Individuals with bilateral vestibular hypofunction suffer reduced quality of life due to loss of postural and ocular reflexes essential to maintaining balance and visual acuity during head movements. Vestibular stimulation has demonstrated success in restoring sensation of angular head rotations using electrical stimulation of the semi-circular canals (SCCs). Efforts toward utricle and saccule stimulation to restore sensation of gravitoinertial acceleration have been limited due to the complexity of the otolith end organs and otolith-ocular reflexes (OORs). Four key pieces of technology were developed to extend prosthetic stimulation to the utricle and saccule: a low-noise scleral coil system to record binocular 3D eye movements; a motion platform control system for automated presentation of rotational and translational stimuli; custom electrode arrays with fifty contacts targeting the SCCs, utricle and saccule; and a general-purpose neuroelectronic stimulator for vestibular and other neuromodulation applications. Using these new technologies, OORs were first characterized in six chinchillas to establish OOR norms during translations and static tilts. Results led to creation of a model that infers the axis of head tilt from measured binocular eye movements and thereby provides a context and means to assess the selectivity of prosthetic utricle and saccule stimulation. The model confirms the expectation that excitation of the left utricle and saccule primarily encodes tilts that bring the left ear down. Three of the chinchillas were implanted with electrode arrays in the left ear. Step changes in pulse rate were delivered to utricle and saccule electrodes near the maculae while measuring 3D binocular eye movements with the animal stationary in darkness. These stimuli elicited sustained ocular counter-roll responses that increased in magnitude as pulse rate or amplitude increased. Bipolar stimulation via neighboring electrodes elicited slow-rising or delayed onset of ocular counter-rolls (consistent with normal translational OOR low-pass filter behavior). Two chinchillas showed different direction of electrically-evoked ocular counter-roll between utricle versus sacculestimulation. Only near-neighbor bipolar electrode combinations elicited eye responses compensatory for tilts other than the ;;usual’ left ear down, suggesting the need for distributing multiple bipolar electrode pairs across the maculae to achieve selective stimulation and restore 3D sensation of gravitoinertial acceleration.
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Restoring Sensation of Gravitoinertial Acceleration through Prosthetic Stimulation of the Utricle and Saccule