Effects of excitatory and non-excitatory suppressor tones on two-tone rate suppression in auditory nerve fibers

Recordings were obtained from individual auditory nerve fibers in anesthetized chinchillas. Rate versus level functions were obtained for best frequency (BF) tones alone and for simultaneously-gated tone pairs comprising a BF tone and a second tone at a fixed intensity that produced evidence of two-tone rate suppression. Care was taken in selecting a range of suppressor tone levels that included excitatory (i.e., the suppressor tone evoked a rate change by itself) and non-excitatory (i.e., no suppressor tone-evoked rate increase) suppressor tone levels. Addition of a suppressor tone produced a shift of the dynamic range portion of the BF rate versus level function to higher test intensities. A parallel shift of the dynamic range portion of the rate versus level function was associated with a non-excitatory suppressor tone. The shift produced by an excitatory suppressor tone was characterized by a decrease in slope. Results indicated that the magnitude of shift increased monotonically as suppressor tone intensity was raised and that there was a gradual transition from a non-excitatory response to an excitatory response. The rate of shift (i.e., dB of shift per dB change in suppressor tone intensity) did not differ for non-excitatory versus excitatory responses, but was substantially greater for below-BF suppressor tones (1.38 dB/dB) than for above-BF suppressor tones (0.54 dB/dB). The rate of shift did not, however, appear to be related systematically to suppressor tone frequency separation from BF. Above- and below-BF suppression was noted for fibers over the range of best frequencies tested (110 Hz to 16.4 kHz).     

Relations between frequency selectivity and two-tone rate suppression in lizard cochlear-nerve fibers

Cochlear-nerve fibers innervating the apicial region of the alligator lizard basilar papilla show sharp frequency selectivity in response to single tones (measured with the frequency threshold contour, or FTC), and the phenomenon of two-tone rate suppression (TTRS) in response to two simultaneously presented tones (measured with the iso-TTRS contour, or ITC). The gross shapes of the FTCs, as characterized by the slopes of the sides and Q_10dB, vary systematically with the fiber's characteristic frequency (CF). ‘Fine-structural’ features are also found: below CF, notches (frequency regions of relatively high threshold) occur in the FTC at frequencies related to CF. Above CF, a break frequency, which varies with CF, divides the FTC into segments of different slope. Features of the ITC also vary with CF. The detailed shapes of the FTCs and ITCs are related: lobes of the ITC interdigitate with notches in the FTC; the side of the FTC with steepest slope is closely associated with the side of the ITC with steepest slope. The close relation that is observed between sharp frequency selectivity and TTRS suggests that both phenomena arise from a common cochlear mechanism.     

Two-tone suppression in cochlear hair cells

The phenomenon of two-tone suppression that is known to occur at the level of the auditory nerve is shown to also occur in the receptor potential of single presumed inner hair cells in the first turn of the guinea pig cochlea.     

Rate/level functions of auditory-nerve fibers in young and quiet-aged gerbils

Steady-state rate/level functions of single auditory-nerve fibers to characteristic frequency (CF) tone bursts were measured in quiet-aged (35-37 months) and young control (4-7 months) gerbils. Rate/level functions of aged gerbils are different from those of young controls in that the thresholds are shifted to higher sound levels, but otherwise the shapes of the aged and young rate/level functions are similar. Specifically, there is little difference in the slope of the dynamic range portion of the rate/level functions when comparing aged gerbils to young controls. This is in contrast to whole-nerve input/output (I/O) functions of aged gerbils, which exhibit slopes that are less steep than those of the young controls (Hellstrom and Schmiedt, 1990b). Thus, it is likely that the deterioration of the CAP I/O function in aged animals is not due to a deterioration of rate/level functions in single units, but rather to other factors such as spiral ganglion cell degeneration or a loss of synchrony.     

Two-tone suppression in inner hair cell responses

In an attempt to characterize certain aspects of two-tone suppression (2TS), ac receptor potentials were recorded from mammalian inner hair cells (IHC) in the third turn of the guinea pig cochlea. By comparing magnitude and phase changes occurring during suppression with predictions made on the basis of level-dependent responses to single-tone inputs, it is possible to determine whether 2TS is mimicked by simply attenuating stimulus intensity.

Results indicate that the effects of suppression are not simulated by simple input attenuation for low probe levels which produce responses below saturation. In these situations, the suppressor causes a decrease in the magnitude of the ac receptor potential with the largest deviations measured at the characteristic frequency (CF) of the cell. Thus, frequency response functions become broader. Response phase goes through a lag/lead transition at CF, also opposite to the results expected by simply decreasing input to the cell.

At higher probe levels, within the saturation region, the magnitude reductions produced during 2TS are largest for stimulus frequencies well below and well above CF. This effect partially reverses the broadening of frequency response functions seen at moderate intensities with possible benefits for the processing of complex stimuli at conversational levels. Although the magnitude data obtained at high probe levels are consistent with the attenuation hypothesis, the companion phase measures did not show the expected lead/lag transition through CF since phase changes were generally lags. Consequently, the high-level suppression data suggest that 2TS may reduce input to the IHC but in a way which is not equivalent to the attenuation of a single-input stimulus.     

Two-tone suppression, excitation and the after effect in rate responses in auditory nerve fibres in the cat.

Responses were recorded from single, auditory nerve fibres in the anaesthetized cat. Acoustic stimuli consisted of two tones, one of which was at characteristic frequency (CF), the other (the suppressor) was at considerably lower frequency. Tones were presented in simultaneous and sequential configurations. For simultaneous presentations, well-known response properties were observed. The rising limb of the two-tone rate-intensity function closely matched that of the appropriately adapted response to the suppressor tone presented alone. Also, whether strongly suppressed relative to CF-driven rate, or equal to CF-driven rate, rate responses to the two-tone stimuli persisted unchanged when the CF tone was terminated and the suppressor tone continued alone. These results support the hypothesis that the suppressor tone has dual influences, suppressive and excitatory, that are distinct and additive. Peristimulus response histograms confirm in the cat that depression and slow recovery of sensitivity to CF may follow termination of the suppressor tone, as reported for the guinea pig [Hill, K.G. and Palmer, A.R. (1991) Hear. Res. 55, 167-176]. This delay in recovery of normal sensitivity to CF appeared to be directly related to the amount of excitation of the fibre that is attributable to the suppressor tone. A similar, delayed re-establishment of sensitivity also occurred in the response to a tone at CF, presented immediately following excitation by a suppressor tone. However, no delay occurred in the onset of response to the suppressor when preceded by the CF tone.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. II. Spontaneous rate

In order to increase our understanding of cochlear mechanisms, we measured changes in the rate of spontaneous firing (SR) of single auditory-nerve fibers in response to the stimulation of medial olivocochlear efferents in cats. During the first second of efferent stimulation, SR was depressed by up to 35%, except in one very sensitive animal in which depressions up to 80% were found. With data from this aberrant cat excluded, the SR depression, on the average, increased as auditory-nerve fiber sensitivity increased, increased as the original SR decreased (data were not obtained for SRs less than two spikes/sec), and had a broad maximum at CFs of about 10 kHz. After the efferent stimulation was turned off, there was an "overshoot" in which the SR increased past the original rate in some fibers. The "overshoot" was larger for fibers with lower SRs and for fibers which showed larger "adaptation" in the efferent-induced depression of SR. The data on SR depression during efferent stimulation are consistent with two hypotheses: (1) that the stronger than usual efferent suppression of "spontaneous" rate found in some very sensitive fibers occurs because the "spontaneous" firing was, in part, a response to sound, and (2) that "true spontaneous" firing is reduced by the efferent-induced hyperpolarization of outer hair cells (OHCs) being electrically coupled through the endocochlear potential to inner hair cells (IHCs). It is suggested that (1) the efferent-induced suppression of "true spontaneous" activity is largest at CFs near 10 kHz because this CF region receives the greatest OHC innervation from medial efferents and the efferent-induced change in OHCs is electrically coupled to IHCs, whereas (2) the efferent suppression of responses to sound is largest at lower CFs because the efferent endings on OHCs act to decrease the motion of the basilar membrane and this change is propagated apically from the active efferent synapses on OHCs.     

Representation of voice pitch in discharge patterns of auditory-nerve fibers

Responses of populations of auditory-nerve fibers were measured for synthesized consonant-vowel stimuli. This paper explores the encoding of fundamental frequency (pitch) in these responses. Post-stimulus time (PST) histograms were computed from 25 ms segments of the spike trains. Discrete Fourier transforms with a 40 Hz resolution were computed from the histograms. Two representations of pitch are considered. The first representation is based on the pitch-related temporal properties of the speech signal. Histograms for individual units can show envelope modulations directly related to the pitch period. These modulations reflect the responses of these fibers to a number of stimulus harmonics near fiber CF. Responses of fibers near formant frequencies are dominated by a single large harmonic component, and thus show small or no pitch-related enveloped modulations. Envelope modulations are reduced in the presence of background noise. The second representation uses both temporal properties of auditory-nerve responses and cochlear place to encode the pitch-related harmonic structure of speech. As a measure of the response of the population of fibers to each harmonic of 40 Hz the magnitude of the component of the Fourier transform at that frequency was averaged across all fibers whose characteristic frequencies were within one-fourth octave of that harmonic. We call this measure the average localized synchronized rate (ALSR). The ALSR provides a good representation of stimulus spectrum, even in the presence of background noise. From the harmonic structure of the ALSR, we are able to extract the stimulus pitch frequency. The relationship of these two representations to pitch perception in both acoustic and electrical stimulation (via cochlear implants) is discussed.     

Representation of whispered vowels in discharge patterns of auditory-nerve fibers

We have previously shown that the spectra of speech sounds can be represented in the temporal patterns of discharge of populations of auditory-nerve fibers. These results were obtained using perfectly periodic stimuli, for which a temporal representation is straightforward. In order to see if our results could be generalized to nonperiodic stimuli, we have studied responses to a whispered vowel with formant frequencies typical of /ε/. The whispered vowel was generated by exciting a vocal tract model with noise; this signal was therefore aperiodic. Temporal patterns of responses to the vowel in populations of auditory-nerve fibers were analyzed using interval histograms. Fourier transforms of these histograms show large components at frequencies near the formant frequencies of the vowel. With these Fourier transform components as a measure of the temporal response, a temporal-place representation of the response of populations of fibers preserves the spectral features of the aperiodic vowel stimulus. Profiles of average rate versus characteristic frequency for fibers with spontaneous rates greater than $\text{1}\text{s}$ show little if any formant-related structure. On the other hand, such profiles for fibers with spontaneous rates less than $\text{1}\text{s}$ may show peaks in the region of the formants.     

Characterizing the dependence of pure-tone frequency difference limens on frequency, duration, and level

The purpose of this study was to reveal synaptic plasticity within the dorsal cochlear nucleus (DCN) as a result of noise trauma and to determine whether effective antioxidant protection to the cochlea can also impact plasticity changes in the DCN. Expression of synapse activity markers (synaptophysin and precerebellin) and ultrastructure of synapses were examined in the DCN of chinchilla 10 days after a 105 dB SPL octave-band noise (centered at 4 kHz, 6 h) exposure. One group of chinchilla was treated with a combination of antioxidants (4-hydroxy phenyl N-tert-butylnitrone, N-acetyl-l-cysteine and acetyl-l-carnitine) beginning 4 h after noise exposure. Down-regulated synaptophysin and precerebellin expression, as well as selective degeneration of nerve terminals surrounding cartwheel cells and their primary dendrites were found in the fusiform soma layer in the middle region of the DCN of the noise exposure group. Antioxidant treatment significantly reduced synaptic plasticity changes surrounding cartwheel cells. Results of this study provide further evidence of acoustic trauma-induced neural plasticity in the DCN and suggest that loss of input to cartwheel cells may be an important factor contributing to the emergence of hyperactivity in the DCN after noise exposure. Results further suggest that early antioxidant treatment for acoustic trauma not only rescues cochlear hair cells, but also has impact on central auditory structures.     

Rapid adaptation of auditory-nerve fibers: fine structure at high stimulus intensities

Simple phenomenological models of rapid adaptation do not account for details in the response of auditory-nerve fibers to the onset of high-intensity sound stimulus. Simple refractory effects, in combination with higher-order discharge-history effects appear necessary to fully account for the oscillations and plateaus observed in post-stimulus time histograms.     

Furosemide selectively reduces one component in rate-level functions from auditory-nerve fibers

Furosemide, an ototoxic diuretic, was administered intravenously while rate- and phase-level functions of auditory nerve fibers were measured in the cat. Normal level functions can demonstrate two components distinguished by an abrupt shift in the phase of the response as the sound level is increased. Furosemide, administered at doses that decrease the endocochlear potential, selectively reduces the discharge rate in response to tones at sound levels below that of the abrupt phase shift.     

Response modulation of auditory-nerve fibers by am stimuli: effects of average intensity

Auditory-nerve responses were obtained for characteristic frequency tones which were amplitude modulated by sinusoids. Response modulation (RM) was determined from folded histograms which were synchronized to the modulating wave form. As the average intensity increased from threshold, RM increased to a maximum and then decreased, and the shape of the RM function resembled that described previously for incremental responses. However, unlike the latter, the RM function could not he predicted directly from the steady-state rate-intensity function. In general, the maximum RM occurred at a higher intensity than predicted, and RM occurred over a wider range of average intensities than predicted. The results are interpreted as reflecting a dynamic response characteristic with an operating range that exceeds that determined from the steady-state rate-intensity function.     

Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data

Characteristics of 245 auditory nerve fibers in eleven Mongolian gerbils are described in terms of spontaneous rates, thresholds, and tuning curves. The animals were reared in a low-noise environment and had similar hearing thresholds across frequency. Tuning curves were obtained with an algorithm developed to characterize the tuning of auditory fibers in cat, thereby allowing direct comparisons to published data from cat. The results demonstrate that basic similarities exist between gerbil and cat data, although some minor differences are also apparent. Tuning curve bandwidths, as measured 10 and 40 dB above the thresholds at the characteristic frequency (CF), follow trends found in cat data. Like cat, auditory nerve fibers in the gerbil have a range of spontaneous rates. In individual gerbils, fibers associated with low spontaneous rates have higher thresholds than do fibers of similar CF with high rates. Five of the eleven gerbils showed profiles of spontaneous rate across frequency reminiscent of those obtained from quiet-raised young cats. The profiles of the remaining gerbils tended to be compressed to a smaller range of spontaneous rates for characteristic frequencies above about five kHz, much like older cats with unknown noise histories. The cause of the spontaneous compression is not obvious. The correspondence between cat and gerbil with regard to spontaneous rate and CF threshold implies the presence of fundamental mechanisms that are common to mammalian auditory systems.     

Towards a unifying basis of auditory thresholds: distributions of the first-spike latencies of auditory-nerve fibers

Detecting sounds in quiet is the simplest task performed by the auditory system, but the neural mechanisms underlying perceptual detection thresholds for sounds in quiet are still not understood. Heil and Neubauer [Heil, P., Neubauer, H., 2003. A unifying basis of auditory thresholds based on temporal summation. Proc. Natl. Acad. Sci. USA 100, 6151-6156] have provided evidence for a simple probabilistic model according to which the stimulus, at any point in time, has a certain probability of exceeding threshold and being detected. Consequently, as stimulus duration increases, the cumulative probability of detection events increases, performance improves, and threshold amplitude decreases. The origin of these processes was traced to the first synapse in the auditory system, between the inner hair cell and the afferent auditory-nerve fiber (ANF). Here we provide further support for this probabilistic "continuous-look" model. It is derived from analyses of the distributions of the latencies of the first spikes of cat ANFs with very low spontaneous discharge rates to tones of different amplitudes. The first spikes in these fibers can be considered detection events. We show that, as predicted, the distributions can be explained by the joint probability of the occurrence of three independent sub-events, where the probability of each of those occurring is proportional to the low-pass filtered stimulus amplitude. The "temporal integration" functions of individual ANFs, derived from their first-spike latencies, are remarkably similar in shape to "temporal integration" functions, which relate threshold sound pressure level at the perceptual level to stimulus duration. This further supports a close link between the mechanisms determining the timing of the first (and other) evoked spikes at the level of the auditory nerve and detection thresholds at the perceptual level. The possible origin and some functional consequences of the expansive power-law non-linearity are discussed.     

Quantifying 2-factor phase relations in non-linear responses from low characteristic-frequency auditory-nerve fibers

Auditory-nerve excitation by two response factors that can be in antiphase has been hypothesized by Kiang (1990) on the basis of non-linear interference in responses to tones (Kiang et al., 1969). The general conditions for antiphasic responses and the relevance of the hypothesis for other auditory stimuli are unknown. Clarification was sought in a systematic modeling study of published data on level-dependent non-linear responses from low characteristics-frequency (CF) auditory-nerve fibers for a broad variety of acoustic stimuli. The MBPNL non-linear I/O model of cochlear frequency analysis (Goldstein, 1990), which incorporates the 2-factor hypothesis, was used to stimulate the reported non-linear phenomena. It was found that experiments with paired click stimuli (Goblick and Pfeiffer, 1969) and with octave-band complex tones (Horst et al., 1990), in addition to experiments with single clicks or tones, are sensitive to the phase difference between factors. Surprisingly, the paired-click transient responses require a quadrature phase, while the complex-tone steady-state responsesrequire an antiphase relation. The MBPNL model simulations of all low-CF data surveyed, for simple and complex stimuli, are consistent with a quadrature phase for transient responses and antiphase relation for steady-state responses. It is hypothesized that some adaptive, low-CF, cochlear mechanism, not described by the basic MBPNL model, produces a temporal transition of the ‘2-factor’ response from an initial quadrature relation (tip leading) to a final antiphase relation. New experimental and modeling research guided by this working hypothesis is proposed.     

Rippled-spectrum resolution dependence on level

Rippled-density resolution of a rippled sound spectrum (probe band) in both the presence and absence of another band (masker) was studied as a function of sound level in normal listeners. The resolvable ripple density in the probe band was measured by finding the highest ripple density at which an interchange of ripple peak and valley positions was detectable (the phase-reversal test). Probe bands were 0.5 oct wide with center frequencies of 1, 2, and 4 kHz. In the control condition (no masker), the ripple-density resolution was almost independent of sound level within a range of 40-90 dB SPL. When an on-frequency masker coincided with the probe band (that resulted in reduced ripple depth), resolution decreased slightly relative to the control condition but remained little dependent on level. With an off-frequency low-side masker, the ripple-density resolution was a little less than in the control but almost independent of level within a range of 40-60 dB SPL and progressively decreased with level increase from 70 to 90 dB SPL. The dependence on level was qualitatively similar at all probe frequencies and at various widths and positions of the low-side off-frequency masker band.     

Evidence for expansive power functions in the generation of the discharges of 'low- and medium-spontaneous' auditory-nerve fibers

Re-analysis of data from Geisler et al. [J. Acoust. Soc. Am. 77, 1102-1109, 1985] indicates that the slopes of the intensity versus discharge-rate curves of auditory nerve (AN) fibers decrease systematically with increasing spontaneous discharge rate. For 'high-spontaneous' fibers, the slope is usually less than 0.5 dB/dB, while for 'low-spontaneous' fibers the slopes reach values greater than 4.0 dB/dB. A two-stage model accounts for this behavior. The first stage is a static non-linearity based on the measured intensity-voltage characteristic of inner hair cells. The second stage, representing action-potential generation, is linear for high-spontaneous fibers, but a squaring function for low- and medium-spontaneous fibers. The output of the model displays realistic slopes for its various intensity-rate curves. There are suggestions that a nonlinearity of still higher power is needed to simulate accurately the behavior of AN fibers having the lowest spontaneous rates (less than 0.1/s). The model also accounts for other observed differences between the discharge patterns of the different fiber classes.     

Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions

In previous studies describing the effects of electrically stimulating the olivocochlear bundle, it seems possible that both medial and lateral (MOC and LOC) efferents may have been stimulated. To selectively stimulate MOC efferents, we used an electrode placed at the origin of the MOC efferents in the brainstem (MOC stimulation). For comparison, a stimulating electrode was placed in the fourth ventricle at the decussation of the crossed olivocochlear bundle where both MOC and LOC efferents are present (midline-OCB stimulation). Rate versus sound level functions from auditory-nerve fibers were obtained with and without efferent stimulation. Stimulation at either location shifted rate vs. level functions to higher sound levels and depressed the rate in the plateau. For fibers with high spontaneous rates, the level shifts and plateau depressions had slightly different distributions as a function of characteristic frequency. The average amplitudes of these effects were largest for midline-OCB stimulation, next largest for crossed MOC stimulation and smallest for uncrossed MOC stimulation. The qualitative pattern of the effects, however, did not depend on the location of the stimulus electrode. The amplitudes of the efferent-induced effects were different for auditory-nerve fibers with different spontaneous rates (by as much as a factor of three for the plateau depression). The results support several hypotheses: (1) the effects of midline-OCB stimulation are due only to the action of MOC efferents, (2) individual crossed and uncrossed MOC fibers produce similar effects, and (3) efferents differentially change the information carrying properties of auditory-nerve fibers in different spontaneous-rate categories. These results, taken together with anatomical data in the literature, are consistent with the hypothesis that, in the cat, MOC and midline-OCB stimulation have their effect solely through synapses on outer hair cells. The data are consistent with the hypothesis that the level shifts are produced by MOC efferents acting on outer hair cells to reduce the mechanical stimulus to inner hair cells. It seems likely that some other mechanism is required to produce the plateau depressions, at least for auditory-nerve fibers with high spontaneous rates.