Coefficient values.ResultsThe outcome of a three-step analytical data classification process was the identification of seven distinctive forms of ILD functions. These seven ILD function classes were found to map to the four "known" ideal ILD sensitivity function types, namely: Sigmoidal-EI, Sigmoidal-IE, Peaked, and Insensitive, ILD functions, and variations within these classes. This indicates that these seven templates can be utilized in future modelling studies.ConclusionsWe developed a taxonomy of ILD sensitivity functions using a methodological data classification approach. The number and types of generic ILD function patterns found with this method mapped well on to our electrophysiologically determined ILD sensitivity functions. While a larger data set of the latter functions may bring a more robust outcome, this good mapping is encouraging in providing a principled method for classifying such data sets, and could be well extended to other such neuronal sensitivity functions, such as contrast tuning in vision.

Dataset Information

Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness.

Publications

Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness.

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