Prosthetic Stimulation of the Vestibular Nerve Can Evoke Robust Eye and Head Movements Despite Prior Labyrinthectomy

Author:

Wiboonsaksakul Kantapon Pum,Della Santina Charles C.1,Cullen Kathleen E.

Affiliation:

1. Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine; Baltimore, MD

Abstract

Hypothesis Prosthetic electrical stimulation can evoke compensatory eye and head movement despite vestibular implant electrode insertion occurring years after prior labyrinthectomy. Background Vestibular implants sense head rotation and directly stimulate the vestibular nerve, bypassing damaged end organs. Animal research and current clinical trials have demonstrated the efficacy of this approach. However, candidacy criteria for vestibular implants currently require presence of a patent labyrinth in the candidate ear and at least aidable hearing in the opposite ear, thus excluding patients who have undergone prior labyrinthectomy for unilateral Menière's disease that later progressed to bilateral vestibular hypofunction. Methods Eight years after right unilateral labyrinthectomy, we implanted stimulating electrodes in the previously exenterated right ear ampullae of a rhesus macaque monkey. The left labyrinth had long-standing hypofunction due to intratympanic gentamicin injection and surgical disruption. We used three-dimensional video-oculography to measure eye movement responses to prosthetic electrical stimulation. We also measured head-movement responses to prosthetic stimulation with the head unrestrained. Results Bilateral vestibular hypofunction was confirmed by absence of vestibuloocular reflex responses to whole-body rotation without prosthetic stimulation. For a subset of the implanted electrodes, prosthetic vestibular stimulation evoked robust compensatory eye and head movements. One electrode reliably elicited responses aligned with the implanted ear's anterior canal nerve regardless of the return electrode used. Similarly, a second electrode also elicited responses consistent with excitation of the horizontal canal nerve. Responses grew quasilinearly with stimulation rate and current amplitude. Conclusion Prosthetic electrical stimulation targeting the vestibular nerve can be effective years after labyrinthectomy, if at least some parts of the vestibular nerve's ampullary branches remain despite destruction or removal of the membranous labyrinth.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Neurology (clinical),Sensory Systems,Otorhinolaryngology

Reference18 articles.

1. Restoration of 3D vestibular sensation in rhesus monkeys using a multichannel vestibular prosthesis;Hear Res,2011

2. An Implanted Vestibular Prosthesis Improves Spatial Orientation in Animals with Severe Vestibular Damage;J Neurosci,2021

3. Nonhuman primate vestibuloocular reflex responses to prosthetic vestibular stimulation are robust to pulse timing errors caused by temporal discretization;J Neurophysiol,2019

4. Continuous vestibular implant stimulation partially restores eye-stabilizing reflexes;JCI Insight,2019

5. Posture, gait, quality of life, and hearing with a vestibular implant;N Engl J Med,2021

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