An Implanted Vestibular Prosthesis Improves Spatial Orientation in Animals with Severe Vestibular Damage

Abstract

Gravity is a pervasive environmental stimulus, and accurate graviception is required for optimal spatial orientation and postural stability. The primary graviceptors are the vestibular organs, which include angular velocity (semicircular canals) and linear acceleration (otolith organs) sensors. Graviception is degraded in patients with vestibular damage, resulting in spatial misperception and imbalance. Since minimal therapy is available for these patients, substantial effort has focused on developing a vestibular prosthesis or vestibular implant (VI) that reproduces information normally provided by the canals (since reproducing otolith function is very challenging technically). Prior studies demonstrated that angular eye velocity responses could be driven by canal VI-mediated angular head velocity information, but it remains unknown whether a canal VI could improve spatial perception and posture since these behaviors require accurate estimates of angular head position in space relative to gravity. Here, we tested the hypothesis that a canal VI that transduces angular head velocity and provides this information to the brain via motion-modulated electrical stimulation of canal afferent nerves could improve the perception of angular head position relative to gravity in monkeys with severe vestibular damage. Using a subjective visual vertical task, we found that normal female monkeys accurately sensed the orientation of the head relative to gravity during dynamic tilts, that this ability was degraded following bilateral vestibular damage, and improved when the canal VI was used. These results demonstrate that a canal VI can improve graviception in vestibulopathic animals, suggesting that it could reduce the disabling perceptual and postural deficits experienced by patients with severe vestibular damage.

A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys

“…As expected, our static mapping generated VOR responses consistent with the results of these prior studies, which were characterized by poor phase compensation. Finally, it is noteworthy that prior work by Merfeld and colleagues employed a dynamic mapping between angular head velocity to a specific pulse rate [ 33 , 37 – 39 ]. However, this mapping only approximated afferent dynamics over a very low frequency range (<0.1 Hz) and thus performed in a comparable manner to the static mapping over most of the natural frequency range (i.e., 0.1 Hz to 20 Hz).…”

Vestibular prosthesis: from basic research to clinics

“…This situation seems to induce a neurosensory conflict that causes plastic changes leading to a reduction of the gain of the afferent input from the SCC with critical functional consequences ( Kornilova and Kozlovskaya, 2003 ; Kornilova et al, 2017 ). Although, in monkeys with VI in the three SCC the brain may extract information about head position ( Karmali et al, 2021 ). Also in humans wearing the Geneva-Maastricht VI, acoustically elicited cervical vestibular evoked myogenic potentials (cVEMPs) can be elicited, suggesting that VI in SCC can improve postural control ( Perez-Fornos et al, 2019 ).…”

“…Results also showed that head movements elicited by horizontal SCC stimulation significantly contributed to gaze stabilization, complementing the VOR ( Mitchell et al, 2013 ). It has also been shown in two rhesus monkeys that head orientation perception improves using a VI that stimulated the three SCC can improve graviception, indicating that the brain may extract information about the head’s orientation from the SCC activity ( Karmali et al, 2021 ).…”

Vestibular contribution to path integration deficits in ‘at-genetic-risk’ for Alzheimer’s disease

“…Vestibular dysfunction and its precipitating factors (such as hearing loss; see recent Review Smith, 2021, vestibular migrane and vertigo) are at least partially modifiable [ 14 , 17 , 18 ]. Thus, identifying and treating early vestibular dysfunction may serve a preventative role in AD.…”