Electrical excitation of the acoustically sensitive auditory nerve: single-fiber responses to electric pulse trains

Abstract

Nearly all studies on auditory-nerve responses to electric stimuli have been conducted using chemically deafened animals so as to more realistically model the implanted human ear that has typically been profoundly deaf. However, clinical criteria for implantation have recently been relaxed. Ears with "residual" acoustic sensitivity are now being implanted, calling for the systematic evaluation of auditory-nerve responses to electric stimuli as well as combined electric and acoustic stimuli in acoustically sensitive ears. This article presents a systematic investigation of single-fiber responses to electric stimuli in acoustically sensitive ears. Responses to 250 pulse/s electric pulse trains were collected from 18 cats. Properties such as threshold, dynamic range, and jitter were found to differ from those of deaf ears. Other types of fiber activity observed in acoustically sensitive ears (i.e., spontaneous activity and electrophonic responses) were found to alter the temporal coding of electric stimuli. The electrophonic response, which was shown to greatly change the information encoded by spike intervals, also exhibited fast adaptation relative to that observed in the "direct" response to electric stimuli. More complex responses, such as "buildup" (increased responsiveness to successive pulses) and "bursting" (alternating periods of responsiveness and unresponsiveness) were observed. Our findings suggest that bursting is a response unique to sustained electric stimulation in ears with functional hair cells.

Fig. 1

Summary of basic acoustic properties of fibers of this study. (A) Acoustic thresholds and best frequencies for 137 fibers. Symbol types classify each fiber as low or high SR and whether or not electric stimulation evoked an identifiable β response. Two contour lines are shown. The solid contour represents the mean thresholds for high-SR fibers of normal-hearing cats (Liberman and Kiang 1978), whereas the dashed line indicates mean thresholds for low-SR fibers of normal-hearing cats, computed using the low-SR correction data of Liberman (1978). (B) Acoustic threshold shifts computed using these two threshold contours. The dashed horizontal line indicates the mean threshold shift (26.4 dB). The approximate location of the stimulating electrode is indicated by the symbol in the bottom right of the graph.

Fig. 2

Examination of within- and across-animal variation of fiber acoustic threshold shifts. Shifts were computed in the manner used for Fig. 1. (A) Threshold shifts for all cats that yielded acoustic data for at least five fibers. The mean shift for the last six cat experiments was 21.5 dB. (B) Acoustic threshold shift versus time of data acquisition for fibers of the two cats (D45, D47) that yielded the most data. The arrows along the abscissa indicate the data collection starting time and completion time in hours and minutes. The data are fit to linear regression lines.

Fig. 3

Spontaneous rate histograms for the fibers of this study (top plot) and the fibers of the Liberman and Kiang (1978) study (bottom plot).

Fig. 4

(A) Firing efficiency (FE) versus sweep number for four fibers and three stimulus levels per fiber. For each sweep, FEs were computed by collapsing fiber activity across the entire epoch of each 300-ms pulse train. The number in the top right corner of each graph indicates stimulus level in mA. (B) Response probabilities for two fibers over the entire time of data collection. Vertical lines separate data for each file (i.e., set of repeated pulse trains) and the numbers at the top of each graph indicate stimulus level in mA.

Fig. 5

Comparison of fiber thresholds (left panel) and fiber dynamic ranges (right panel) from the “hearing ears” of this study and the “deaf ears” from the study of Miller et al. (2001b). The solid line segments indicate linear regression results; the dashed line represents the linear regression obtained after removing the top two points indicated by asterisks.

Fig. 6

Period histograms for a fiber exhibiting both “direct” (α) responses and electrophonic (β) responses, as evidenced by two distinct modes. Each row corresponds to a different stimulus level (indicated along the right margin of the figure) and each column corresponds to a different analysis window (indicated at the top of each column). The histograms indicate that the β response is dominant at the lowest levels and prone to relatively fast adaptation. The two numbers (in italics) shown in each graph indicate the firing efficiency of the α and β responses.

Fig. 7

Poststimulus time (PST) histograms for two fibers that exhibited both a direct response (filled symbols) and an electrophonic response (open symbols). Each electrophonic curve is fit to a decaying exponential curve. Along with the stimulus current level, the fitted time constant (τ) and coefficient of determination (r²) are shown in each panel.

Fig. 8

Frequency spectra of the interval histograms of a fiber (D41-2-6) exhibiting both a direct (α) and an electrophonic (β) response. Fast Fourier transform spectra were computed as described in the text.

Fig. 9

(A) Temporal dispersion (jitter) plotted as a function of firing efficiency for 118 fibers. The symbol type indicates whether or not the fiber was a low- or high-SR fiber, and fibers in which an electrophonic response was evident. Firing efficiencies greater than 1 were observed in some fibers with high spontaneous rates and electrophonic responses. (B) Jitter at a firing efficiency of 50% plotted as a function of spontaneous rate. Also shown (by the horizontal line) is the mean jitter (again at an FE 50%) for deaf fibers from cats of Miller et al. (2001b).

Fig. 10

PST histograms for four fibers, assessed at four stimulus levels each, using both narrow (50 μs) bin widths (upper set of histograms) and wide (4 ms) bin widths (lower set of histograms). Also plotted on the lower set are the mean jitter values for each 4-ms bin. In that set, jitter data are plotted using open symbols, while filled symbols indicate FE values.

Fig. 11

Shown in the lower graph is a plot of a binary variable indicating the presence or absence of the “buildup” response as a function of acoustic threshold shift. Each circle indicates an individual fiber. The two upper graphs show the incidence of the buildup response as a function of the category (low, high) of spontaneous rate and as a function of the presence or absence of an electrophonic response.

Fig. 12

Dot-raster plots of the responses to 300-ms pulse trains in three fibers exhibiting “bursting” patterns. The plots obtained at three different stimulus levels are shown in each column, with the current levels indicated in the top right corner of each plot.

Fig. 13

Histograms of the length of each sequence of spikes (filled symbols) and the length of each sequence of spike failures (open symbols) are shown for seven fibers that exhibited bursting.

Fig. 14

Dot-raster plots of a fiber exhibiting bursting. Three different stimuli were used. In the top plot, a 96-dB SPL wideband noise stimulus was presented for 100 ms, beginning at 50 ms. In the middle plot, the standard 250 pulse/s electric train was presented. In the bottom plot, both of the above stimuli were presented together. In that plot, note the loss of the bursting pattern following offset of the acoustic stimulus.