Implanted Vestibular Prosthesis Improves Spatial Orientation in Animals with Severe Vestibular Damage
Key findings
- This study tested in monkeys a vestibular implant that senses angular head velocity in three dimensions and provides motion-modulated electrical stimulation of afferent nerves in the semicircular canals
- In a healthy normal state, the monkeys accurately sensed the orientation of the head relative to gravity during dynamic tilts
- This ability was degraded after severe bilateral vestibular damage and substantially improved when the vestibular implant was activated
- These results suggest a canal vestibular implant could reduce the disabling perceptual and postural deficits experienced by patients with bilateral vestibular hypofunction
Vestibular damage results in the misperception of one's position in space, poor balance and blurred vision during head movements. The latter occurs because of the vestibulo-ocular reflex (VOR)—the transfer of vestibular information to the brain generates eye movements that stabilize images on the retina during head motion.
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Damage to the vestibular organs is typically permanent, and physical therapy provides only modest improvement. Therefore, research is focusing on a vestibular implant (VI) for the semicircular canals, the part of the vestibular system that collects information about angular head motion.
Previous work established that a VI can generate normal VOR responses in animals and humans with vestibular damage. Building on those findings, Mass Eye and Ear researchers demonstrated in monkeys that a canal VI can improve the brain's representation of head position after the vestibular system is damaged.
Faisal Karmali, PhD, and Richard F. Lewis, MD, co-directors of the Jenks Vestibular Physiology Laboratory at Mass Eye and Ear, and colleagues report the findings in The Journal of Neuroscience.
Methods
Two rhesus monkeys underwent surgery for implantation of eye coils and ear electrodes (one in each of the three canals of one ear).
Training—The monkeys were trained to perform a subjective visual vertical (SVV) task that could be used to test their perception of head orientation relative to gravity. Each animal sat in a primate chair with its head immobilized and looked at a light bar displayed on a monitor. By rotating a steering wheel the monkey rotated the light bar about the earth-horizontal axis.
The animal at first learned to align the light bar parallel to a reference line on the monitor aligned with gravity. Later, for testing purposes, they learned to align the bar in the dark without any visual orientation cues while being roll-tilted around the earth-horizontal axis.
Testing—SVV testing and eye movement recordings were performed in four vestibular states:
- Normal
- After induction of severe bilateral vestibular damage (labyrinthectomy in one ear; exposure of the electrodes in the other ear to aminoglycosides)
- After activation of the VI, which provided chronic stimulation for months as the monkeys moved freely around their housing; testing was performed intermittently when head motion–modulated stimulation of the canal afferent nerves was off or on
Eye Movement
As expected from previous research, motion-modulated VI stimulation provided adequate information about roll rotation to generate a compensatory VOR.
Perceptual Responses
SVV test results showed that in the normal state, the monkeys accurately sensed the orientation of the head relative to gravity during dynamic tilts. This ability was degraded after the bilateral vestibular damage.
Activation of the canal VI improved the animals' ability to estimate angular head position, as evidenced by improved perception of spatial orientation. In addition, the VI reproduced a substantial fraction of the normal vestibular contribution to tilt perception, and the perceptual effects paralleled the amount of vestibular information supplied by the prosthesis relative to the normal labyrinth.
The Path Forward
It seems likely a canal VI will someday be able to reduce the disabling effects of bilateral vestibular hypofunction in humans. The Mass Eye and Ear team is planning technical enhancements and the study of bilateral instead of unilateral stimulation.
To expedite the development of the VI, animal and human research is being performed in parallel since these approaches yield complementary information about the device's behavioral effects, efficacy and safety.
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