Responses of "high-spontaneous" auditory-nerve fibers to consonant-vowel syllables in noise

Responses of "high-spontaneous" single auditory-nerve fibers in anesthetized cat to nine different spoken stop and nasal consonant-vowel syllables presented in four different levels of speech-shaped noise are reported. The temporal information contained in the responses was analyzed using "composite" spectrograms and pseudo-3D spatial-frequency plots. Spectral characteristics of both consonant and vowel segments of the CV syllables were strongly encoded at S/N ratios of 30 and 20 dB. At S/N = 10 dB, formant information during the vowel segments was all that was reliably detectable in most cases. Even at S/N = 0 dB, most vowel formants were detectable, but only with relatively long analysis windows (40 ms). The increases (and decreases) in discharge rate during various phases of the responses were also determined. The rate responses to the "release" and to the voicing of the stop-consonant syllables were quite robust, being detectable at least half of the time, even at the highest noise level. Comparisons with psychoacoustic studies using similar stimuli are made.     

Responses of "lower-spontaneous-rate" auditory-nerve fibers to speech syllables presented in noise. II: Glottal-pulse periodicities.

The responses of single cat auditory-nerve fibers to naturally spoken voiced sounds (the vowels [a, i, u] and the murmur [m]) presented at normal intensity (70 dB SPL) in various levels of speech-shaped noise were analyzed for the encoding of the glottal-pulse (fundamental) period. To quantify the strength of this fundamental-period encoding, selected segments of the response histograms were autocorrelated, rectified, and fitted with the best-fitting sinusoid of the fundamental frequency. The magnitude of this best-fitting sinusoid was taken as the magnitude of synchronization. In most cases, it was found that the "lower-SR" fibers (those with spontaneous discharge rates less than 20/s) encoded the fundamental periodicity more strongly and more robustly than did the "high-SR" fibers (those with spontaneous discharge rates greater than 20/s). When either a single strong spectral peak or a relatively "flat" spectrum excited a fiber, it showed poor synchronization to the fundamental period, regardless of its spontaneous-rate class. Judging from a few examples, the glottal-pulse synchronization appears to be intensity dependent, with the relative performance of the high-SR fibers improving at lower intensities. A conceptual model is given which accounts for the general characteristics of the data.     

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.     

Coding of spectral fine structure in the auditory nerve. I. Fourier analysis of period and interspike interval histograms

The temporal fine structure of discharge patterns of single auditory-nerve fibers in adult cats was analyzed in response to signals consisting of a variable number of equal-intensity, in-phase harmonics of a common low-frequency fundamental. Two analytic methods were employed. The first method considered Fourier spectra of period histograms based on the period of the fundamental, and the second method considered Fourier spectra of interspike interval histograms (ISIH's). Both analyses provide information about fiber tuning properties, but Fourier spectra of ISIH's also allow estimates to be made of the degree of resolution of individual stimulus components. At low intensities (within 20-40 dB of threshold), indices of synchronization to individual components of complex tones were similar to those obtained for pure tones. This was true even when fibers were capable of responding to several signal components simultaneously. Response spectra obtained at low intensities resembled fibers' tuning curves, and fibers with low spontaneous discharge rates tended to provide better resolution of stimulus components than fibers with high spontaneous rates. Strongly nonlinear behavior existed at higher stimulus intensities. In this, information was transmitted about progressively fewer signal components and about frequencies not present in the acoustic stimulus, and the component eliciting the largest response shifted away from the fiber's characteristic frequency and toward the edges of the stimulus spectrum. This high-intensity "edge enhancement" can result from the combined effects of a compressive input-output nonlinearity, suppression, and the fortuitous addition of internally generated combination tones. The data indicate that sufficient information exists for the auditory system to determine the frequencies of narrowly spaced stimulus components from the temporal fine structure of nerve fiber's responses.     

Strategies for the representation of a tone in background noise in the temporal aspects of the discharge patterns of auditory-nerve fibers

The responses of populations of auditory-nerve fibers to both a 1.0-kHz tone, and 1.0-kHz tone in broadband noise, have been measured. Period histograms were generated from fiber spike trains and discrete Fourier transforms (DFTs) with a resolution of 125 Hz were computed from each histogram. Sample mean and sample variance statistics were generated for period histograms of response and for temporal response measures derived from discrete Fourier transforms. It is demonstrated how the statistical properties of auditory-nerve fiber response determine the strategy for the estimation and discrimination of particular stimulus components. When the tone is presented alone, the entire population of auditory-nerve fibers provides statistically reliable estimates of the 1.0-kHz tone. Upon addition of the broadband noise stimulus only those units with characteristic frequencies which are close in frequency to the 1.0-kHz stimulus provide spectral estimates which have high signal-to-noise ratios (mean-squared-to-variance ratios). Estimates of the 1.0-kHz-tone stimulus derived from auditory-nerve fibers with characteristic frequencies which are far from the 1.0-kHz stimulus are statistically unreliable. Based on the responses of the population of auditory-nerve fibers, the strategy for estimating the 1.0-kHz-tone stimulus is to derive estimates of the 1.0-kHz stimulus from the subpopulation of neurons with characteristic frequencies close to the 1.0-kHz stimulus. It is concluded that neurons which are tuned close to 1.0-kHz provide the central nervous system (CNS) with the most salient information about the 1.0-kHz stimulus in the presence of the broadband background.     

Speech coding in the auditory nerve: V. Vowels in background noise

Responses of auditory-nerve fibers to steady-state, two-formant vowels in low-pass background noise (S/N = 10 dB) were obtained in anesthetized cats. For fibers over a wide range of characteristic frequencies (CFs), the peaks in discharge rate at the onset of the vowel stimuli were nearly eliminated in the presence of noise. In contrast, strong effects of noise on fine time patterns of discharge were limited to CF regions that are far from the formant frequencies. One effect is a reduction in the amplitude of the response component at the fundamental frequency in the high-CF regions and for CFs between F1 and F2 when the formants are widely separated. A reduction in the amplitude of the response components at the formant frequencies, with concomitant increase in components near CF or low-frequency components occurs in CF regions where the signal-to-noise ratio is particularly low. The processing schemes that were effective for estimating the formant frequencies and fundamental frequency of vowels in quiet generally remain adequate in moderate-level background noise. Overall, the discharge patterns contain many cues for distinctions among the vowel stimuli, so that the central processor should be able to identify the different vowels, consistent with psychophysical performance at moderate signal-to-noise ratios.     

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.     

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.     

Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers.

This paper is concerned with the representation of the spectra of synthesized steady-state vowels in the temporal aspects of the discharges of auditory-nerve fibers. The results are based on a study of the responses of large numbers of single auditory-nerve fibers in anesthetized cats. By presenting the same set of stimuli to all the fibers encountered in each cat, we can directly estimate the population response to those stimuli. Period histograms of the responses of each unit to the vowels were constructed. The temporal response of a fiber to each harmonic component of the stimulus is taken to be the amplitude of the corresponding component in the Fourier transform of the unit's period histogram. At low sound levels, the temporal response to each stimulus component is maximal among units with CFs near the frequency of the component (i.e., near its place). Responses to formant components are larger than responses to other stimulus components. As sound level is increased, the responses to the formants, particularly the first formant, increase near their places and spread to adjacent regions, particularly toward higher CFs. Responses to nonformant components, exept for harmonics and intermodulation products of the formants (2F1,2F2,F1 + F2, etc), are suppressed; at the highest sound levels used (approximately 80 dB SPL), temporal responses occur almost exclusively at the first two or three formants and their harmonics and intermodulation products. We describe a simple calculation which combines rate, place, and temporal information to provide a good representation of the vowels' spectra, including a clear indication of at least the first two formant frequencies. This representation is stable with changes in sound level at least up to 80 dB SPL; its stability is in sharp contrast to the behavior of the representation of the vowels' spectra in terms of discharge rate which degenerates at stimulus levels within the conversational range.     

Coding of spectral fine structure in the auditory nerve. II: Level-dependent nonlinear responses

Phase-locked discharge patterns of single cat auditory-nerve fibers were analyzed in response to complex tones centered at fiber characteristic frequency (CF). Signals were octave-bandwidth harmonic complexes defined by a center frequency F and an intercomponent spacing factor N, such that F/N was the fundamental frequency. Parameters that were manipulated included the phase spectrum, the number of components, and the intensity of the center component. Analyses employed Fourier transforms of period histograms to assess the degree to which responses were synchronized to the frequencies present in the acoustic stimulus. Several nonlinearities were observed in the response as intensity was varied between threshold and 80-90 dB SPL. Response nonlinearities were strong for all signals except those with random phase spectra. The most commonly observed nonlinearity was an emphasis of one or more stimulus components in the response. The degree of nonlinearity usually increased with intensity and signal complexity and decreased with fiber frequency selectivity. Half-wave rectification introduced synchronization to the missing fundamental. The strength of the response at the fundamental was related to stimulus crest factor. Signals with low center frequencies and high crest factors often elicited instantaneous discharge rates at the theoretical maximum of pi CF. This suggests that the probability of spike generation approaches one during high-amplitude waveform segments. Response nonlinearity was interpreted as arising from three sources, namely, cochlear mechanics, compression of instantaneous discharge rate, and saturation of average discharge rate. At near-threshold intensities, fibers with high spontaneous rates exhibited responses that were linear functions of stimulus waveshape, whereas fibers with low spontaneous spike rates produced responses that were best described in terms of an expansive nonlinearity.     

Auditory nerve representation of a complex communication sound in background noise.

A population study of auditory nerve responses in the bullfrog, Rana catesbeiana, analyzed the relative contributions of spectral and temporal coding in representing a complex, species-specific communication signal at different stimulus intensities and in the presence of background noise. At stimulus levels of 70 and 80 dB SPL, levels which approximate that received during communication in the natural environment, average rate profiles plotted over fiber characteristic frequency do not reflect the detailed spectral fine structure of the synthetic call. Rate profiles do not change significantly in the presence of background noise. In ambient (no noise) and low noise conditions, both amphibian papilla and basilar papilla fibers phase lock strongly to the waveform periodicity (fundamental frequency) of the synthetic advertisement call. The higher harmonic spectral fine structure of the synthetic call is not accurately reflected in the timing of fiber firing, because firing is "captured" by the fundamental frequency. Only a small number of fibers synchronize preferentially to any harmonic in the call other than the first, and none synchronize to any higher than the third, even when fiber characteristic frequency is close to one of these higher harmonics. Background noise affects fiber temporal responses in two ways: It can reduce synchronization to the fundamental frequency, until fiber responses are masked; or it can shift synchronization from the fundamental to the second or third harmonic of the call. This second effect results in a preservation of temporal coding at high noise levels. These data suggest that bullfrog eighth nerve fibers extract the waveform periodicity of multiple-harmonic stimuli primarily by a temporal code.     

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.     

Effect of masker level on overshoot

Overshoot refers to the phenomenon where signal detectability improves for a short-duration signal as the onset of that signal is delayed relative to the onset of a longer duration masker. A popular explanation for overshoot is that it reflects short-term adaptation in auditory-nerve fibers. In this study, overshoot was measured for a 10-ms, 4-kHz signal masked by a broadband noise. In the first experiment, masker duration was 400 ms and signal onset delay was 1 or 195 ms; masker spectrum level ranged from - 10-50 dB SPL. Overshoot was negligible at the lowest masker levels, grew to about 10-15 dB at the moderate masker levels, but declined and approached 0 dB at the highest masker levels. In the second experiment, the masker duration was reduced to 100 ms, and the signal was presented with a delay of 1 or 70 ms; masker spectrum level was 10, 30, or 50 dB SPL. Overshoot was about 10 dB for the two lower masker levels, but about 0 dB at the highest masker level. The results from the second experiment suggest that the decline in overshoot at high masker levels is probably not due to auditory fatigue. It is suggested, instead, that the decline may be attributable to the neural response at high levels being dominated by those auditory-nerve fibers that do not exhibit short-term adaptation (i.e., those with low spontaneous rates and high thresholds).     

Speech coding in the auditory nerve: IV. Sounds with consonant-like dynamic characteristics

Discharge patterns of auditory-nerve fibers in anesthetized cats were obtained for two stimulus levels in response to synthetic stimuli with dynamic characteristics appropriate for selected consonants. A set of stimuli was constructed by preceding a signal that was identified as /da/by another sound that was systematically manipulated so that the entire complex would sound like either /da/, /ada/, /na/, /sa/, /sa/, or others. Discharge rates of auditory-nerve fibers in response to the common /da/-like formant transitions depended on the preceding context. Average discharge rates during these transitions decreased most for fibers whose CFs were in frequency regions where the context had considerable energy. Some effect of the preceding context on fine time patterns of response to the transitions was also found, but the identity of the largest response components (which often corresponded to the formant frequencies) was in general unaffected. Thus the response patterns during the formant transitions contain cues about both the nature of the transitions and the preceding context. A second set of stimuli sounding like /s/ and /c/ was obtained by varying the duration of the rise in amplitude at the onset of a filtered noise burst. At both 45 and 60 dB SPL, there were fibers which showed a more prominent peak in discharge rate at stimulus onset for /c/ than for /s/, but the CF regions that reflected the clearest distinctions depended on stimulus level. The peaks in discharge rate that occur in response to rapid changes in amplitude or spectrum might be used by the central processor as pointers to portions of speech signals that are rich in phonetic information.     

Maturation of the traveling-wave delay in the human cochlea

The maturation of the traveling-wave delay in the human cochlea was investigated in 227 subjects ranging in age from 29 weeks conceptional age to 49 years by using frequency specific auditory brain-stem responses (ABRs). The derived response technique was applied to ABRs obtained with click stimuli (presented at a fixed level equal to 60-dB sensation level in normal hearing adults) in the presence of high-pass noise masking (slope 96 dB/oct) to obtain frequency specific responses from octave-wide bands. The estimate of traveling-wave delay was obtained by taking the difference between wave I latencies from adjacent derived bands. It was found that the traveling-wave delay between the octave band with center frequency (CF) of 11.3 kHz and that with CF of 5.7 kHz decreased (about 0.4 ms on average) in exponential fashion with age to reach adult values at 3-6 months of age. This decrease was in agreement with reported data in kitten auditory-nerve fibers. The traveling-wave delays between adjacent octave bands with successive lower CF did not change with age.     

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.     

Extraction and enhancement of spectral structure by the cochlea

The intensity dependence of signal processing in the cat cochlea was studied in responses of single auditory-nerve fibers for harmonic complexes having various amplitude and phase spectra. Analyses were based on information present in temporal discharge cadences, and they consisted of assessing Fourier spectra of period histograms synchronized to the period of the waveform fundamental. At low intensities, response spectra resembled filtered versions of the stimulus spectrum, with the amounts of filtering being determined by fibers' tuning curves. At high intensities, response spectra exhibited nonlinear behavior and could differ dramatically from spectra obtained at low intensities. The high-intensity response typically emphasized one or more aspects of the stimulus spectrum. When the stimulus possessed equal component amplitudes and phases, the features that were emphasized at high intensities were the high- and low-frequency edges of the spectrum, and when the component at fiber CF was changed in phase or amplitude relative to the others, fibers primarily signaled the presence of the phase- or amplitude-shifted component. Many of the intensity-dependent changes in response spectra are accounted for by considering the effects of the compressive input-output nonlinearity operating at or peripheral to the hair-cell level on the temporal waveform.     

Speech coding in the auditory nerve: II. Processing schemes for vowel-like sounds

Several processing schemes by which phonetically important information for vowels can be extracted from responses of auditory-nerve fibers are analyzed. The schemes are based on power spectra of period histograms obtained in response to a set of nine two-formant, steady-state, vowel-like stimuli presented at 60 and 75 dB SPL. One class of "local filtering" schemes, which was originally proposed by Young and Sachs [J. Acoust. Soc. Am. 66, 1381-1403 (1979)], consists of analyzing response patterns by filters centered at the characteristic frequencies (CF) of the fibers, so that a tonotopically arranged measure of synchronized response can be obtained. Various schemes in this class differ in the characteristics of the filter. For a wide range of filter bandwidths, formant frequencies correspond approximately to the CFs for which the response measure is maximal. If in addition, the bandwidths of the analyzing filters are made compatible with psychophysical measures of frequency selectivity, low-frequency harmonics of the stimulus fundamental are resolved in the output profile, so that fundamental frequency can also be estimated. In a second class of processing schemes, a dominant response component is defined for each fiber from a 1/6 octave spectral representation of the response pattern, and the formant frequencies are estimated from the most frequent values of the dominant component in the ensemble of auditory-nerve fibers. The local filtering schemes and the dominant component schemes can be related to "place" and "periodicity" models of auditory processing, respectively.