Responses Of Auditory Nerve Fibers Research Articles

Electrical stimulation of the auditory nerve: II. Effect of stimulus waveshape on single fibre response properties

To investigate the generation of action potentials by electrical stimulation we studied the response of auditory nerve fibres (ANFs) to a variety of stimulus waveforms. Current pulses were presented to longitudinal bipolar scala tympani electrodes implanted in normal and deafened cochleae. Capacitively coupled monophasic current pulses evoked single ANF responses that were more sensitive to one phase (the ‘excitatory’ phase) than the other. Anodic pulses produced a significantly shorter mean latency compared with cathodic pulses, indicating that their site for spike initiation is located more centrally along the ANF. The fine temporal structure of ANF responses to biphasic pulses appeared similar to that evoked by monophasic pulses. An excitatory monophasic pulse evoked a significantly lower threshold than a biphasic current pulse having the same polarity and duration leading phase, i.e. the addition of a second phase leads to an increase in threshold. Increasing the temporal separation of the two phases of a biphasic pulse resulted in a moderate reduction in threshold which approached that of an excitatory monophasic pulse for interphase gaps >100 μs. Greater threshold reductions were observed with narrower current pulses. There was a systematic reduction in threshold with increasing pulse width for biphasic current pulses, reflecting the general charge-dependent properties of ANFs for narrow pulse widths. Chopped biphasic current pulses, which uniformly delivered multiple packets of charge (2×30 μs, 3×20 μs or 6×10 μs) with the same polarity over a 120 μs period, followed by a similar series in the reverse polarity, demonstrated the ability of the neural membrane to integrate sub-threshold packets of charge to achieve depolarisation. Moreover, thresholds for these current pulses were ∼1.5 dB lower than 60 μs/phase biphasic current pulses with no interphase gap. Finally, stimulation using charge-balanced triphasic and asymmetric current pulses produced systematic changes in threshold and latency consistent with the charge-dependent properties of ANFs. These findings provide insight into the mechanisms underlying the generation of action potentials using electrical stimuli. Moreover, a number of these novel stimuli may have potential clinical application.

Auditory nerve fiber responses following chronic cochlear de-efferentation.

The aim of the present study was to examine the role of the olivocochlear system in auditory processing by examining the long-term effects of cochlear de-efferentation on auditory nerve response properties in adult chinchillas. Spontaneous rates, response thresholds, tuning curves, discharge rate-level functions, and adaptation of single auditory nerve fibers were measured in chinchillas with complete cochlear de-efferentation produced by sectioning the olivocochlear bundle in the internal auditory meatus. De-efferentation was verified as successful on the basis of acetylcholinesterase staining of surface preparations of the organ of Corti. Following chronic de-efferentation, there was a striking decrease in spontaneous rate, consistent with earlier observations in cats. In addition, the present study shows that complete de-efferentation results in: (1) increased driven discharge rates and decreased dynamic range of discharge rate-level functions, (2) larger onset-to-steady state ratio of discharge rate at moderate intensities, and (3) a hypersensitive tail of the tuning curve. These effects, largely confined to neurons that were most sensitive to frequencies between 2-8 kHz, indicate that the cochlear efferent system is important in maintaining normal function (e.g., frequency and intensity selectivity) of the auditory periphery by modulating auditory nerve fiber response properties.

Auditory nerve fiber responses following chronic cochlear de-efferentation

The aim of the present study was to examine the role of the olivocochlear system in auditory processing by examining the long-term effects of cochlear de-efferentation on auditory nerve response properties in adult chinchillas. Spontaneous rates, response thresholds, tuning curves, discharge rate-level functions, and adaptation of single auditory nerve fibers were measured in chinchillas with complete cochlear de-efferentation produced by sectioning the olivocochlear bundle in the internal auditory meatus. De-efferentation was verified as successful on the basis of acetylcholinesterase staining of surface preparations of the organ of Corti. Following chronic de-efferentation, there was a striking decrease in spontaneous rate, consistent with earlier observations in cats. In addition, the present study shows that complete de-efferentation results in: (1) increased driven discharge rates and decreased dynamic range of discharge rate-level functions, (2) larger onset-to-steady state ratio of discharge rate at moderate intensities, and (3) a hypersensitive tail of the tuning curve. These effects, largely confined to neurons that were most sensitive to frequencies between 2–8 kHz, indicate that the cochlear efferent system is important in maintaining normal function (e.g., frequency and intensity selectivity) of the auditory periphery by modulating auditory nerve fiber response properties. J. Comp. Neurol. 406:72–86, 1999. © 1999 Wiley-Liss, Inc.

The upper frequency range in pigeon hearing: Response properties in auditory nerve and cohlear nucleus—is tuning different in birds?

Information on responses of auditory nerve fibers in birds is generally limited to the low and mid-frequency ranges of hearing, due to anatomical constraints using the standard ganglion cell approach through the opened tympanic recess. Intracranially recorded responses of single units from the auditory nerve and the overlying cochlear nuclei in the pigeon (Columba livia) were compared to those recorded from the ganglion. Characteristic frequencies (CFs) of auditory units ranged from 0.08–5.7 kHz with intracranial compared to 0.06–1.6 kHz with intrascalar recordings. Response properties were qualitatively and quantitatively comparable in the overlapping CF ranges (0.08–1.6 kHz). Mean spontaneous firing rate decreased monotonically with CF. The CF thresholds were lowest (0–5 dB SPL) in the CF range 0.6–1.5 kHz. Mean sharpness of tuning (Q10 dB) varied nonmonotonically with CF, with a maximum near 2 kHz. In addition, Q10 dB of pigeon auditory units up to CFs of 2 kHz was much higher than that of gerbil (Meriones unguiculatus) primary fibers in the same CF range, recorded in the same setup. As it is highly improbable that mechanical tuning in birds would by far exceed that in mammals, this finding is further evidence for a difference in avian and mammalian tuning mechanisms. [Work supported by the DFG, SFB 269.]

Computer models of the auditory periphery

Enough is now known about the auditory periphery to allow the development of useful computational models. These accept an arbitrary acoustic stimulus and predict the response of auditory nerve fibers. Current models are largely based on linear filters representing the mechanical frequency selectivity of the cochlear. Nonlinear models would be more appropriate if they could be developed in a form that replicated physiological measurements. This paper describes one approach that combines a nonlinear model of frequency selectivity with a revised inner hair cell model. The nonlinear filters are evaluated using published data collected at three sites on the basilar membrane. They behave nonlinearly at frequencies close to best frequency and linearly at remote frequencies. They show appropriate impulse responses and patterns of two-tone suppression. The hair cell model incorporates a simple account of the receptor potential and retains a previously developed reservoir model of synaptic flow. An innovation includes a model of the discrete release of transmitter quanta that explicitly assumes a presynaptic origin for the stochastic nature of the auditory nerve response. The combined model gives a useful account of the differences between low-, medium-, and high-spontaneous rate fibers that is consistent with earlier physiological speculation.

Discriminability of vowel representations in cat auditory-nerve fibers after acoustic trauma.

This paper attempts to connect deficits seen in the neural representation of speech with perceptual deficits. Responses of auditory-nerve fibers were studied in cats exposed to acoustic trauma. Four synthetic steady-state vowels were used as test signals; these stimuli are identical, except that the second format (F2) resonator in the synthesizer was set to 1.4, 1.5, 1.7, or 2 kHz, producing four spectra that differ mainly in the vicinity of the F2 frequency. These stimuli were presented to a large population (523) of auditory-nerve fibers in four cats with sloping high-frequency threshold shifts that reached 50-70 dB at 2-4 kHz. In normal animals, May et al. [Auditory Neurosci 3, 135-162 (1996)] showed previously that the discharge rates of fibers with best frequencies near the F2 frequencies provide enough information to allow discrimination of these stimuli at the performance levels shown by cats in behavioral experiments. Here it is shown that, after acoustic trauma, there is essentially no rate information which would allow the vowels with different F2 frequencies to be discriminated. However, information that could allow discrimination remains in the temporal (phase-locked) aspects of the responses.

Temporal aspects of the effects of cooling on responses of single auditory nerve fibers

During an investigation of the effects of cochlear cooling on frequency tuning and input/output relations of single auditory nerve fibers in gerbil (Ohlemiller and Siegel (1994) Hear. Res. 80, 174–190), cooling-related changes in post-stimulus time histogram (PSTH) shape and phase-locking to tonebursts were characterized in a small sample of neurons. Local cochlear cooling by 5–10°C below normal core temperature did not alter overall PSTH shape, although some evidence was found for a reduction in the time constants of rapid and short term rate adaptation. The relative contributions of rapid and short term response components appeared unaltered. Effects of cooling on phase-locking were assessed by calculating the synchronization index for responses to intense (>70 dB SPL) tonebursts at 0.5, 1.0, and 2.0 kHz. Synchronization filter functions exhibited modest reductions in both magnitude and the upper frequency limit of phase-locking. The effects of cooling on the temporal character of responses appear distinct from those of a simple reduction in stimulus intensity. Results are interpreted in terms of cooling-related changes in responses of cochlear hair cells and afferent neurons, and suggest that temperature artifacts are unlikely to underlie reported species differences in PSTH shape and phase-locking.

Responses of auditory nerve fibers to trains of clicks.

Responses of auditory nerve fibers to trains of clicks were recorded in ketamine anesthetized chinchillas. By varying the number of clicks and the interclick interval, this study examined whether "post-onset adaptation," described in psychoacoustic experiments on localization, occurred in auditory nerve fibers. The results showed that the number of action potentials recorded from a nerve fiber in response to a train of clicks was a power function of the number of clicks. For interclick intervals of 2 ms or greater the exponent of the power function was 0.5, and this exponent did not change over a 20-dB range of intensities. The timing of action potentials relative to the click stimuli was measured using synchronization coefficients. The coefficients increased with interclick interval, decreased with increasing intensity, and were greater for fibers with low rates of spontaneous activity than for high spontaneous fibers. Recovery functions showed that for interclick intervals of 2 ms or more, the responses to the second click were at least 70% of the response to the initial click. The recovery depended upon the number of clicks in the train. These findings indicate that auditory nerve fibers respond to high rates of stimulus presentation and do not display the adaptation observed in localization studies.

Dissecting the frog inner ear with Gaussian noise. II. Temperature dependence of inner ear function

The temperature dependence of the response of single primary auditory nerve fibers ( n = 31) was investigated in the European edible frog, Rana esculenta (seven ears). Nerve fiber responses were analyzed with Wiener kernel analysis and polynomial correlation. The responses were described with a cascade model, consisting of a linear bandpass filter, a static nonlinearity, and a linear lowpass filter. From the computed Wiener kernels and the polynomial correlation functions, the characteristics of the three model components were obtained. With increasing temperature (1) tuning of the first filter increased in the majority ( n = 16) of amphibian papilla fibers (best excitatory frequency, BEF < 1 kHz, n = 21) but remained unchanged in the majority ( n = 10) of basilar papilla fibers (BEF > 1 kHz, n = 11), (2) the gain of the first filter remained unchanged, (3) the shape of nonlinear 10 function remained unchanged, (4) the combined gain of the static nonlinearity and the second filter usually increased, but displayed considerable scatter across fibers (from −0.7 dB/†C to 3 dB/†C), and (5) the cutoff frequency of the second lowpass filter increases, with average 0.13 oct/°C. The immunity of the shape of the nonlinearity is considered evidence of a temperature independent gating mechanism in the transduction channels. The temperature dependence of the second filter may have resulted from a decrease of the hair cell membrane resistance, but may also reflect changes in subsequent staging of nerve fiber excitation.

Cochlear mechanisms of frequency and intensity coding. I. The place code for pitch

In the past, several researchers have reported a substantial shift in the peak of the tone-evoked excitation pattern toward the base of the cochlea following an increase in the SPL of the stimulating tone. Evidence for such peak shifts has been found in the responses of auditory nerve fibers, cochlear microphonics, and the responses of outer hair cells and supporting cells in the cochlea, as well as in basilar membrane vibration measurements, and indirectly, in psychophysical data. However, direct evidence for such a peak shift in inner hair cell (IHC) responses has been relatively sparse. If the peak shift is preserved in the information conveyed to the auditory nerve fibers by the IHCs, the classical `place theory' for frequency coding in the cochlea requires modification. In this study, the nature and extent of the SPL-dependent peak shift is examined with the help of recordings in the IHCs and other cells of the organ of Corti in the 0.5–2.5 kHz region of the Mongolian gerbil cochlea. It is demonstrated that the peak shift is a universal phenomenon in the diverse cell types in this region of the cochlea. Most importantly, a large SPL-dependent peak shift is demonstrated in IHC responses. On the other hand, the recordings indicate that the apical cutoff of the spatial excitation pattern is SPL-independent. We conclude, therefore, that the place theory of pitch perception must be abandoned or at least modified.

Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria. I. Spike rate responses.

We studied the directionality of spike rate responses of auditory nerve fibers of the grassfrog, Rana temporaria, to pure tone stimuli. All auditory fibers showed spike rate directionality. The strongest directionality was seen at low frequencies (200-400 Hz), where the spike rate could change by up to nearly 200 spikes s-1, with sound direction. At higher frequencies the directional spike rate changes were mostly below 100 spikes s-1. In equivalent dB SPL terms (calculated using the fibers' rate-intensity curves) the maximum directionalities were up to 15 dB at low frequencies and below 10 dB at higher frequencies. Two types of directional patterns were observed. At frequencies below 500 Hz relatively strong responses were evoked by stimuli from the ipsilateral (+90 degrees) and contralateral (-90 degrees) directions while the weakest responses were evoked by stimuli from frontal (0 degree or +30 degrees) or posterior (-135 degrees) directions. At frequencies above 800 Hz the strongest responses were evoked by stimuli from the ipsilateral direction while gradually weaker responses were seen as the sound direction shifted towards the contralateral side. At frequencies between 500 and 800 Hz both directional patterns were seen. The directionality was highly intensity dependent. No special adaptations for localization of conspecific calls were found.

Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria . II. Spike timing

We studied the directionality of spike timing in the responses of single auditory nerve fibers of the grass frog, Rana temporaria, to tone burst stimulation. Both the latency of the first spike after stimulus onset and the preferred firing phase during the stimulus were studied. In addition, the directionality of the phase of eardrum vibrations was measured. The response latency showed systematic and statistically significant changes with sound direction at both low and high frequencies. The latency changes were correlated with response strength (spike rate) changes and were probably the result of directional changes in effective stimulus intensity. Systematic changes in the preferred firing phase were seen in all fibers that showed phaselocking (i.e., at frequencies below 500-700 Hz). The mean phase lead for stimulation from the contralateral side was approximately 140 degrees at 200 Hz and decreased to approximately 100 degrees at 700 Hz. These phaseshifts correspond to differences in spike timing of approximately 2 ms and 0.4 ms respectively. The phaseshifts were nearly independent of stimulus intensity. The phase directionality of eardrum vibrations was smaller than that of the nerve fibers. Hence, the strong directional phaseshifts shown by the nerve fibers probably reflect the directional characteristics of extratympanic pathways.

Auditory-nerve fiber responses to clicks in guinea pigs with a damaged cochlea.

This paper describes auditory-nerve single-fiber responses to clicks in noise-damaged cochleas. Poststimulus time histograms (PSTHs) were recorded for various click intensities and for the two click polarities. The PSTHs found in fibers with elevated thresholds are discussed in relation to the frequency threshold curves (FTCs) measured in these fibers. Five types of abnormal FTCs are distinguished. Type I is elevated as a whole, type II has an elevated (and often broadened) tip and a tail at normal level, type III has low thresholds in the tail (often hypersensitive), type IV represents a flat tuning, and type V has no tip but shows a clear appearance of the tail (often hypersensitive). The click PSTHs of abnormal fibers were compared to normal PSTHs at equal sound-pressure levels, and various abnormal trends were found corresponding to the type of FTC. PSTHs for type I have longer dominant-peak latencies and smaller amplitudes; PSTHs for type II were normal well above the fiber's threshold; PSTHs for type III revealed remarkable patterns with multiple peaks, part of them with a latency strongly varying with polarity; PSTHs for type IV showed narrow peaks and steep amplitude/intensity curves; PSTHs for type V showed a multiple peaked pattern and large amplitudes and steep amplitude/intensity curves to rarefaction polarity. The various features in the click responses were in most cases consistent with the type of FTC. The results can be used to explain deviations in whole-nerve recordings in abnormal cochleas.

Long-term suppression of the responses of auditory nerve fibers to a characteristic-frequency tone by a low-frequency suppressor

The classical two-tone suppression requires the characteristic-frequency (CF) tone and the suppressor (SUP) tone to act simultaneously. We report a novel phenomenon whereby the responses to the CF tone alone were ‘suppressed’ by a preceding low-side SUP tone. Increasing the repetition interval to about 3000 ms or longer eliminated such suppression. The magnitude of this ‘long-term’ suppression was not dependent upon fiber CF, but fibers with low spontaneous rates (SR) generally showed more suppression than high-SR fibers did. The suppression threshold was not dependent upon fiber SR. This suppression of the CF responses did not affect the phases of responses to either the CF or SUP tone, or the phase of suppression. This phenomenon is not due to adaptation or fatigue, but due to the presence of the preceding SUP tone. The efferent system, particularly the ‘slow’ effect, might be responsible for it.

Suppression in auditory-nerve fibers of cats using low-side suppressors. II. Effect of spontaneous rates

The responses of auditory nerve fibers with different spontaneous rates were studied in anesthetized cats, using harmonically related characteristic frequency (CF) tone and suppressor (SUP) tone (50–2000 Hz) as stimuli. The relative-response index, defined as the ratio of the maximum response level in the two-tone segment to the response level in the CF-alone segment, at or near the intensity of maximum suppression (i.e., where the two-tone rate was lowest), was dependent on fiber's spontaneous rate (SR). For all the SUP frequencies used, lower-SR fibers almost always showed values less than unity, while high-SR fibers almost always gave values near or greater than unity. The phase of maximum suppression was not dependent upon fiber SR. In one experiment, a pair of low- and high-SR fibers with the same CF (12 kHz) were recorded consecutively in the same electrode penetration, and were studied with the same stimulus parameters. Their temporal responses showed dramatic temporal resemblances, with very similar phases of suppression and response. But the relative-response indexes were different. The similarities in the lower- and high-SR fibers support the idea that the basic response and suppression patterns in all fibers are formed at or before the inner hair cell (IHC) stage, while the differences suggest that processes more central than the IHC receptor potential are important in determining the magnitudes of suppression, particularly in the lower-SR fibers.

Responses of auditory nerve fibers of the unanesthetized decerebrate cat to click pairs as simulated echoes.

1. To elucidate the peripheral contribution to "echo" processing in the auditory system, we examined the characteristics of auditory nerve responses to click-pair stimuli in unanesthetized, decerebrate cats. We used equilevel click pairs at peak levels of 45, 65, and 85 dB SPL re 20 microPa. The interclick intervals ranged from 1 to 32 ms. This study reports results from 78 auditory nerve fibers in 7 cats. The fibers were divided into 2 groups: 33 low- and 45 high-spontaneous rate (SR), with SRs less than and > or = 20 spikes/s, respectively. A method was introduced to quantify the second-click response, and its recovery was examined as a function of the interclick interval. 2. In general, auditory nerve fibers showed a gradual recovery of the second-click response as interclick interval was increased. Noticeable differences in the second-click response recovery functions emerged among fiber populations that were related to the SR. Low-SR fibers showed little change in the recovery functions of the second-click response as the click level was increased from 45 to 85 dB SPL. In contrast, high-SR fibers showed slower recoveries with increasing click level from 45 to 85 dB SPL. At 45 and 65 dB SPL, the recovery functions of the two SR groups were similar. At 85 dB SPL, high-SR fibers exhibited slower recovery than low-SR fibers, regardless of fiber characteristic frequency. The interclick intervals at 50% second-click response ranged from 1 to 6 ms (mean, 1.4 ms) among low-SR fibers. The interclick intervals at 50% second-click response for high-SR fibers, whereas similar to those for the low-SR fibers at 45 and 65 dB SPL, ranged from 2 to 16 ms (mean, 3 ms) for high-SR fibers, at 85 dB SPL. 3. We also examined auditory nerve compound action potentials (CAPs) evoked by click-pair stimuli for various interclick intervals and click levels. With increasing interclick interval, the amplitude of the second-click CAP increased, and with increasing level, the second-click CAP showed slower recovery. At 45 dB SPL, the recovery functions of the second-click CAP were similar to those of the high- and low-SR fibers. At higher levels, the CAP exhibited lower second-click response values than both high- and low-SR fiber populations for interclick intervals < 4-8 ms. At 85 dB SPL, as interclick interval increased, between 8 and 16 ms, the CAP second-click response converged with that of the high-SR fibers, and by 32 ms, the second-click response values were similar for the CAP, high- and low-SR fibers. 4. The present results are consistent with those of forward masking studies at the level of the auditory nerve in that both demonstrate a short-term reduction of the neural responses. However, the two results differ in that we observed that high-SR fibers exhibited slower recovery than low-SR fibers in response to click-pair stimuli, opposite of the trend observed in the forward masking studies of responses to pure-tone bursts. 5. The present results on auditory nerve fiber responses to click-pair stimuli provide a reference for comparison with responses of central auditory neurons to similar stimuli. This information should serve to elucidate the peripheral contribution to the processing of echoes in the auditory system.

Temporal patterns of the responses of auditory-nerve fibers to low-frequency tones

The temporal response patterns of auditory-nerve fibers to low-frequency tones were studied in anesthetized cats using period histograms. ‘Peak-splitting’ was observed mostly in fibers with lower characteristic frequencies (CF < 2 kHz) and with lower-frequency stimulation (⪯ 500 Hz). The occurrence of peak-splitting, the number of peaks, and the time between the peaks were all dependent upon the stimulus frequency. The phases of responses, although complex functions of stimulus frequency, intensity, and the fiber's CF, clearly showed traveling-wave characteristics for all frequencies at or above 100 Hz. The amount of phase change with intensity was generally small for lower-frequency stimuli ( < ∼ 50°), although larger phase changes (e.g., ∼ 180°) were occasionally seen with higher-frequency stimuli. At 50 and 100 Hz, the phase of neural responses in the basal region roughly corresponds to the maximum velocity of the basilar membrane towards scala tympani (as inferred from cochlear microphonic recordings).

Distortion Generated by the Ear: Its Emergence and Evolution During Development

Physiologically vulnerable active mechanics associated with the transduction of sounds in adults distort cochlear output. Specifically, frequencies not present in the incoming acoustic signal are represented in its output (ie., the spike trains of auditory nerve fibers). The purpose of this investigation was to study the appearance and evolution of intermodulation distortion during development. Established surgical and electrophysiologic techniques were used to record the extracellular electrical activity of individual auditory nerve fibers from developing kittens. Discharge-rate or synchrony-based responses to two tones (f1 and f2) presented simultaneously at various ratios of f2/f1 were recorded. The cubic distortion product (CDP; 2f1-f2, where f1<f2) and the difference tone (f2-f1) were the intermodulation distortion products (DPs) emphasized in the investigation. CDPs were first observed nearly 10 days after the earliest auditory nerve fiber responses to simple tone-burst stimuli could be elicited in neonatal cats. Furthermore, the spectrum of DPs generated in the cochlea changed dramatically during the second postnatal week and achieved adultlike characteristics after the first postnatal month. Findings reported here support the notion that cochlear transduction is initially linear in neonatal cats, possibly representing a critical period of auditory development, and that the content of distortion-related spectral information carried in auditory nerve fiber spike trains increases during development, in concert with other peripheral auditory attributes.

Neural representation and psychophysical discrimination of vowel formants.

Auditory-nerve fiber responses were modeled to estimate neural representations of frequency changes in the second formant (ΔF2) of the steady-state vowel /eh. Simulations were performed at vowel levels of 33–84 dB, both in quiet and in continuous noise at a constant 3-dB signal-to-noise ratio (S/N). Signal detection analysis of model outputs suggested that formant changes at higher stimulus levels and in background noise were better represented by rate responses of fibers with low spontaneous rates (SR). Psychophysical tests were then performed in cats to measure behavioral thresholds for the detection of formant frequency changes under stimulus conditions similar to those of the neural simulations. Behavioral ΔF2’s were obtained at vowel levels of 10–70 dB, in quiet and in continuous background noise at S/Ns of 3, 13, and 23 dB. ΔF2 decreased with increasing vowel level and increased with decreasing S/N. These trends in psychophysical performance paralleled changes in the quality of vowel representations, particularly those based on discharge rates of low SR auditory-nerve fibers. [Work supported by NIDCD Grant Nos. 5R01DC01388-04 and 2R01DC00109-22.]

Long-term adaptation in cat auditory-nerve fiber responses.

Driven responses of cat auditory-nerve fibers to long-duration characteristic-frequency (CF) tones could decrease substantially over time periods ranging from seconds to minutes. In extreme cases, the discharge rate could fall before the pre-stimulation spontaneous rate (SR). Reductions in response were characterized by two processes, each of which followed a decaying exponential function. long-term adaptation affects the discharge rate in the first several seconds following stimulus onset. The average amount in high-SR fibers was 42.5% for tones at 20-40 dB SL, and the mean time constant was 3.65 s. Long-term adaptation increased significantly with sensation level (SL, or level above threshold), decreased with SR, and was not significantly correlated with CF or fiber response threshold. Time constants did not depend on CF, SR, or SL. Very-long-term adaptation refers to further, smaller reductions in the discharge rate that accumulate over a period of minutes. Fiber responses formed two groups. The larger group adapted with a mean time constant of 45.22 s for CF tones at 20-40 dB SL, and the smaller group did not adapt over very long terms. Considerable variability in amounts of long-term and very-long-term effects do not arise from cochlear mechanics or middle ear muscle activity. No long-term effects were observed in responses of fibers directly stimulated by high-intensity electrical pulses present at rates up to 500/s through a cochlear implant. This suggests that the effects do not arise from fundamental differences in spike-generating properties of spiral ganglion cells. The data suggest that long-term adaptation may occur either when neurotransmitter utilization at inner hair cell synapses exceeds the rate at which it is replenished from global stores or uptake mechanisms, or which metabolic resources influencing neurotransmitter release become depleted. The neural data are related to perceptual findings in human listeners, in which unusually large amounts of tone decay may be observed at high frequencies, and they indicate that the perceptual effects originate peripherally.