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Virtual labyrinth model of vestibular afferent excitation via implanted electrodes: validation and application to design of a multichannel vestibular prosthesis

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An Erratum to this article was published on 03 April 2011

Abstract

To facilitate design of a multichannel vestibular prosthesis that can restore sensation to individuals with bilateral loss of vestibular hair cell function, we created a virtual labyrinth model. Model geometry was generated through 3-dimensional (3D) reconstruction of microMRI and microCT scans of normal chinchillas (Chinchilla lanigera) acquired with 30–48 μm and 12 μm voxels, respectively. Virtual electrodes were positioned based on anatomic landmarks, and the extracellular potential field during a current pulse was computed using finite element methods. Potential fields then served as inputs to stochastic, nonlinear dynamic models for each of 2,415 vestibular afferent axons with spiking dynamics based on a modified Smith and Goldberg model incorporating parameters that varied with fiber location in the neuroepithelium. Action potential propagation was implemented by a well validated model of myelinated fibers. We tested the model by comparing predicted and actual 3D angular vestibulo-ocular reflex (aVOR) axes of eye rotation elicited by prosthetic stimuli. Actual responses were measured using 3D video-oculography. The model was individualized for each animal by placing virtual electrodes based on microCT localization of real electrodes. 3D eye rotation axes were predicted from the relative proportion of model axons excited within each of the three ampullary nerves. Multiple features observed empirically were observed as emergent properties of the model, including effects of active and return electrode position, stimulus amplitude and pulse waveform shape on target fiber recruitment and stimulation selectivity. The modeling procedure is partially automated and can be readily adapted to other species, including humans.

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Acknowledgments

Supported by the United States National Institute on Deafness and Other Communication Disorders K08DC6216 (PI: CCDS), R01DC9255 (PI: CCDS) and R01DC2390 (Current PI: CCDS; Prior PI: Lloyd B. Minor) and by a Medtronic Student Fellowship (PI: RH). CDS, GYF and BC are inventors on pending and awarded patents relevant to prosthesis technology, and CDS holds an equity interest in Labyrinth Devices LLC.

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Authors and Affiliations

  1. Johns Hopkins Vestibular NeuroEngineering Laboratory, 601 N. Caroline Street, Rm 6253, Baltimore, MD, 21287-0910, USA

    Russell Hayden, Stacia Sawyer, Eric Frey, Susumu Mori, Americo A. Migliaccio & Charles C. Della Santina

  2. Departments of Otolaryngology—Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Russell Hayden, Americo A. Migliaccio & Charles C. Della Santina

  3. Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Russell Hayden, Americo A. Migliaccio & Charles C. Della Santina

  4. Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Stacia Sawyer, Eric Frey & Susumu Mori

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  1. Russell Hayden
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  2. Stacia Sawyer
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  3. Eric Frey
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  5. Americo A. Migliaccio
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  6. Charles C. Della Santina
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Correspondence to Charles C. Della Santina.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00221-011-2640-0

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Hayden, R., Sawyer, S., Frey, E. et al. Virtual labyrinth model of vestibular afferent excitation via implanted electrodes: validation and application to design of a multichannel vestibular prosthesis. Exp Brain Res 210, 623–640 (2011). https://doi.org/10.1007/s00221-011-2599-x

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