Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis

Abstract

An implantable prosthesis that stimulates vestibular nerve branches to restore sensation of head rotation and vision-stabilizing reflexes could benefit individuals disabled by bilateral loss of vestibular sensation. The normal vestibular system encodes head movement by increasing or decreasing firing rate of the vestibular afferents about a baseline firing rate in proportion to head rotation velocity. Our multichannel vestibular prosthesis emulates this encoding scheme by modulating pulse rate and pulse current amplitude above and below a baseline stimulation rate (BSR) and a baseline stimulation current. Unilateral baseline prosthetic stimulation that mimics normal vestibular afferent baseline firing results in vestibulo-ocular reflex (VOR) eye responses with a wider range of eye velocity in response to stimuli modulated above baseline (excitatory) than below baseline (inhibitory). Stimulus modulation about higher than normal baselines resulted in increased range of inhibitory eye velocity, but decreased range of excitatory eye velocity. Simultaneous modulation of rate and current (co-modulation) above all tested baselines elicited a significantly wider range of excitatory eye velocity than rate or current modulation alone. Time constants associated with the recovery of VOR excitability following adaptation to elevated BSRs implicate synaptic vesicle depletion as a possible mechanism for the small range of excitatory eye velocity elicited by rate modulation alone. These findings can be used toward selecting optimal baseline levels for vestibular stimulation that would result in large inhibitory eye responses while maintaining a wide range of excitatory eye velocity via co-modulation.

Characterization of pulse amplitude and pulse rate modulation for a human vestibular implant during acute electrical stimulation

“…This finding was consistent with reports in chinchillas and monkeys, where PRM levels did not significantly affect peak eye velocities at similarly high baseline pulse rates (Davidovics et al 2012. Only patient 2 showed significant differences between some PRM levels, which were possibly facilitated by the large dynamic range in that patient.…”

“…In other studies, increasing pulse amplitude by 100% or more led to markedly larger peak eye velocities (Davidovics et al 2012, Nie et al 2013, Phillips et al 2015. Our patients, however, had limited dynamic ranges and thus only modest increases between medium and high PAM levels.…”

Multichannel Vestibular Prosthesis Employing Modulation of Pulse Rate and Current with Alignment Precompensation Elicits Improved VOR Performance in Monkeys

“…2). A possible explanation for this phenomenon (when observed in chinchillas) was offered by Davidovics et al (2012). They suggested that increasing either current amplitude or pulse rate may increase the total number of action potentials (AP) firing on a vestibular afferent nerve since larger currents can increase the region of neural excitation, thereby recruiting more neural fibers to fire, and higher pulse rates can entrain a given population of nerve fibers to fire at higher frequencies (BeMent and Ranck 1969).…”

“…Secondly, monkey eye movements were elicited using co-modulated stimuli, whereas chinchilla eye movements were elicited using rate-modulated stimuli. Since misalignment increases with increasing current Davidovics et al 2011Davidovics et al , 2012, it is likely that responses to co-modulating stimuli (which have varying current amplitudes) of different intensities would have different degrees of misalignment. Significant differences in response misalignment between different octants would necessitate eight unique transformation matrices to significantly improve alignment.…”

“…We extended this approach to a multichannel vestibular prosthesis (MVP) that senses 3D head rotation and encodes it via stimulation of all three ampullary nerves in the labyrinth, and we demonstrated its ability to partly restore the 3D VOR in both rodents and rhesus monkeys rendered vestibular deficient via bilateral intratympanic injection of gentamicin (Della Santina et al 2005aFridman et al 2010a;Dai et al 2011b, c;Davidovics et al 2011Davidovics et al , 2012Sun et al 2011).…”