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Sensitivity to Pulse Rate and Amplitude Modulation in an Animal Model of the Auditory Brainstem Implant (ABI)

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Abstract

The auditory brainstem implant (ABI) is an auditory neuroprosthesis that provides hearing by electrically stimulating the cochlear nucleus (CN) of the brainstem. Our previous study (McInturff et al., 2022) showed that single-pulse stimulation of the dorsal (D)CN subdivision with low levels of current evokes responses that have early latencies, different than the late response patterns observed from stimulation of the ventral (V)CN. How these differing responses encode more complex stimuli, such as pulse trains and amplitude modulated (AM) pulses, has not been explored. Here, we compare responses to pulse train stimulation of the DCN and VCN, and show that VCN responses, measured in the inferior colliculus (IC), have less adaption, higher synchrony, and higher cross-correlation. However, with high-level DCN stimulation, responses become like those to VCN stimulation, supporting our earlier hypothesis that current spreads from electrodes on the DCN to excite neurons located in the VCN. To AM pulses, stimulation of the VCN elicits responses with larger vector strengths and gain values especially in the high-CF portion of the IC. Additional analysis using neural measures of modulation thresholds indicate that these measures are lowest for VCN. Human ABI users with low modulation thresholds, who score best on comprehension tests, may thus have electrode arrays that stimulate the VCN. Overall, the results show that the VCN has superior response characteristics and suggest that it should be the preferred target for ABI electrode arrays in humans.

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Availability of Data and Materials

All data and materials used in this study will be available upon request to Stephen McInturff.

Code Availability

The MATLAB code used for data analysis will be available upon request to Stephen McInturff.

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Acknowledgements

We thank Dr. Ken Hancock and Evan Foss for their technical assistance, and Dr. Mahan Azadpour for his helpful comments on the research.

Funding

(1) Sinergia Grant from the Swiss National Science Foundation (530733); (2) Bertarelli Foundation program for Translational Neuroscience and Neuro-Engineering; (3) NIDCD/NIH grant (01089).

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Authors and Affiliations

  1. Eaton-Peabody Laboratories, Department of Otolaryngology—Head and Neck Surgery, Massachusetts Eye and Ear, Boston, MA, 02114, USA

    Stephen McInturff, Victor Adenis, Daniel J. Lee & M. Christian Brown

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

    Stephen McInturff, Daniel J. Lee & M. Christian Brown

  3. Department of Otolaryngology—Head and Neck Surgery, Harvard Medical School, Boston, MA, USA

    Victor Adenis, Daniel J. Lee & M. Christian Brown

  4. Laboratory for Soft Bioelectronic Interfaces, Institute of Microengineering, Institute of Bioengineering, Centre for Neuroprosthetics, École Polytechnique Fédérale de Lausanne (EPFL), 1202, Geneva, Switzerland

    Florent-Valéry Coen & Stéphanie P. Lacour

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Contributions

SM performed all experiments. SM processed all data with significant help from VA. SM and MCB equally wrote manuscript with help from VA. SM and MCB contributed equally to experimental designs and protocols. FVC and SPL developed and provided electrical implants used in this study.

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Correspondence to Stephen McInturff.

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All animal procedures were approved by the animal care and use protocols at the Massachusetts Eye & Ear Infirmary, Boston, MA (protocol number 2021N000064).

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McInturff, S., Adenis, V., Coen, FV. et al. Sensitivity to Pulse Rate and Amplitude Modulation in an Animal Model of the Auditory Brainstem Implant (ABI). JARO 24, 365–384 (2023). https://doi.org/10.1007/s10162-023-00897-z

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