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Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis

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Abstract

By sensing three-dimensional (3D) head rotation and electrically stimulating the three ampullary branches of a vestibular nerve to encode head angular velocity, a multichannel vestibular prosthesis (MVP) can restore vestibular sensation to individuals disabled by loss of vestibular hair cell function. However, current spread to afferent fibers innervating non-targeted canals and otolith end organs can distort the vestibular nerve activation pattern, causing misalignment between the perceived and actual axis of head rotation. We hypothesized that over time, central neural mechanisms can adapt to correct this misalignment. To test this, we rendered five chinchillas vestibular deficient via bilateral gentamicin treatment and unilaterally implanted them with a head-mounted MVP. Comparison of 3D angular vestibulo-ocular reflex (aVOR) responses during 2 Hz, 50°/s peak horizontal sinusoidal head rotations in darkness on the first, third, and seventh days of continual MVP use revealed that eye responses about the intended axis remained stable (at about 70% of the normal gain) while misalignment improved significantly by the end of 1 week of prosthetic stimulation. A comparable time course of improvement was also observed for head rotations about the other two semicircular canal axes and at every stimulus frequency examined (0.2–5 Hz). In addition, the extent of disconjugacy between the two eyes progressively improved during the same time window. These results indicate that the central nervous system rapidly adapts to multichannel prosthetic vestibular stimulation to markedly improve 3D aVOR alignment within the first week after activation. Similar adaptive improvements are likely to occur in other species, including humans.

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Acknowledgments

We thank Lani Swarthout for assistance with animal care. This work was funded by NIH NIDCD grants R01DC009255, K08DC6216, R01DC2390, and 5F32DC009917. 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. Departments of Otolaryngology—Head & Neck Surgery and Biomedical Engineering, Vestibular NeuroEngineering Laboratory, Johns Hopkins University School of Medicine, Ross Bldg Rm 830, 720 Rutland Ave., Baltimore, MD, 21205, USA

    Chenkai Dai, Gene Y. Fridman, Bryce Chiang, Natan S. Davidovics, Thuy-Anh Melvin & Charles C. Della Santina

  2. Department of Physiology, McGill University, Montreal, QC, Canada

    Kathleen E. Cullen

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  1. Chenkai Dai
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  2. Gene Y. Fridman
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  4. Natan S. Davidovics
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  5. Thuy-Anh Melvin
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  6. Kathleen E. Cullen
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  7. Charles C. Della Santina
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Correspondence to Charles C. Della Santina.

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Dai, C., Fridman, G.Y., Chiang, B. et al. Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res 210, 595–606 (2011). https://doi.org/10.1007/s00221-011-2591-5

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