Simultaneous activation of multiple vestibular pathways upon electrical stimulation of semicircular canal afferents

Abstract

Background and purpose: Vestibular implants seem to be a promising treatment for patients suffering from severe bilateral vestibulopathy. To optimize outcomes, we need to investigate how, and to which extent, the different vestibular pathways are activated. Here we characterized the simultaneous responses to electrical stimuli of three different vestibular pathways.

Methods: Three vestibular implant recipients were included. First, activation thresholds and amplitude growth functions of electrically evoked vestibulo-ocular reflexes (eVOR), cervical myogenic potentials (ecVEMPs) and vestibular percepts (vestibulo-thalamo-cortical, VTC) were recorded upon stimulation with single, biphasic current pulses (200 µs/phase) delivered through five different vestibular electrodes. Latencies of eVOR and ecVEMPs were also characterized. Then we compared the amplitude growth functions of the three pathways using different stimulation profiles (1-pulse, 200 µs/phase; 1-pulse, 50 µs/phase; 4-pulses, 50 µs/phase, 1600 pulses-per-second) in one patient (two electrodes).

Results: The median latencies of the eVOR and ecVEMPs were 8 ms (8-9 ms) and 10.2 ms (9.6-11.8 ms), respectively. While the amplitude of eVOR and ecVEMP responses increased with increasing stimulation current, the VTC pathway showed a different, step-like behavior. In this study, the 200 µs/phase paradigm appeared to give the best balance to enhance responses at lower stimulation currents.

Conclusions: This study is a first attempt to evaluate the simultaneous activation of different vestibular pathways. However, this issue deserves further and more detailed investigation to determine the actual possibility of selective stimulation of a given pathway, as well as the functional impact of the contribution of each pathway to the overall rehabilitation process.

Keywords: Bilateral vestibulopathy; Electrical stimulation; Neuroprosthesis; Vestibular implant; Vestibulo-ocular reflex; Vestibulo-spinal reflex.

Conflict of interest statement

AB, CC, NG, RVdB and APF have received travel and research grants from MED-EL Elektromedizinische Geräte GmbH (Innsbruck, Austria).

Figures

Fig. 1

Example of recordings and data processing of results obtained in patient S1 (SAN electrode) upon stimulation with a charge-balanced, cathodic-first, biphasic current pulse of 200 µs per phase. a Horizontal, vertical, and vector norm components of the averaged eVOR signal (respectively, solid dark red, solid orange, and dotted green lines). LATeVOR marks the beginning of the eye movement (i.e., the latency), and P1 marks the first peak of the total peak eye velocity vector (P1VOR). b Example of the evolution of the norm of the eye velocity vector (PEV) while applying increasing stimulation currents from 0 to 475 µA. c Average ecVEMP response. P1 and N1 mark the location of the first positive and second negative peak of the response, respectively, to stimulation currents ranging from 0 to 475 µA. Note that each of the panels represents a different response. Consequently, the vertical axes of each graph have different scales (see the scale bars in each panel)

Fig. 2

Latencies of the eVOR and ecVEMP responses elicited upon stimulation with a biphasic, charge-balanced, cathodic-first current pulse of 200 µs per phase at the UCL (see also Fig. 3). Box plots indicate median values, 25th and 75th percentile values (coloured boxes) as well as 10th and 90th percentile values (error bars) for all subjects and all electrodes tested. Three patients participated in this experiment (S1, S2 and S3), in whom a total of five electrodes were tested (S1-SAN, S1-LAN, S2-SAN, S2-LAN and S3-PAN)

Fig. 3

Growth function of the normalized amplitude of the P1 eVOR (red plot), the N–P amplitude for ecVEMPs (orange plot), and individual self-reported percept intensity (green plot) versus current amplitude. Each panel represents responses measured simultaneously in one subject and upon stimulation with one vestibular electrode, for a single-pulse stimulation paradigm, 200 µs phase width

Fig. 4

Growth function of the amplitude of the eVOR P1, the ecVEMPs P1 and individual self-reported percept recorded using different stimulation profiles (single pulse, 50 µs per phase—red plot; single pulse, 200 µs per phase—orange plot; train of four pulses, 50 µs per phase, 1600 pps—green plot) versus current amplitude. Only subject S1 was available for this experiment where two electrodes were investigated (electrode SAN—left column and LAN—right column)

Fig. 5

Slope of the growth function of eVOR (left panels) and ecVEMP responses, calculated using linear regression analyses of the normalized data versus stimulation current (see also Fig. 4). Three stimulation paradigms are compared: single pulse, 50 µs per phase—red plot; single pulse, 200 µs per phase—orange plot; train of four pulses, 50 µs per phase, 1600 pps—green plot) versus current amplitude. Only subject S1 was available for this experiment where two electrodes were investigated (electrode SAN—upper line and LAN—lower line). Note that the slope of the growth function for the intensity of percepts was not calculated since it showed a step-like behavior (not a monotonical increase with respect to stimulation current)