Binocular 3D otolith-ocular reflexes: responses of chinchillas to prosthetic electrical stimulation targeting the utricle and saccule

Abstract

From animal experiments by Cohen and Suzuki et al. in the 1960s to the first-in-human clinical trials now in progress, prosthetic electrical stimulation targeting semicircular canal branches of the vestibular nerve has proven effective at driving directionally appropriate vestibulo-ocular reflex eye movements, postural responses, and perception. That work was considerably facilitated by the fact that all hair cells and primary afferent neurons in each canal have the same directional sensitivity to head rotation, the three canals’ ampullary nerves are geometrically distinct from one another, and electrically evoked three-dimensional (3D) canal-ocular reflex responses approximate a simple vector sum of linearly independent components representing relative excitation of each of the three canals. In contrast, selective prosthetic stimulation of the utricle and saccule has been difficult to achieve, because hair cells and afferents with many different directional sensitivities are densely packed in those endorgans and the relationship between 3D otolith-ocular reflex responses and the natural and/or prosthetic stimuli that elicit them is more complex. As a result, controversy exists regarding whether selective, controllable stimulation of electrically evoked otolith-ocular reflexes (eeOOR) is possible. Using micromachined, planar arrays of electrodes implanted in the labyrinth, we quantified 3D, binocular eeOOR responses to prosthetic electrical stimulation targeting the utricle, saccule, and semicircular canals of alert chinchillas. Stimuli delivered via near-bipolar electrode pairs near the maculae elicited sustained ocular countertilt responses that grew reliably with pulse rate and pulse amplitude, varied in direction according to which stimulating electrode was employed, and exhibited temporal dynamics consistent with responses expected for isolated macular stimulation. NEW & NOTEWORTHY As the second in a pair of papers on Binocular 3D Otolith-Ocular Reflexes, this paper describes new planar electrode arrays and vestibular prosthesis architecture designed to target the three semicircular canals and the utricle and saccule. With this technological advancement, electrically evoked otolith-ocular reflexes due to stimulation via utricle- and saccule-targeted electrodes were recorded in chinchillas. Results demonstrate advances toward achieving selective stimulation of the utricle and saccule.

The Anatomical and Physiological Basis of Clinical Tests of Otolith Function. A Tribute to Yoshio Uchino

“…The otoconia, attached to the upper surface of the otoconial membrane, tend to stay in place and so drag the hair bundles of utricular receptors opposite to the lateral translation (Figure 10). In this way lateral translation should cause OCR opposite to the translation direction, and that result has been reported in humans [72] and chinchillas [73]. There were also small horizontal eye movements -lateral translation to the left causes both eyes to move horizontally to the right [74,75], depending on many factors such as fixation direction and distance [76].…”

The Anatomical and Physiological Basis of Clinical Tests of Otolith Function. A Tribute to Yoshio Uchino

“…The otoconia, attached to the upper surface of the otoconial membrane, tend to stay in place and so drag the hair bundles of utricular receptors opposite to the lateral translation (Figure 10A). In this way lateral translation should cause OCR opposite to the translation direction, and that result has been reported in humans (73) and chinchillas (74). There were also small horizontal eye movements-lateral translation to the left causes both eyes to move horizontally to the right (75,76), depending on many factors such as fixation direction and distance (77).…”

Binocular 3D otolith-ocular reflexes: responses of normal chinchillas to tilt and translation

“…Understanding and emulating that process will be a necessary precursor to development of vestibular prostheses that encode tilt and translational stimuli via artificial stimulation of the utricle and saccule, analogous to canal-stimulating prostheses that have shown promise for restoration of the 3D aVOR in the setting of bilateral vestibular hypofunction [reviewed in the companion paper by Hageman et al (2020) and Boutros et al (2019)].…”