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.     

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.     

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.     

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.     

Suppression of auditory nerve responses. II. Suppression threshold and growth, iso-suppression contours

Two-tone "synchrony suppression" was studied in responses of single auditory nerve fibers recorded from anesthetized cats. Suppression thresholds for suppressor tones set to a fiber's characteristic frequency (CF) were approximately equal to discharge rate thresholds for CF tones. Suppression thresholds above and below CF were usually lower than the corresponding discharge rate thresholds. However, at all frequencies studied (including CF), suppression thresholds were higher than the corresponding thresholds for discharge synchronization. Across fibers, rates of suppression growth for suppressors at CF were greatest in low-CF fibers and least in high-CF fibers, and there was a systematic decrease in suppression growth rate at CF as CF increased. Within fibers, rates of suppression growth above CF were typically less than at CF, and slopes were monotonically decreasing functions of frequency. Within-fiber rates of suppression growth below CF were variable, but they usually were greater than rates of growth at CF. Iso-suppression contours (frequencies and intensities producing criterion amounts of suppression) indicated that tones near CF are the most potent suppressors at near-threshold intensities, and that the frequency producing the most suppression usually shifts downward as the amount of suppression increases. These data support the notion that synchrony suppression arises primarily as a passive consequence of hair cell activation.     

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.     

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.     

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.     

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.     

Frequency selectivity of single cochlear-nerve fibers based on the temporal response pattern to two-tone signals

The physiological basis of auditory frequency selectivity was investigated by recording the temporal response patterns of single cochlear-nerve fibers in the cat. The characteristic frequency and sharpness of tuning was determined for low-frequency cochlear-nerve fibers with two-tone signals whose frequency components were of equal amplitude and starting phase. The measures were compared with those obtained with sinusoidal signals. The two-tone characteristic frequency (2TCF) is defined as the arithmetic-center frequency at which the fiber is synchronized to both signal frequencies in equal measure. The 2TCF closely corresponds to the characteristic frequency as determined by the frequency threshold curve. Moreover, the 2TCF changes relatively little (2%-12%) over a 60-dB intensity range. The 2TCF generally shifts upward with increasing intensity for cochlear-nerve fibers tuned to frequencies below 1 kHz and shifts downward as a function of intensity for units with characteristic frequencies (CF's) above 1 kHz. The shifts in the 2TCF are considerably smaller than those observed with sinusoidal signals. Filter functions were derived from the synchronization pattern to the two-tone signal by varying the frequency of one of the components over the fiber's response area while maintaining the other component at the 2TCF. The frequency selectivity of the two-tone filter function was determined by dividing the vector strength to the variable frequency signal by the vector strength to the CF tone. The filter function was measured 10 dB down from the peak (2T Q 10 dB) and compared with the Q 10 dB of the frequency threshold curve. The correlation between the two measures of frequency selectivity was 0.72. The 2T Q 10 dB does change as a function of intensity. The magnitude and direction of the change is dependent on the sharpness of tuning at low and moderate sound-pressure levels (SPL's). The selectivity of the more sharply tuned fibers (2T Q 10 dB greater than 3) diminishes at intensities above 60 dB SPL. However, the broadening of selectivity is relatively small in comparison to discharge rate-based measures of selectivity. The selectivity of the more broadly tuned units remains unchanged or improves slightly at similar intensity levels. The present data indicate that the frequency selectivity and tuning of low-frequency cochlear-nerve fibers are relatively stable over a 60-dB range of SPL's when measured in terms of their temporal discharge properties.     

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.     

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.     

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.     

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.     

The representation of the spectra and fundamental frequencies of steady-state single- and double-vowel sounds in the temporal discharge patterns of guinea pig cochlear-nerve fibers

Psychophysical results using double vowels imply that subjects are able to use the temporal aspects of neural discharge patterns. To investigate the possible temporal cues available, the responses of fibers in the cochlear nerve of the anesthetized guinea pig to synthetic vowels were recorded at a range of sound levels up to 95 dB SPL. The stimuli were the single vowels /i/ [fundamental frequency (f0) 125 Hz], /a/ (f0, 100 Hz), and /c/ (f0, 100 Hz) and the double vowels were /a(100),i(125)/ and /c(100),i(125)/. Histograms synchronized to the period of the double vowels were constructed, and locking of the discharge to individual harmonics was estimated from them by Fourier transformation. One possible cue for identifying the f0's of the constituents of a double vowel is modulation of the neural discharge with a period of 1/f0. Such modulation was found at frequencies between the formant peaks of the double vowel, with modulation at the periods of 100 and 125 Hz occurring at different places in the fiber array. Generation of a population response based on synchronized responses [average localized synchronized rate (ALSR): see Young and Sachs [J. Acoust. Soc. Am. 66, 1381-1403 (1979)] allowed estimation of the f0's by a variety of methods and subsampling the population response at the harmonics of the f0 of the constituent vowel achieved a good reconstruction of its spectrum. Other analyses using interval histograms and autocorrelation, which overcome some problems associated with the ALSR approach, also allowed f0 identification and vowel segregation. The present study has demonstrated unequivocally that the timing of the impulses in auditory-nerve fibers provides copious possible cues for the identification of the fundamental frequencies and spectra associated with each of the constituents of double vowels.     

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.     

Diversity of adaptation patterns in responses of eighth nerve fibers in the bullfrog, Rana catesbeiana

The firing patterns of eighth nerve fibers in the bullfrog, Rana catesbeiana, were analyzed for responses to long duration tone bursts at best excitatory frequency ( BEF ) and at frequencies along the upper and lower boundaries of the excitatory tuning curve of each fiber. These firing patterns were used as an index of the degree of short-term adaptation of each fiber. Amphibian papilla fibers (with BEFs 100-1000 Hz) exhibited marked diversity in their firing patterns to BEF tones, ranging from very flat or tonic (sustained responses throughout the duration of the stimulus) to very peaked or phasic (responding primarily or exclusively to stimulus onset). Moreover, the degree of short-term adaptation shown by an individual fiber varied with stimulating frequency. The firing patterns of amphibian papilla fibers tended to become more tonic as stimulus frequency was lowered below BEF ; conversely, as stimulus frequency was increased above BEF , firing patterns either showed little change from that at BEF , or became more phasic. A similar frequency dependence of adaptation has not been reported in responses of mammalian eighth nerve fibers with comparable BEFs . The firing patterns of basilar papilla fibers ( BEFs greater than 1000 Hz) remained similar in response to both BEF and non- BEF tones. These data reveal that the firing patterns and degrees of short-term adaptation of amphibian papilla fibers vary considerably across the tuning curve, whereas those of basilar papilla fibers remain relatively more constant with changes in stimulating frequency.(ABSTRACT TRUNCATED AT 250 WORDS)     

Rate responses of auditory nerve fibers to tones in noise near masked threshold

The rate responses of auditory nerve fibers were measured for best frequency (BF) tone bursts in the presence of continuous background noise. Rate functions for BF tones were constructed over a 32-dB range of levels, centered on the behavioral masked thresholds of cats. The tone level at which noticeable rate changes are evoked by the tones corresponds closely to behavioral masked threshold at all noise levels used (-10- to 30-dB spectrum level). As the noise level increases, the response rate to the background noise approaches saturation, and the incremental rate response to tones decreases. At high noise levels, the rate responses to tones of low and medium spontaneous rate fibers are larger than those of high spontaneous rate fibers. Empirical statistics of auditory nerve fiber spike counts are reported; these differ from those expected of a Poisson process in that the variance is smaller than the mean. A new measure of discharge rate is described that allows rate changes to be expressed in units of a standard deviation. This measure allows tone-evoked responses to be interpreted in terms of their detectability in a signal detection task. Rate responses of low and medium spontaneous rate fibers are more detectable than those of high spontaneous rate fibers, especially at high noise levels. There appears to be sufficient information in the rate response of a small number of auditory nerve fibers to support behaviorally observed levels of detection performance.