Reduction in excitability of the auditory nerve following electrical stimulation at high stimulus rates

While recent studies have suggested that electrical stimulation of the auditory nerve at high stimulus rates (e.g., 1000 pulses/s) may lead to an improved detection of the fine temporal components in speech among cochlear implant patients, neurophysiological studies have indicated that such stimulation could place metabolic stress on the auditory nerve, which may lead to neural degeneration. To examine this issue we recorded the electrically evoked auditory brainstem response (EABR) of guinea pigs following acute bipolar intracochlear electrical stimulation using charge-balanced biphasic current pulses at stimulus rates varying from 100 to 1000 pulses/s and stimulus intensities ranging from 0.16 to 1.0 microC/phase. Charge density was held constant (approximately 75 microC cm-2 geom/phase) in those experiments. To monitor the recovery in excitability of the auditory nerve following this acute stimulation. EABR thresholds, wave I and III amplitudes and their latencies were determined for periods of up to 12 h following the acute stimulation. Higher stimulus rates and, to a lesser extent, higher intensities led to greater decrements in the post-stimulus EABR amplitude and prolonged the recovery period. While continuous stimulation at 100 pulses/s induced no decrement in the EABR, stimulation at 200 and 400 pulses/s produced an increasingly significant post-stimulus reduction of the EABR amplitude, which showed only partial recovery during the monitoring period. No EABR response could be evoked immediately following stimulation at 1000 pulses/s, using a probe intensity 16-19 dB below the stimulus intensity. However, partial EABR recovery was observed for wave III following stimulation at the lowest stimulus intensity (0.16 microC/phase). These stimulus-induced reductions in the EABR amplitude were also reflected in increased thresholds and latencies. Providing stimulus rate and intensity were held constant, stimulation at different charge densities (37.7, 75.5 and 150.7 microC cm-2 geom/phase) had no influence on the post-stimulus EABR recovery. Significantly, the introduction of a 50% duty cycle into the stimulus pulse train resulted in a more rapid and complete post-stimulus recovery of the EABR compared to continuous stimulation. These data suggest that stimulus rate is a major contributor to the observed reduction in excitability of the electrically stimulated auditory nerve. This reduction may be a result of an activity-induced depletion of neural energy resources required to maintain homeostasis. The present findings have implications for the design of safe speech-processing strategies for use in multichannel cochlear implants.