Current and future management of bilateral loss of vestibular sensation - an update on the Johns Hopkins Multichannel Vestibular Prosthesis Project

Abstract

Bilateral loss of vestibular sensation can disable individuals whose vestibular hair cells are injured by ototoxic medications, infection, Ménière's disease or other insults to the labyrinth including surgical trauma during cochlear implantation. Without input to vestibulo-ocular and vestibulo-spinal reflexes that normally stabilize the eyes and body, affected patients suffer blurred vision during head movement, postural instability, and chronic disequilibrium. While individuals with some residual sensation often compensate for their loss through rehabilitation exercises, those who fail to do so are left with no adequate treatment options. An implantable neuroelectronic vestibular prosthesis that emulates the normal labyrinth by sensing head movement and modulating activity on appropriate branches of the vestibular nerve could significantly improve quality of life for these otherwise chronically dizzy patients. This brief review describes the impact and current management of bilateral loss of vestibular sensation, animal studies supporting the feasibility of prosthetic vestibular stimulation, and a vestibular prosthesis designed to restore sensation of head rotation in all directions. Similar to a cochlear implant in concept and size, the Johns Hopkins Multichannel Vestibular Prosthesis (MVP) includes miniature gyroscopes to sense head rotation, a microcontroller to process inputs and control stimulus timing, and current sources switched between pairs of electrodes implanted within the vestibular labyrinth. In rodents and rhesus monkeys rendered bilaterally vestibulardeficient via treatment with gentamicin and/or plugging of semicircular canals, the MVP partially restores the vestibulo-ocular reflex for head rotations about any axis of rotation in 3-dimensional space. Our efforts now focus on addressing issues prerequisite to human implantation, including refinement of electrode designs and surgical technique to enhance stimulus selectivity and preserve cochlear function, optimization of stimulus protocols, and reduction of device size and power consumption.

Figure 1

In chinchillas treated with gentamicin to ablate vestibular sensation bilaterally, pulse-frequency-modulated prosthetic stimulation partially restored a 3D vestibulo-ocular reflex with gain similar to that of normal animals. (Column 1) Mean head rotation and eye rotations of a normal chinchilla during 2 Hz 50°/s head rotations about mean horizontal (top), left-anterior/right-posterior (LARP, middle), and right-anterior/left-posterior (RALP, bottom) semicircular canal (SCC) axes in darkness. Each component of the 3D response is shown. This animal’s gains were higher than the average responses of 5 normal animals (thin dotted line in each panel). Head or eye traces are inverted as required to facilitate visual comparison; n=number of cycles averaged. (Column 2) Responses for a chinchilla treated bilaterally with gentamicin and implanted with electrodes in the three left SCCs, with prosthetic stimulation off. (Column 3) Responses of same animal to same head rotations, 3.5 h after activation of the multichannel prosthesis. (Adapted with permission from Della Santina et al., 2007).

Figure 2

(A) The Johns Hopkins Multichannel Vestibular Prosthesis (version MVP1) uses three silicon gyroscopes to measure 3D head rotation and a microprocessor to emulate normal semicircular canal sensation and processing. Scale bar units = cm. (B) Rotation of the device about each semicircular canal axis modulates pulse rates on the electrodes implanted in that canal’s ampulla.(C) Stimuli are biphasic, charge-balanced constant-current pulses similar to those used in cochlear implants. (Adapted with permission from Della Santina et al., 2007)

Figure 3

Eye movement responses to pulse-rate modulated, biphasic constant-current pulses delivered via monopolar prosthesis electrodes implanted in the left labyrinth of a stationary alert rhesus monkey tested in darkness. Methods for stimulus delivery and scleral coil recording of eye movements are as described in (Dai et al., 2010). Lower traces show stimulus waveforms modulating pulse rates on electrodes in the left horizontal (LZ), left anterior (LA) and left posterior (LP) semicircular canal ampullary nerves. In each case, modulation frequency is 5 Hz (i.e., encoding a 5 Hz virtual head rotation about the axis of the stimulated canal), baseline pulse rate is 100 pulse/sec, and the three different stimulus intensities shown represent 40%, 60% and 80% of maximum possible pulse frequency modulation depth. (At 100% intensity, pulse rate would modulate down to 0 and up to 400 pulse/sec.) Upper traces show eye movements about the horizontal (Z), left-anterior/right-posterior (LARP), and right-anterior/left-posterior (RALP) axes of the head, which approximately align with the implanted semicircular canals. Slow phase nystagmus segments are black; saccades, quick phases and blinks are shown in gray. Stimulation via each canal’s electrode generates eye movements that approximately align with that canal.