Steven M. Bierer

Modeling the electrode–neuron interface of cochlear implants: Effects of neural survival, electrode placement, and the partial tripolar configuration

The partial tripolar electrode configuration is a relatively novel stimulation strategy that can generate more spatially focused electric fields than the commonly used monopolar configuration. Focused stimulation strategies should improve spectral resolution in cochlear implant users, but may also be more sensitive to local irregularities in the electrode-neuron interface. In this study, we develop a practical computer model of cochlear implant stimulation that can simulate neural activation in a simplified cochlear geometry and we relate the resulting patterns of neural activity to basic psychophysical measures. We examine how two types of local irregularities in the electrode-neuron interface, variations in spiral ganglion nerve density and electrode position within the scala tympani, affect the simulated neural activation patterns and how these patterns change with electrode configuration. The model shows that higher partial tripolar fractions activate more spatially restricted populations of neurons at all current levels and require higher current levels to excite a given number of neurons. We find that threshold levels are more sensitive at high partial tripolar fractions to both types of irregularities, but these effects are not independent. In particular, at close electrode-neuron distances, activation is typically more spatially localized which leads to a greater influence of neural dead regions.

Implantation of the Semicircular Canals with Preservation of Hearing and Rotational Sensitivity: a vestibular neurostimulator suitable for clinical research

Hypothesis It is possible to implant a stimulating electrode array in the semicircular canals without damaging rotational sensitivity or hearing. The electrodes will evoke robust and precisely controlled eye movements. Background A number of groups are attempting to develop a neural prosthesis to ameliorate abnormal vestibular function. Animal studies demonstrate that electrodes near the canal ampullae can produce electrically evoked eye movements. The target condition of these studies is typically bilateral vestibular hypofunction. Such a device could potentially be more widely useful clinically and would have a simpler roadmap to regulatory approval if it produced minimal or no damage to the native vestibular and auditory systems. Methods An electrode array was designed for insertion into the bony semicircular canal adjacent to the membranous canal. It was designed to be sufficiently narrow so as to not compress the membranous canal. The arrays were manufactured by Cochlear, Ltd., and linked to a Nucleus Freedom receiver/stimulator. Seven behaviorally trained rhesus macaques had arrays placed in 2 semicircular canals using a transmastoid approach and “soft surgical” procedures borrowed from Hybrid cochlear implant surgery. Postoperative vestibulo-ocular reflex was measured in a rotary chair. Click-evoked auditory brainstem responses were also measured in the 7 animals using the contralateral ear as a control. Results All animals had minimal postoperative vestibular signs and were eating within hours of surgery. Of 6 animals tested, all had normal postoperative sinusoidal gain. Of 7 animals, 6 had symmetric postoperative velocity step responses toward and away from the implanted ear. The 1 animal with significantly asymmetric velocity step responses also had a significant sensorineural hearing loss. One control animal that underwent canal plugging had substantial loss of the velocity step response toward the canal-plugged ear. In 5 animals, intraoperative electrically evoked vestibular compound action potential recordings facilitated electrode placement. Postoperatively, electrically evoked eye movements were obtained from electrodes associated with an electrically evoked vestibular compound action potential wave form. Hearing was largely preserved in 6 animals and lost in 1 animal. Conclusion It is possible to implant the vestibular system with prosthetic stimulating electrodes without loss of rotational sensitivity or hearing. Because electrically evoked eye movements can be reliably obtained with the assistance of intraoperative electrophysiology, it is appropriate to consider treatment of a variety of vestibular disorders using prosthetic electrical stimulation. Based on these findings, and others, a feasibility study for the treatment of human subjects with disabling Ménière’s disease has begun.

Prosthetic implantation of the human vestibular system

Hypothesis A functional vestibular prosthesis can be implanted in human such that electrical stimulation of each semicircular canal produces canal-specific eye movements while preserving vestibular and auditory function. Background A number of vestibular disorders could be treated with prosthetic stimulation of the vestibular end organs. We have previously demonstrated in rhesus monkeys that a vestibular neurostimulator, based on the Nucleus Freedom cochlear implant, can produce canal-specific electrically evoked eye movements while preserving auditory and vestibular function. An investigational device exemption has been obtained from the FDA to study the feasibility of treating uncontrolled Ménière’s disease with the device. Methods The UW/Nucleus vestibular implant was implanted in the perilymphatic space adjacent to the three semicircular canal ampullae of a human subject with uncontrolled Ménière’s disease. Preoperative and postoperative vestibular and auditory function was assessed. Electrically evoked eye movements were measured at 2 time points postoperatively. Results Implantation of all semicircular canals was technically feasible. Horizontal canal and auditory function were largely, but not totally, lost. Electrode stimulation in 2 of 3 canals resulted in canal-appropriate eye movements. Over time, stimulation thresholds increased. Conclusion Prosthetic implantation of the semicircular canals in humans is technically feasible. Electrical stimulation resulted in canal-specific eye movements, although thresholds increased over time. Preservation of native auditory and vestibular function, previously observed in animals, was not demonstrated in a single subject with advanced Ménière’s disease.

Partial tripolar cochlear implant stimulation: Spread of excitation and forward masking in the inferior colliculus

This study examines patterns of neural activity in response to single biphasic electrical pulses, presented alone or following a forward masking pulse train, delivered by a cochlear implant. Recordings were made along the tonotopic axis of the central nucleus of the inferior colliculus (ICC) in ketamine/xylazine anesthetized guinea pigs. The partial tripolar electrode configuration was used, which provided a systematic way to vary the tonotopic extent of ICC activation between monopolar (broad) and tripolar (narrow) extremes while maintaining the same peak of activation. The forward masking paradigm consisted of a 200 ms masker pulse train (1017 pulses per second) followed 10 ms later by a single-pulse probe stimulus; the current fraction of the probe was set to 0 (monopolar), 1 (tripolar), or 0.5 (hybrid), and the fraction of the masker was fixed at 0.5. Forward masking tuning profiles were derived from the amount of masking current required to just suppress the activity produced by a fixed-level probe. These profiles were sharper for more focused probe configurations, approximating the pattern of neural activity elicited by single (non-masked) pulses. The result helps to bridge the gap between previous findings in animals and recent psychophysical data.

Characterization of the electrically-evoked compound action potential of the vestibular nerve

Objective: We recorded intraoperative and postoperative electrically evoked compound action potentials (ECAPs) in rhesus monkeys implanted with a vestibular neurostimulator. The objectives were to correlate the generation of slow-phase nystagmus or eye twitches induced by electrical stimulation of the implanted semicircular canal with the presence or absence of the vestibular ECAP responses and to assess the effectiveness of ECAP monitoring during surgery to guide surgical insertion of electrode arrays into the canals. Design: Four rhesus monkeys (a total of 7 canals) were implanted with a vestibular neurostimulator modified from the Nucleus Freedom cochlear implant. ECAP recordings were obtained during surgery or at various intervals after surgery using the Neural Response Telemetry feature of the clinical Custom Sound EP software. Eye movements during electrical stimulation of individual canals were recorded with a scleral search coil system in the same animals. Results: Measurable vestibular ECAPs were observed intraoperatively or postoperatively in 3 implanted animals. Robust and sustained ECAPs were obtained in 3 monkeys at the test intervals of 0, 7, or greater than 100 days after implantation surgery. In all 3 animals, stimulation with electrical pulse trains produced measurable eye movements in a direction consistent with the vestibulo-ocular reflex from the implanted semicircular canal. In contrast, electrically evoked eye movements could not be measured in 3 of the 7 implanted canals, none of which produced distinct vestibular ECAPs. In 2 animals, ECAP waveforms were systematically monitored during surgery, and the procedure proved crucial to the success of vestibular implantation. Conclusion: Vestibular ECAPs exhibit similar morphology and growth characteristics to cochlear ECAPs from human cochlear implant patients. The ECAP measure is well correlated with the functional activation of eye movements by electrical stimulation after implantation surgery. The intraoperative ECAP recording technique is an efficient tool to guide the placement of electrode array into the semicircular canals.

An Experimental Vestibular Neural Prosthesis: Design and Preliminary Results With Rhesus Monkeys Stimulated With Modulated Pulses

A vestibular neural prosthesis was designed on the basis of a cochlear implant for treatment of Menieres disease and other vestibular disorders. Computer control software was developed to generate patterned pulse stimuli for exploring optimal parameters to activate the vestibular nerve. Two rhesus monkeys were implanted with the prototype vestibular prosthesis and they were behaviorally evaluated post implantation surgery. Horizontal and vertical eye movement responses to patterned electrical pulse stimulations were collected on both monkeys. Pulse amplitude modulated (PAM) and pulse rate modulated (PRM) trains were applied to the lateral canal of each implanted animal. Robust slow-phase nystagmus responses following the PAM or PRM modulation pattern were observed in both implanted monkeys in the direction consistent with the activation of the implanted canal. Both PAM and PRM pulse trains can elicit a significant amount of in-phase modulated eye velocity changes and they could potentially be used for efficiently coding head rotational signals in future vestibular neural prostheses.

Auditory outcomes following implantation and electrical stimulation of the semicircular canals

We measured auditory brainstem responses (ABRs) in eight Rhesus monkeys after implantation of electrodes in the semicircular canals of one ear, using a multi-channel vestibular prosthesis based on cochlear implant technology. In five animals, click-evoked ABR thresholds in the implanted ear were within 10 dB of thresholds in the non-implanted control ear. Threshold differences in the remaining three animals varied from 18 to 69 dB, indicating mild to severe hearing losses. Click- and tone-evoked ABRs measured in a subset of animals before and after implantation revealed a comparable pattern of threshold changes. Thresholds obtained five months or more after implantation--a period in which the prosthesis regularly delivered electrical stimulation to achieve functional activation of the vestibular system--improved in three animals with no or mild initial hearing loss and increased in a fourth with a moderate hearing loss. These results suggest that, although there is a risk of hearing loss with unilateral vestibular implantation to treat balance disorders, the surgery can be performed in a manner that preserves hearing over an extended period of functional stimulation.

Optical nerve stimulation for a vestibular prosthesis

Infrared Nerve Stimulation (INS) offers several advantages over electrical stimulation, including more precise spatial selectivity and improved surgical access. In this study, INS and electrical stimulation were compared in their ability to activate the vestibular branch of the VIIIth nerve, as a potential way to treat balance disorders. The superior and lateral canals of the vestibular system of Guinea pigs were identified and approached with the aid of precise 3-D reconstructions. A monopolar platinum stimulating electrode was positioned near the ampullae of the canals, and biphasic current pulses were used to stimulate vestibular evoked potentials and eye movements. Thresholds and input/output functions were measured for various stimulus conditions. A short pulsed diode laser (Capella, Lockheed Martin-Aculight, Inc., Bothell WA) was placed in the same anatomical position and various stimulus conditions were evaluated in their ability to evoke similar potentials and eye movements.

Real-time communication of head velocity and acceleration for an externally mounted vestibular prosthesis

Loss of vestibular function results in imbalance, disorientation, and oscillopsia. Several groups have designed and constructed implantable devices to restore vestibular function through electrical stimulation of the vestibular nerve. We have designed a two-part device in which the head motion sensing and signal processing elements are externally mounted to the head, and are coupled through an inductive link to a receiver stimulator that is based on a cochlear implant. The implanted electrode arrays are designed to preserve rotational sensitivity in the implanted ear. We have tested the device in rhesus monkeys by rotating the animals in the plane of the implanted canals, and then using head velocity and acceleration signals to drive electrical stimulation of the vestibular system. Combined electrical and rotational stimulation results in a summation of responses, so that one can control the modulation of eye velocity induced by sinusoidal yaw rotation.

Longitudinal performance of a vestibular prosthesis as assessed by electrically evoked compound action potential recording

Electrical stimulation of the vestibular end organ with a vestibular prosthesis may provide an effective treatment for vestibular loss if the stimulation remains effective over a significant period of time after implantation of the device. To assess efficacy of electrical stimulation in an animal model, we implanted 3 rhesus monkeys with a vestibular prosthesis based on a cochlear implant. We then recorded vestibular electrically evoked compound action potentials (vECAPs) longitudinally in each of the implanted canals to see how the amplitude of the response changed over time. The results suggest that vECAPs, and therefore electrical activation of vestibular afferent fibers, can remain largely stable over time following implantation.