Examining the auditory nerve fiber response to high rate cochlear implant stimulation: chronic sensorineural hearing loss and facilitation

Abstract

Neural prostheses, such as cochlear and retinal implants, induce perceptual responses by electrically stimulating sensory nerves. These devices restore sensory system function by using patterned electrical stimuli to evoke neural responses. An understanding of their function requires knowledge of the nerves responses to relevant electrical stimuli as well as the likely effects of pathology on nerve function. We describe how sensorineural hearing loss (SNHL) affects the response properties of single auditory nerve fibers (ANFs) to electrical stimuli relevant to cochlear implants. The response of 188 individual ANFs were recorded in response to trains of stimuli presented at 200, 1,000, 2,000, and 5,000 pulse/s in acutely and chronically deafened guinea pigs. The effects of stimulation rate and SNHL on ANF responses during the 0-2 ms period following stimulus onset were examined to minimize the influence of ANF adaptation. As stimulation rate increased to 5,000 pulse/s, threshold decreased, dynamic range increased and first spike latency decreased. Similar effects of stimulation rate were observed following chronic SNHL, although onset threshold and first spike latency were reduced and onset dynamic range increased compared with acutely deafened animals. Facilitation, defined as an increased nerve excitability caused by subthreshold stimulation, was observed in both acute and chronic SNHL groups, although the magnitude of its effect was diminished in the latter. These results indicate that facilitation, demonstrated here using stimuli similar to those used in cochlear implants, influences the ANF response to pulsatile electrical stimulation and may have important implications for cochlear implant signal processing strategies.

Figures

Fig. 1.

Spiral ganglion cell density. Representative photomicrographs taken from the upper basal turn (i.e., turn 1) in Rosenthal's canal of an acutely (A) and chronically (B) deafened guinea pig. C: spiral ganglion neuron density (means ± SE) was calculated at each cochlear turn (1 = basal, 4 = apical). Spiral ganglion neuron density was lower across all cochlear turns in the chronic sensorineural hearing loss group.

Fig. 2.

Electrically evoked auditory brain stem response. Example electrically evoked auditory brain stem response waveforms recorded from an acutely and chronically deafened guinea pig. The wave III response occurs ∼2–3 ms following the stimulus pulse, and the response amplitude increased with stimulus current level in all guinea pigs studied. At each stimulus current level, 2 averaged response recordings are shown. The first 800 μs () of the recording has been “blanked out,” masking the large-amplitude stimulus artifact and the wave I response.

Fig. 3.

Electrically evoked auditory nerve fiber spike waveforms. A: representative auditory nerve fiber spike waveforms of a single fiber, following stimulus artifact removal, recorded from an acutely deafened guinea pig. The number of spikes evoked increased with stimulus current level across all stimulation rates examined. The number of spikes evoked also varied with stimulation rate and changed across the stimulus duration. B: multiple spikes obtained at a single stimulus current level (700 μA) overlaid against each other for the fiber shown above. While spike amplitude was somewhat variable, spike waveform was consistent across stimulation rate and current levels.

Fig. 4.

Peri-stimulus time histograms. A: peristimulus time histograms (PSTHs), calculated for the auditory nerve fiber shown in Fig. 3, calculated over the entire stimulus duration. The average spike rate varied with stimulus current level and stimulation rate and decreased (i.e., adapted) over the stimulus duration. B: an expanded view of the first 2 ms following the stimulus onset at 600 μA as a function of stimulation rate showing increased activity during the onset period as stimulation rate increased.

Fig. 5.

Auditory nerve fiber threshold and dynamic range. A: threshold (means ± SE), calculated at 3 onset spike probabilities (0.1, 0.5, 0.9). B: dynamic range (shown as the median and interquartile range) calculated for the onset period, measured as a function of stimulation rate. As stimulation rate increased, onset threshold decreased and dynamic range increased. Compared with the acute sensorineural hearing loss (SNHL) group, thresholds were lower and dynamic range was wider in the chronically deafened cohort.

Fig. 6.

Predicting the facilitation effect. The cumulative probability function, calculated over the onset (0–2 ms) period for a representative fiber, is shown for an independent stimulus pulse (left). The onset response predicted in response to stimuli presented at 5,000 pulse/s (right), assuming the fiber's response to each pulse is independent. The measured onset response to stimuli presented at 5,000 pulses/s is also shown (right). The onset probability is the value of the cumulative probability function at the 2 ms time point, and the facilitation effect is estimated as the difference between the measured and predicted response.

Fig. 7.

Onset response and the facilitation effect. The onset spike probability (A, C, and E) and facilitation effect (B, D, and F) measured as a function of stimulation rate at 3 levels across the fibers dynamic range. Levels, defined as the current level(s) that evoked a specified spike probability over the onset period at 200 pulse/s, are high (0.75–0.98, A and B), moderate (0.3–0.7, C and D), and low (0.02–0.18, E and F). Onset spike probability increased with stimulation rate across all levels; the greatest magnitude increase occurred at low spike probabilities. Facilitation was partially responsible for the increase in onset spike probability at low levels, although its effect was diminished in the chronic SNHL group. At moderate and high levels, the measured onset probability was lower than that predicted at 1,000 pulse/s using our simple approach, giving rise to “negative” facilitation. Data are displayed using median and interquartile range values.

Fig. 8.

First spike latency and jitter. Median first spike latency (A, C, and E) and jitter (B, D, and F) measured as a function of stimulation rate at 3 levels across the fibers dynamic range. Levels, defined by the spike probability calculated over the onset period, are high (0.75–0.98, A and B), moderate (0.3–0.7, C and D), and low (0.02–0.18, E and F). Latency and jitter decreased with increasing level and latency was shorter in the chronically deafened group. At low and moderate levels, latency and jitter were greater at 1,000 and 2,000 pulse/s compared with 200 and 5,000 pulse/s; no significant differences between 200 and 5,000 pulse/s were observed. At high levels, no effect of stimulation rate on latency was observed. Data are displayed using median and interquartile range values.