Tonotopic distribution of short-term adaptation properties in the cochlear nerve of normal and acoustically overexposed chicks

Abstract

Cochlear nerve adaptation is thought to result, at least partially, from the depletion of neurotransmitter stores in hair cells. Recently, neurotransmitter vesicle pools have been identified in chick tall hair cells that might play a role in adaptation. In order to understand better the relationship between adaptation and neurotransmitter release dynamics, short-term adaptation was characterized by using peristimulus time histograms of single-unit activity in the chick cochlear nerve. The adaptation function resulting from 100-ms pure tone stimuli presented at the characteristic frequency, +20 dB relative to threshold, was well described as a single exponential decay process with an average time constant of 18.6+/-0.8 ms (mean+/-SEM). The number of spikes contributed by the adapting part of the response increased tonotopically for characteristic frequencies up to approximately 0.8 kHz. Comparison of the adaptation data with known physiological and anatomical hair cell properties suggests that depletion of the readily releasable pool is the basis of short-term adaptation in the chick. With this idea in mind, short-term adaptation was used as a proxy for assessing tall hair cell synaptic function following intense acoustic stimulation. After 48 h of exposure to an intense pure tone, the time constant of short-term adaptation was unaltered, whereas the number of spikes in the adapting component was increased at characteristic frequencies at and above the exposure frequency. These data suggest that the rate of readily releasable pool emptying is unaltered, but the neurotransmitter content of the pool is increased, by exposure to intense sound. The results imply that an increase in readily releasable pool size might be a compensatory mechanism ensuring the strength of the hair cell afferent synapse in the face of ongoing acoustic stress.

FIG. 1

Analysis of PST histograms. The raw data were collected with a sampling resolution of 0.1 ms (upper plot). The histograms were re-binned at 1.0-ms resolution to decrease the local variability (lower plot). Parameters describing the PST response at 1.0-ms resolution are defined as follows: peak firing rate = maximum driven firing rate; adapted firing rate = average firing rate during the 91st through 100th 1-ms bins after stimulus onset (blackened portion of the gray curve); percent adaptation = percent change from the peak to adapted firing rate; phasic component (dark gray area) = number of spikes in the adapting part of the curve. The single exponential fit [Eq. (1), dashed line] of the adaptation function (gray curve) provided the adaptation time constant, as well as the predicted final adapted rate (y₀) for this stage of adaptation.

FIG. 2

Example PST histograms and adaptation curve fits. Left-hand panels show an example histogram from each CF analysis bin for normal ears described in Methods. Right-hand panels show the adapting portion of the same histograms in greater detail. The adaptation function of each PST histogram is fit with both single and double exponentials [Eqs. (1) and (2)]. The adaptation functions were well described by the single exponential equation.

FIG. 3

Averaged PST histograms. The PST histograms analyzed for each of the CF bins were averaged to generate composite histograms for each frequency range. The center frequency of the CF bin is shown for each plot. High CF units appeared to have larger, more quickly adapting onset responses than units with low CFs.

FIG. 4

Analysis of PST histogram parameters. Circles represent data for individual units, whereas the squares with error bars (SEM) are the means for the same data when grouped into the CF bins. (A) Units showed a progressive increase in the peak firing rate across CF (p < 0.001). (B) The adapted firing rates were more constant (only the 0.41-kHz bin was significantly different from the 0.13-kHz bin). (C) The adapted rates directly measured from the histograms showed a near one-to-one relationship (linear regression slope = 0.95) with the predicted asymptotic rates from single exponential fits, indicating that this stage of adaptation is complete by the end of the 100-ms stimulus. (D) Percent adaptation was greatest in high CF units (p < 0.001). (E) Units with higher CFs generally adapted more quickly (p < 0.001). Time constants were in the range of those classified as “short-term” adaptation in mammals. (F) The number of spikes in the phasic component of the response grew up to the 0.73-kHz CF bin (p < 0.001). Above this bin, the phasic component remained constant. (n ≥ 137 for each scatter plot.)

FIG. 5

Summary of stimulus level manipulation. Peak (A) and adapted (B) rates were increased at the higher stimulus level, but the percent adaptation (C) and time constant (D) were stable. (E) Histogram collected at 100 dB SPL where the adaptation function was better described as a double exponential decay process. This histogram was excluded from the analysis of time constant in D. (n = 14 for A, B, and C; n = 13 for D.)

FIG. 6

Analysis of stimulus frequency effects on histogram parameters. Left-hand panels represent the data collected when units were stimulated both at and below the CF, whereas the right-hand panels represent the data collected when units were stimulated both at and above the CF. The data are broken into two CF ranges: CF ≤ 829 Hz and CF > 829 Hz. Asterisk (*) denotes significantly different from the “at CF” condition within the same CF group. The adaptation time constant of units with an 829-Hz or less CF was sensitive to stimulus frequency when stimulated below the CF. Peak and adapted firing rates of units with CFs above 829 Hz were sensitive to stimulation below the CF.

FIG. 7

Effect of acoustic overexposure on threshold and spontaneous activity. Exposure to the 0.9-kHz, 120-dB SPL tone for 48 h produced similar effects on threshold and spontaneous activity as those reported previously (Saunders et al. 1996b). PST histograms from these units were analyzed to determine the effects of acoustic overexposure on PST histogram parameters.

FIG. 8

Averaged PST histograms for the acoustic overexposure. When the histograms from each CF bin described in Methods for the acoustic overexposure experiment were averaged, an exaggerated onset response in exposed units was seen in comparison to age-matched controls, particularly in units in the 1.14- and 2.29-kHz CF bins. Note the similar activity level to which control and exposed units adapted. The center frequency of the CF bin is shown for each plot.

FIG. 9

Analysis of PST histogram parameters for the acoustic overexposure. (A) Peak firing rates were elevated after the exposure in the 1.14- and 2.29-kHz bins (p < 0.05). (B) The adapted firing rates were unchanged. (C) In both control and exposed units, the adapted rates directly measured from the histograms were comparable to the asymptotic rates predicted from single exponential fits (linear regression slopes = 0.95 for both conditions), indicating that the short-term adaptation stage was complete by the end of the stimulus for both groups. (D) Percent adaptation was increased in the three highest CF bins (p < 0.05). (E) The short-term adaptation time constant was unaltered by the exposure. (F) The phasic component of the response was significantly larger (p < 0.05) in exposed units for all CF bins except 0.14 kHz. (For parameters that relied on single exponential fits, the four histograms with double exponential adaptation functions were excluded from the analysis. n ≥ 78 for each control scatter plot, n ≥ 64 for each exposed scatter plot.)

FIG. 10

Example of a histogram from an exposed unit with an adaptation function that was better described as a double exponential process. Three other exposed units showed similar behavior.