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

  1. Nicole Rosskothen-Kuhl  Is a corresponding author
  2. Alexa N Buck
  3. Kongyan Li
  4. Jan W H Schnupp  Is a corresponding author
  1. University Medical Center Freiburg, Germany
  2. City University of Hong Kong, Hong Kong

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 μs. 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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Data have been deposited to Dryad, under the DOI 10.5061/dryad.573n5tb6d.

The following data sets were generated

Article and author information

Author details

  1. Nicole Rosskothen-Kuhl

    Department of Otorhinolaryngology, University Medical Center Freiburg, Freiburg, Germany
    For correspondence
    nicole.rosskothen-kuhl@uniklinik-freiburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4724-5550
  2. Alexa N Buck

    Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, Hong Kong
    Competing interests
    The authors declare that no competing interests exist.
  3. Kongyan Li

    Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, Hong Kong
    Competing interests
    The authors declare that no competing interests exist.
  4. Jan W H Schnupp

    Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, Hong Kong
    For correspondence
    jan.schnupp@googlemail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutscher Akademischer Austauschdienst (P.R.I.M.E. - Postdoctoral Researchers International Mobility Experience,REA grant agreement n 605728)

  • Nicole Rosskothen-Kuhl

Hong Kong General Research Fund (Hong Kong General Research Fund (11100219))

  • Jan W H Schnupp

Deutsche Forschungsgemeinschaft (Cluster of Excellence BrainLinks-BrainTools,Grant number EXC1086)

  • Nicole Rosskothen-Kuhl

Taube Kinder lernen hoeren e.V.

  • Nicole Rosskothen-Kuhl

Hong Kong (Medical Research Fund (06172296))

  • Jan W H Schnupp

Shenzhen Science and Innovation Fund (Shenzhen Science and Innovation Fund (JCYJ20180307124024360))

  • Jan W H Schnupp

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures involving experimental animals reported here were approved by the Department of Health of Hong Kong (#16-52 DH/HA&P/8/2/5) or Regierungspräsidium Freiburg (#35-9185.81/G-17/124), as well as by the appropriate local ethical review committee. All surgery was performed under ketamine and xylazine anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Lina Reiss, Oregon Health and Science University, United States

Publication history

  1. Received: June 16, 2020
  2. Accepted: January 7, 2021
  3. Accepted Manuscript published: January 11, 2021 (version 1)
  4. Version of Record published: January 18, 2021 (version 2)

Copyright

© 2021, Rosskothen-Kuhl et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nicole Rosskothen-Kuhl
  2. Alexa N Buck
  3. Kongyan Li
  4. Jan W H Schnupp
(2021)
Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness
eLife 10:e59300.
https://doi.org/10.7554/eLife.59300
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