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

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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 single-unit 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 early-deafened 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.

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Acknowledgements

This work was supported by the National Institutes of Health Grants R01 DC005775 and P30 DC005209. We thank Ken Hancock, Camille Shaw, Alice Gelman, Stephanie Ventura, and Marie Ortega for technical assistance. We thank M. Charles Liberman, Leslie Liberman, and Melissa McKinnon for valuable advice and assistance on processing of temporal bones and Pooja Balaram for advice on processing of brain tissue.

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Authors and Affiliations

  1. Eaton-Peabody Laboratories, Massachusetts Eye & Ear, Boston, MA, 02114, USA

    Yoojin Chung, Brian D. Buechel, Woongsang Sunwoo, Joseph D. Wagner & Bertrand Delgutte

  2. Department of Otolaryngology, Harvard Medical School, Boston, MA, 02115, USA

    Yoojin Chung, Woongsang Sunwoo & Bertrand Delgutte

  3. Program in Speech and Hearing Bioscience and Technology, Harvard Medical School, Boston, MA, 02115, USA

    Brian D. Buechel

  4. Department of Otolaryngology, Gachon University Gil Medical Center, Incheon, 405-760, South Korea

    Woongsang Sunwoo

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  1. Yoojin Chung
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Correspondence to Yoojin Chung.

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Y. Chung, B.D. Buechel, W. Sunwoo, J.D. Wagner, and B. Delgutte have no conflict of interest to declare.

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Chung, Y., Buechel, B.D., Sunwoo, W. et al. Neural ITD Sensitivity and Temporal Coding with Cochlear Implants in an Animal Model of Early-Onset Deafness. JARO 20, 37–56 (2019). https://doi.org/10.1007/s10162-018-00708-w

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