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.     

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.     

Speech coding in the auditory nerve: III. Voiceless fricative consonants

Responses of auditory-nerve fibers in anesthetized cats were recorded for synthetic voiceless fricative consonants. The four stimuli (/x/, /s/, /s/, and /f/) were presented at two levels corresponding to speech in which the levels of the vowels would be approximately 60 and 75 dB SPL, respectively. Discharge patterns were characterized in terms of PST histograms and their power spectra. For both stimulus levels, frequency regions in which the stimuli had considerable energy corresponded well with characteristic-frequency (CF) regions in which average discharge rates were the highest. At the higher level, the profiles of discharge rate against CF were more distinctive for the stimulus onset than for the central portion. Power spectra of PST histograms had large response components near fiber characteristic frequencies for CFs up to 3-4 kHz, as well as low-frequency components for all fibers. The relative amplitudes of these components varied for the different stimuli. In general, the formant frequencies of the fricatives did not correspond with the largest response components, except for formants below about 3 kHz. Processing schemes based on fine time patterns of discharge that were effective for vowel stimuli generally failed to extract the formant frequencies of fricatives.     

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.     

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.     

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.     

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.     

Masking patterns in the bullfrog (Rana catesbeiana). II: Physiological effects

Responses of individual eighth-nerve fibers in the bullfrog (Rana catesbeiana) were measured to tone bursts at best frequency against a background of continuous, broadband masking noise. These data were used to calculate critical masking ratios to describe the fibers' responses to tones embedded in noise. In the frequency response range of the amphibian papilla (100-1000 Hz), critical ratios increase with tone frequency. Critical ratios of basilar papilla fibers (1000-2000 Hz) are generally higher than those of amphibian papilla fibers. Critical ratios are also significantly related to fiber threshold such that fibers with high thresholds, regardless of their best frequencies, have higher critical ratios and are thus less selective to signals embedded in noise. Critical ratios based on neural responses show a somewhat different frequency-dependent trend than do critical ratios based on psychophysical data presented previously for this species [A. M. Simmons, J. Acoust. Soc. Am. 83, 1087-1092 (1988a)]. In addition, these neural critical ratios do not appear to be level independent, as are psychophysical critical ratios. The data suggest that frequency selectivity of hearing in the bullfrog as measured behaviorally is probably not mediated solely by spectral filtering in the auditory periphery.     

Neuronal responses to amplitude-modulated and pure-tone stimuli in the guinea pig inferior colliculus, and their modification by broadband noise

Neuronal responses were recorded to pure and to sinusoidally amplitude-modulated (AM) tones at the characteristic frequency (CF) in the central nucleus of the inferior colliculus of anesthetized guinea pigs. Temporal (synchronized) and mean-rate measures were derived from period histograms locked to the stimulus modulation waveform to characterize the modulation response. For stimuli presented in quiet, the modulation gain at low frequencies of modulation (approx less than 50 Hz) was inversely proportional to the neuron's mean firing rate in response to both the modulated stimulus and to a pure tone at an equivalent level. In 43% of units the mean discharge rates in response to the AM stimuli were greatest for those modulation frequencies that generated the largest temporal responses. These discharge-rate maxima occurred at signal intensities corresponding to the steeply sloping part of the neuron's pure-tone rate-intensity function (RIF). The change in mean-rate response to modulated stimuli, as a function of intensity, was qualitatively similar to the pure-tone RIF. Adding broadband noise to the modulated stimulus increased the neuron's temporal response to low modulation frequencies. This increase in modulation gain was correlated with mean firing rate in response to the modulation but did not bear a simple relationship to the noise-induced shift in the RIF measured for a pure tone.     

Quantifying the implications of nonlinear cochlear tuning for auditory-filter estimates

The relation between auditory filters estimated from psychophysical methods and peripheral tuning was evaluated using a computational auditory-nerve (AN) model that included many of the response properties associated with nonlinear cochlear tuning. The phenomenological AN model included the effects of dynamic level-dependent tuning, compression, and suppression on the responses of high-, medium-, and low-spontaneous-rate AN fibers. Signal detection theory was used to evaluate psychophysical performance limits imposed by the random nature of AN discharges and by random-noise stimuli. The power-spectrum model of masking was used to estimate psychophysical auditory filters from predicted AN-model detection thresholds for a tone signal in fixed-level notched-noise maskers. Results demonstrate that the role of suppression in broadening peripheral tuning in response to the noise masker has implications for the interpretation of psychophysical auditory-filter estimates. Specifically, the estimated psychophysical auditory-filter equivalent-rectangular bandwidths (ERBs) that were derived from the nonlinear AN model with suppression always overestimated the ERBs of the low-level peripheral model filters. Further, this effect was larger for an 8-kHz signal than for a 2-kHz signal, suggesting a potential characteristic-frequency (CF) dependent bias in psychophysical estimates of auditory filters due to the increase in strength of cochlear nonlinearity with increases in CF.     

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 processing in the auditory system. I: The representation of speech sounds in the responses of the auditory nerve

In a previous paper the speech evoked spatio-temporal response patterns recorded in large populations of auditory-nerve fibers in the cat were examined [M.I. Miller and M.B. Sachs, J. Acoust. Soc. Am. 74, 502-517 (1983)]. The distribution of the relative phases of synchronized activity emerges as an important response feature reflecting the stimulus spectral parameters. Specifically, each strong low-order harmonic of the stimulus (less than or equal to 1.5-2 kHz) dominates the synchrony of a relatively broad segment of fibers near its corresponding characteristic frequency (CF) location in a pattern which mirrors the underlying traveling wave component. Each such fiber segment can be roughly subdivided into two regions: (1) a region basal to the point of resonance of the harmonic where the fiber PST histograms accumulate only small delays (or phase shifts) relative to each other reflecting the fast speed of propagation of the traveling wave, and (2) a region at or very near the point of resonance where the responses exhibit drastic relative phase shifts owing to the sudden slow down of the traveling wave and the consequent rapid accumulation of phase shifts. These rapid phase shifts thus manifest themselves as steep and localized spatial discontinuities in an otherwise relatively uniform instantaneous pattern of activity across the fiber array, all occurring at the CF locations corresponding to the low-order harmonics of the stimulus.     

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.     

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.     

Responses of "lower-spontaneous-rate" auditory-nerve fibers to speech syllables presented in noise. I: General characteristics.

Responses of auditory-nerve fibers in anesthetized cats to nine different spoken stop- and nasal-consonant/vowel syllables presented at 70 dB SPL in various levels of speech-shaped noise [signal-to-noise (S/N) ratios of 30, 20, 10, and 0 dB] are reported. The temporal aspects of speech encoding were analyzed using spectrograms. The responses of the "lower-spontaneous-rate" fibers (less than 20/s) were found to be more limited than those of the high-spontaneous-rate fibers. The lower-spontaneous-rate fibers did not encode noise-only portions of the stimulus at the lowest noise level (S/N = 30 dB) and only responded to the consonant if there was a formant or major spectral peak near its characteristic frequency. The fibers' responses at the higher noise levels were compared to those obtained at the lowest noise level using the covariance as a quantitative measure of signal degradation. The lower-spontaneous-rate fibers were found to preserve more of their initial temporal encoding than high-spontaneous-rate fibers of the same characteristic frequency. The auditory-nerve fibers' responses were also analyzed for rate-place encoding of the stimuli. The results are similar to those found for temporal encoding.     

Effects of acoustic overstimulation on spectral and temporal processing in the amphibian auditory nerve

Activity of isolated auditory-nerve fibers in tree frogs (Eleutherodactylus coqui) exposed to continuous 3-min tones of different intensities at their characteristic frequencies (CFs) was recorded. Period histograms show a retardation in the preferred phase of discharge during and after the cessation of the exposure. Postexposure phase shift is concomitant with an elevation in CF thresholds and related to the level of tone exposure above threshold. Vector strength does not show comparable trends of change; postexposure shifts are related to preexposure CF thresholds. Recovery of phase retardation is rapid; units exposed to successive 3-min tones of the same intensities with intervals of 10-14 min between exposures experienced similar changes in their patterns of temporal discharge. Micromechanical changes affecting stereocilia stiffness or structural alterations in the tectorial membrane of the amphibian papilla may underly the transitory phase shifts observed in traumatized anuran auditory fibers.     

A possible neurophysiological basis of the octave enlargement effect

Although the physical octave is defined as a simple ratio of 2:1, listeners prefer slightly greater octave ratios. Ohgushi [J. Acoust. Soc. Am. 73, 1694-1700 (1983)] suggested that a temporal model for octave matching would predict this octave enlargement effect because, in response to pure tones, auditory-nerve interspike intervals are slightly larger than the stimulus period. In an effort to test Ohgushi's hypothesis, auditory-nerve single-unit responses to pure-tone stimuli were collected from Dial-anesthetized cats. It was found that although interspike interval distributions show clear phase-locking to the stimulus, intervals systematically deviate from integer multiples of the stimulus period. Due to refractory effects, intervals smaller than 5 msec are slightly larger than the stimulus period and deviate most for small intervals. On the other hand, first-order intervals are smaller than the stimulus period for stimulus frequencies less than 500 Hz. It is shown that this deviation is the combined effect of phase-locking and multiple spikes within one stimulus period. A model for octave matching was implemented which compares frequency estimates of two tones based on their interspike interval distributions. The model quantitatively predicts the octave enlargement effect. These results are consistent with the idea that musical pitch is derived from auditory-nerve interspike interval distributions.     

Response dynamics of goldfish saccular fibers: effects of stimulus frequency and intensity on fibers with different tuning, sensitivity, and spontaneous activity

The effects of stimulus frequency and intensity on response patterns (PST histograms) to tone burst stimulation were examined in differently tuned saccular fibers of the goldfish. In addition, the sensitivity of these fibers to amplitude-modulated (AM) signals of different carrier frequencies was measured. The response patterns evoked by unmodulated signals were a complex function of tuning, spontaneous activity and sensitivity of the fiber, and the frequency and intensity of the signal. Frequency-dependent response patterns were found in low-frequency fibers with best frequencies (BF) below 200 Hz. Responses in these fibers ranged from tonic to phasic in nonspontaneous fibers and included more complex patterns in spontaneously active fibers, such as suppression of evoked activity below spontaneous levels. Midfrequency fibers (BF = 500-600 Hz) showed responses similar to those in low-frequency fibers, but with less dependence on frequency. In contrast, both high-frequency (BF = 800-1000 Hz) and wideband, untuned fibers showed frequency-invariant patterns of adaptation. High-frequency fibers were equally sensitive to AM signals at all frequencies tested. The sensitivity of low-frequency fibers to AM, however, increased as a function of carrier frequency and corresponded to the degree of adaptation in response to unmodulated tones. In general, the AM sensitivity of a fiber could be predicted more by its pattern of response to unmodulated signals than by its tuning characteristics.