Chinchilla auditory-nerve responses to low-frequency tones

Single unit activity was recorded in the auditory nerves of chinchillas. Period histograms were constructed for responses to tones with frequencies 30-1000 Hz. For low-frequency tones at near-threshold levels, peak period histogram phases for low- and medium-best-frequency (BF) neurons (less than or equal to kHz) ranged from synchronous with condensation at the eardrum to 90 degrees leading it. At near-threshold (but high absolute) levels, high-BF (greater than or equal to 8 kHz) neurons responded in phase with rarefaction. At even higher levels, period histograms for responses of high-BF neurons tended to become bimodal, with one of the modes lagging rarefaction by 90 degrees. Using cochlear microphonics as an indicator of basilar membrane (BM) displacement, at threshold levels, response phase of low- and medium-BF neurons fall within a range between displacement and velocity of the BM toward scala vestibuli. High-BF neurons respond, at threshold (but high) intensities, in phase with BM displacement toward scala tympani. The rates of growth of frequency sensitivity in responses of low-BF (+ 18 dB/oct) and high-BF (+ 12 dB/oct) neurons are consistent with preferred response phases corresponding to BM SV velocity and ST displacement, respectively. At supra-threshold levels high-BF neurons may fire preferentially to both scala tympani displacement and scala vestibuli velocity. These results support the notion that, for high-intensity, low-frequency stimuli, OHC hyperpolarization can induce excitation of the dendrites innervating IHCs.     

Conservation of adapting components in auditory-nerve responses

The responses of single auditory-nerve fibers of Mongolian gerbil were studied using tonal stimuli. The peristimulatory adaptation of firing rate in response to tone bursts presented in quiet and during a background stimulus is described quantitatively. The total transient response which can be produced to the onset of a tone burst, whether presented in quiet or as an intensity increment, is limited and appears to demonstrate a form of conservation. Specifically, the total numbers of spikes produced by the rapidly adapting component, and the slower short-term adaptation component, are proportional at all intensities, and are limited for each fiber. Furthermore, when an incremental stimulus is presented on a background, the total transient response to the background and to the increment is limited and depends upon the final intensity, not the background intensity. When the presumed underlying synaptic drive is derived by removing the effects of refractoriness from the spike train, the same conservation of the transient response components, and proportionality between rapid and short-term components, are observed.     

Frequency glides in the impulse responses of auditory-nerve fibers

Previous reports of frequency modulations, or glides, in the impulse responses of the auditory periphery have been limited to analyses of basilar-membrane measurements and responses of auditory-nerve (AN) fibers with best frequencies (BFs) greater than 1.7 kHz. These glides increased in frequency as a function of time. In this study, the instantaneous frequency as a function of time was measured for impulse responses of AN fibers in the cat with a range of BFs (250-4500 Hz). Impulse responses were estimated from responses to wideband noise using the reverse-correlation technique. The impulse responses had increasing frequency glides for fibers with BFs greater than 1500 Hz, nearly constant frequency as a function of time of BFs between 750 and 1500 Hz, and decreasing frequency glides for BFs below 750 Hz. Over the levels tested, the glides for fibers at all BFs were nearly independent of stimulus level, consistent with previous reports of impulse responses of the basilar membrane and AN fibers. Implications of the different glide directions observed for different BFs are discussed, specifically in relation to models for the auditory periphery as well as for the derivation of impulse responses for the human auditory periphery based on psychophysical measurements.     

Predictions of formant-frequency discrimination in noise based on model auditory-nerve responses

To better understand how the auditory system extracts speech signals in the presence of noise, discrimination thresholds for the second formant frequency were predicted with simulations of auditory-nerve responses. These predictions employed either average-rate information or combined rate and timing information, and either populations of model fibers tuned across a wide range of frequencies or a subset of fibers tuned to a restricted frequency range. In general, combined temporal and rate information for a small population of model fibers tuned near the formant frequency was most successful in replicating the trends reported in behavioral data for formant-frequency discrimination. To explore the nature of the temporal information that contributed to these results, predictions based on model auditory-nerve responses were compared to predictions based on the average rates of a population of cross-frequency coincidence detectors. These comparisons suggested that average response rate (count) of cross-frequency coincidence detectors did not effectively extract important temporal information from the auditory-nerve population response. Thus, the relative timing of action potentials across auditory-nerve fibers tuned to different frequencies was not the aspect of the temporal information that produced the trends in formant-frequency discrimination thresholds.     

A temporal analysis of auditory-nerve fiber responses to spoken stop consonant-vowel syllables

Auditory-nerve fiber spike trains were recorded in response to spoken English stop consonant-vowel syllables, both voiced (/b,d,g/) and unvoiced (/p,t,k/), in the initial position of syllables with the vowels /i,a,u/. Temporal properties of the neural responses and stimulus spectra are displayed in a spectrographic format. The responses were categorized in terms of the fibers' characteristic frequencies (CF) and spontaneous rates (SR). High-CF, high-SR fibers generally synchronize to formants throughout the syllables. High-CF, low/medium-SR fibers may also synchronize to formants; however, during the voicing, there may be sufficient low-frequency energy present to suppress a fiber's synchronized response to a formant near its CF. Low-CF fibers, from both SR groups, synchronize to energy associated with voicing. Several proposed acoustic correlates to perceptual features of stop consonant-vowel syllables, including the initial spectrum, formant transitions, and voice-onset time, are represented in the temporal properties of auditory-nerve fiber responses. Nonlinear suppression affects the temporal features of the responses, particularly those of low/medium-spontaneous-rate fibers.     

Nonparametric estimation of phase variance in auditory-nerve fiber's responses to tonal stimuli.

Statistical estimation of the phase variance from the auditory-nerve fiber's action potential timing data is studied in this paper. A detailed derivation of the sample-based estimation formulas, which deals specifically with the circularity of the phase variable, is given. The development of the estimator is based on nonparametric statistical inference techniques, making no assumptions on the parametric form of the phase distribution (i.e., shape of period histogram). Some desirable properties of the estimator are demonstrated through numerical examples and applications of the estimator in auditory research are discussed.     

Changes in the phase of excitor-tone responses in cat auditory-nerve fibers by suppressor tones and fatigue

The responses of single auditory-nerve fibers in anesthetized cats to two-tone stimuli were studied. One of the two tones, F1, was near, above, or below characteristic frequency (CF). The second tone, F2, was located above CF. With sufficient care, F2 was made purely suppressive, eliciting no synchrony responses by itself. The vector phases of the associated period histogram calculated for F1 were carefully studied. For 78% of the fibers under study, a statistically significant increase in phase lag was consistently observed when a suppression of rate discharge occurred. The phase-intensity curve did not approximate a horizontally shifted version of the unsuppressed curve, as is seen for the related rate- and synchrony-intensity curves; rather, the amount of phase shift at any one stimulus condition tended to be monotonically related to the amount of rate suppression generated (vertical shift). Using two different measures, a significant correlation was found between the added phase lag and the discharge-rate reduction caused by F2. The amount of phase lag, along with the corresponding rate reduction, increases with the increasing intensity of F2 within the suppression area, and decreases as F2 moves away from it. These phase-lag effects were found to be uncorrelated with a fiber's CF, with its spontaneous rate, with its threshold, or with its Q value. By contrast, a reduction of discharge rate due to adaptation was not accompanied by any significant phase shift. Fatigue of the fiber due to lengthy sound exposure was found to have strong effects on the shift of response phase to single-tone stimuli.     

Medial efferent effects on auditory-nerve responses to tail-frequency tones II: alteration of phase

It is often assumed that at frequencies in the tuning-curve tail there is a passive, constant coupling of basilar-membrane motion to inner hair cell (IHC) stereocilia. This paper shows changes in the phase of auditory-nerve-fiber (ANF) responses to tail-frequency tones and calls into question whether basilar-membrane-to-IHC coupling is constant. In cat ANFs with characteristic frequencies > or = 10 kHz, efferent effects on the phase of ANF responses to tail-frequency tones were measured. Efferent stimulation caused substantial changes in ANF phase (deltaphi) (range -80 degrees to +60 degrees, average -15 degrees, a phase lag) with the largest changes at sound levels near threshold and 3-4 octaves below characteristic frequency (CF). At these tail frequencies, efferent stimulation had much less effect on the phase of the cochlear microphonic (CM) than on ANF phase. Thus, since CM is synchronous with basilar-membrane motion for low-frequency stimuli in the cochlear base, the efferent-induced change in ANF phase is unlikely to be due entirely to a change in basilar-membrane phase. At tail frequencies, ANF phase changed with sound level (often by 90 degrees-180 degrees) and the deltaphi from a fiber was positively correlated with the slope of its phase-versus-sound-level function at the same frequency, as if deltaphi were caused by a 2-4 dB increase in sound level. This correlation suggests that the processes that produce the change in ANF phase with sound level at tail frequencies are also involved in producing deltaphi. It is hypothesized that both efferent stimulation and increases in sound level produce similar phase changes because they both produce a similar mix of cochlear vibrational modes.     

Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery

This paper presents a computational model to simulate normal and impaired auditory-nerve (AN) fiber responses in cats. The model responses match physiological data over a wider dynamic range than previous auditory models. This is achieved by providing two modes of basilar membrane excitation to the inner hair cell (IHC) rather than one. The two modes are generated by two parallel filters, component 1 (C1) and component 2 (C2), and the outputs are subsequently transduced by two separate functions. The responses are then added and passed through the IHC low-pass filter followed by the IHC-AN synapse model and discharge generator. The C1 filter is a narrow-band, chirp filter with the gain and bandwidth controlled by a nonlinear feed-forward control path. This filter is responsible for low and moderate level responses. A linear, static, and broadly tuned C2 filter followed by a nonlinear, inverted and nonrectifying C2 transduction function is critical for producing transition region and high-level effects. Consistent with Kiang's two-factor cancellation hypothesis, the interaction between the two paths produces effects such as the C1/C2 transition and peak splitting in the period histogram. The model responses are consistent with a wide range of physiological data from both normal and impaired ears for stimuli presented at levels spanning the dynamic range of hearing.     

Medial efferent effects on auditory-nerve responses to tail-frequency tones. I. Rate reduction.

One way medial efferents are thought to inhibit responses of auditory-nerve fibers (ANFs) is by reducing the gain of the cochlear amplifier thereby reducing motion of the basilar membrane. If this is the only mechanism of medial efferent inhibition, then medial efferents would not be expected to inhibit responses where the cochlear amplifier has little effect, i.e., at sound frequencies in the tails of tuning curves. Inhibition at tail frequencies was tested for by obtaining randomized rate-level functions from cat ANFs with high characteristic frequencies (CF > or = 5 kHz), stimulated with tones two or more octaves below CF. It was found that electrical stimulation of medial efferents can indeed inhibit ANF responses to tail-frequency tones. The amplitude of efferent inhibition depended on both sound level (largest near to threshold) and frequency (largest two to three octaves below CF). On average, inhibition of high-CF ANFs responding to 1 kHz tones was around 5 dB. Although an efferent reduction of basilar-membrane motion cannot be ruled out as the mechanism producing the inhibition of ANF responses to tail frequency tones, it seems more likely that efferents produce this effect by changing the micromechanics of the cochlear partition.     

Medial-olivocochlear-efferent inhibition of the first peak of auditory-nerve responses: evidence for a new motion within the cochlea

Despite the insights obtained from click responses, the effects of medial-olivocochlear (MOC) efferents on click responses from single-auditory-nerve (AN) fibers have not been reported. We recorded responses of cat single AN fibers to randomized click level series with and without electrical stimulation of MOC efferents. MOC stimulation inhibited (1) the whole response at low sound levels, (2) the decaying part of the response at all sound levels, and (3) the first peak of the response at moderate to high sound levels. The first two effects were expected from previous reports using tones and are consistent with a MOC-induced reduction of cochlear amplification. The inhibition of the AN first peak, which was strongest in the apex and middle of the cochlea, was unexpected because the first peak of the classic basilar-membrane (BM) traveling wave receives little or no amplification. In the cochlear base, the click data were ambiguous, but tone data showed particularly short group delays in the tail-frequency region that is strongly inhibited by MOC efferents. Overall, the data support the hypothesis that there is a motion that bends inner-hair-cell stereocilia and can be inhibited by MOC efferents, a motion that is present through most, or all, of the cochlea and for which there is no counterpart in the classic BM traveling wave.     

Responses of auditory-nerve fibers to multiple-tone complexes

To relate level-dependent properties of auditory-nerve-fiber responses to nasal consonant-vowels to the basic frequency selective and suppressive properties of the fibers, multitone complexes, with the amplitude of a single (probe) component incremented, were used as stimuli. Quantitative relations were obtained between the systematic increase of fiber synchrony to the probe tone and the decrease of synchrony to CF, as the amplitude of the probe tone was increased. When such relations are interpreted as a measure of fiber frequency selectivity based on a relative synchrony criterion, a breadth of frequency tuning is obtained, at a 70-dB SPL multitone sound-pressure level, which is generally broader than that of the fiber's threshold tuning curve. Quantitative comparisons with the same fiber's responses to the nasal speech sounds indicate that the fiber's speech responses share some common features with its probe-tone responses.     

The responses of models of "high-spontaneous" auditory-nerve fibers in a damaged cochlea to speech syllables in noise

The responses of four high-spontaneous fibers from a damaged cat cochlea responding to naturally uttered consonant-vowel (CV) syllables [m], [p], and [t], each with [a], [i], and [u] in four different levels of noise were simulated using a two-stage computer model. At the lowest noise level [+30 dB signal-to-noise (S/N) ratio], the responses of the models of the three fibers from a heavily damaged portion of the cochlea [characteristic frequencies (CFs) from 1.6 to 2.14 kHz] showed quite different response patterns from those of fibers in normal cochleas: There was little response to the noise alone, the consonant portions of the syllables evoked small-amplitude wide-bandwidth complexes, and the vowel-segment response synchrony was often masked by low-frequency components, especially the first formant. At the next level of noise (S/N = 20 dB), spectral information regarding the murmur segments of the [m] syllables was essentially lost. At the highest noise levels used (S/N = +10 and 0 dB), the noise was almost totally disruptive of coding of the spectral peaks of the consonant portions of the stop CVs. Possible implications of the results with regard to the understanding of speech by hearing-impaired listeners are discussed.     

Responses of auditory-nerve fibers to nasal consonant-vowel syllables

Responses of single auditory-nerve fibers in anesthetized cat to spoken nasal consonant-vowel syllables were recorded. Analyses in the form of spectrograms and of three-dimensional spatial-time and spatial-frequency plots were made. Among other features, formant transitions are clearly represented in the fibers' response synchronization properties. During vocalic segments, especially those in /mu/and/ma/, at a stimulus level near 75 dB SPL, a strong dominance in the responses by frequencies near the second formant (F2) is found for most fibers whose characteristic frequencies (CFs) are at or above F2. In contrast, at more moderate levels, the same fibers may show response synchrony to frequencies closer to their own CFs. There are significant differences in the response properties of high and low/medium-spontaneous-rate fibers.     

Physiological responses to the pulsation threshold paradigm. II: Representations of high-pass noise in average rate measures of auditory-nerve fiber discharge

In a companion article [L. I. Hellstrom, J. Acoust. Soc. Am. 85, 230-242 (1989)], it was shown that psychophysical pulsation threshold masking patterns (PTPs) for high-pass noise maskers are not a simple transformation of the profile of activity evoked in the auditory nerve by the masker. In this article, PTPs are compared with neural representations in which interactions of masker and probe are considered. It is hypothesized that, at pulsation threshold, some criterion value of rate change occurs when the stimulus switches from masker to probe. The iso-rate probe level, defined for single auditory-nerve fibers, is the probe level at which this rate change is zero. Iso-rate probe levels are lowest when probe frequency equals best frequency (BF) of the fiber. Profiles of iso-rate probe level versus BF (equal to probe frequency) are qualitatively similar to PTPs but differ quantitatively, e.g., in the rate of growth of probe level with masker level (1.2 dB/dB for PTPs, 0.54 dB/dB for iso-rate profiles). Quantitative differences can be further reduced by requiring a positive rate criterion. These results suggest that PTPs are not solely a reflection of the internal representation of the masker, but reflect responses to the probe tone as well.     

Noise susceptibility and immunity of phase locking in amphibian auditory-nerve fibers

Recordings from auditory-nerve fibers in the anesthetized frog revealed that addition of broadband noise results in a reduction in the ability of a fiber to phase lock to a continuous pure tone. In particular, our results suggest that: (i) there is a threshold below which masking noise has little or no effect on vector strength (VS); then with increasing masking noise level, VS appears to decrease monotonically for all test frequencies (TFs); (ii) there exist subpopulations of auditory-nerve fibers in the frog for which the deterioration of phase locking to tones in wideband noise depends critically on the relationship of the TF to the fiber's CF. Specifically, in one subpopulation (43% of the fibers studied), the rate of VS decrease with increasing levels of masking noise is greater for CF tones than it is for TFs greater than CF. The net result is a "crossing" of the VS versus masking noise functions (e.g., Fig. 6); (iii) there exists a small subpopulation of amphibian papillar (a.p.) fibers for which the rate of VS decrease with increasing levels of masking noise is less for TFs less than CF than it is for CF tones (e.g., Fig. 5); (iv) there is a pronounced noise-induced phase lead for TFs greater than CF, whereas, for stimulus tones at or below CF, the preferred firing phase is nearly noise-level independent; (v) the remainder of the sample consists of fibers in which the VS-falloff rates appear to be test-frequency independent; (vi) addition of wideband masking noise to a CF tone, and increasing the CF-tone level in the absence of noise, produced (qualitatively) similar effects on the preferred firing phase of auditory-nerve fibers (e.g., Figs. 1 and 7). Thus amphibian auditory-nerve fibers appear to be energy detectors, i.e., exhibit phase shifts corresponding to the total energy within the filter passband defined by the frequency-threshold curve.     

Effects of stimulus frequency on adaptation in auditory-nerve fibers.

Several experimental methods of depressing the response of auditory-nerve fibers to tonal stimuli have been shown to reduce the response to signal frequencies at or near fiber CF (characteristic frequency) more than to frequencies greater or less than CF. In this study we have used a short adapting tone presented before each test-tone burst to reduce the fiber's response to the test tone. We observed the effects of changing test frequency when the adapting frequency was held constant at fiber CF. The depression in discharge rate was found to be approximately constant across test frequency.     

Algorithms for removing recovery-related distortion from auditory-nerve discharge patterns

The probability that a cochlear nerve fiber discharges during some specified time interval depends on both the acoustic stimulus and on refractory effects due to earlier spike discharges. With the objective of separating the stimulus-related effects from refractory-related effects seen in poststimulus-time histograms, various maximum-likelihood estimation schemes have been developed. By modeling auditory-nerve fiber discharges as a self-exciting point process in which the intensity depends on both the time during stimulation and the history of discharge, we have been able to independently verify the likelihood estimates of Gaumond et al. [J. Acoust. Soc. Am. 74, 1392-1398 (1983)] under conditions when the recovery function is known. Secondly by maximizing the likelihood function of the neural event process subject to periodic stimulus constraints we have derived estimates which as the number of stimulus presentations and or stimulus periods increase are free from the effects of both absolute and relative recovery-related distortion. Under conditions when the recovery function is unknown, a recursive algorithm is proposed that yields the joint maximum-likelihood estimates of both the stimulus-and recovery-related components in the response histograms. We state the conditions under which unique maximum-likelihood estimates exist and prove that the recursive algorithm converges to those unique estimates.