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.     

Responses to amplitude-modulated tones in the auditory nerve of the cat.

Sinusoidally amplitude-modulated (AM) tones are frequently used in psychophysical and physiological studies, yet a comprehensive study on the coding of AM tones in the auditory nerve is lacking. AM responses of single auditory-nerve fibers of the cat are studied, systematically varying modulation depth, frequency, and sound level. Synchrony-level functions were nonmonotonic with maximum values that were inversely correlated with spontaneous rate (SR). In most fibers, envelope phase-locking showed a positive gain. Modulation transfer functions were uniformly low pass. Their corner frequency increased with characteristic frequency (CF), but changed little for CFs above 10 kHz. The highest modulation frequencies to which phase locking occurred were more than 0.8 oct lower than the highest frequencies to which phase locking to pure tones occurs. Cumulative, or unwrapped, phase increased linearly with modulation frequency: The slope was inversely related to CF, and slightly higher than group delays reported for pure tones. High SR, low CF fibers showed the poorest envelope phase locking. In some low CF fibers, phase locking increased at high levels, associated with "peak-splitting" phenomena. Changes in average rate due to modulation were small, and could be enhancement or suppression.     

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.     

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.     

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.     

Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate

Responses of large populations of auditory-nerve fibers to synthesized steady-state vowels were recorded in anesthetized cats. Driven discharge rate to vowels, normalized by dividing by saturation rate (estimated from the driven rate to CF tones 50 dB above threshold), was plotted versus fiber CF for a number of vowel levels. For the vowels /I/ and /e/, such rate profiles showed a peak in the region of the first formant and another in the region of the second and third formants, for sound levels below about 70 dB SPL. For /a/ at levels below about 40 dB SPL there are peaks in the region of the first and second formants. At higher levels these peaks disappear for all the vowels because of a combination of rate saturation and two-tone suppression. This must be qualified by saying that rate profiles plotted separately for units with spontaneous rates less than one spike per second may retain peaks at higher levels. Rate versus level functions for units with CFs above the first formant can saturate at rates less than the saturation rate to CF to-es or they can be nonmonotonic; these effects are most likely produced by the same mechanism as that involved in two-tone suppression.     

Maturation of cochlear nonlinearity as measured by distortion product otoacoustic emission suppression growth in humans

The growth of distortion product otoacoustic emission (DPOAE) suppression follows a systematic, frequency-dependent pattern. The pattern is consistent with direct measures of basilar-membrane response growth, psychoacoustic measures of masking growth, and measures of neural rate growth. This pattern has its basis in the recognized nonlinear properties of basilar-membrane motion and, as such, the DPOAE suppression growth paradigm can be applied to human neonates to study the maturation of cochlear nonlinearity. The objective of this experiment was to investigate the maturation of human cochlear nonlinearity and define the time course for this maturational process. Normal-hearing adults, children, term-born neonates, and premature neonates, plus a small number of children with sensorineural hearing loss, were included in this experiment. DPOAE suppression growth was measured at two f2 frequencies (1500 and 6000 Hz) and three primary tone levels (55-45, 65-55, and 75-65 dB SPL). Slope of DPOAE suppression growth, as well as an asymmetry ratio (to compare slope for suppressor tones below and above f2 frequency), were generated. Suppression threshold was also measured in all subjects. Findings indicate that both term-born neonates and premature neonates who have attained term-like age, show non-adult-like DPOAE suppression growth for low-frequency suppressor tones. These age effects are most evident at f2 = 6000 Hz. In neonates, suppression growth is shallower and suppression thresholds are elevated for suppressor tones lower in frequency than f2. Additionally, the asymmetry ratio is smaller in neonates, indicating that the typical frequency-dependent pattern of suppression growth is not present. These findings suggest that an immaturity of cochlear nonlinearity persists into the first months of postnatal life. DPOAE suppression growth examined for a small group of hearing-impaired children also showed abnormalities.     

Multicomponent stimulus interactions observed in basilar-membrane vibration in the basal region of the chinchilla cochlea.

Multicomponent stimuli consisting of two to seven tones were used to study suppression of basilar-membrane vibration at the 3-4-mm region of the chinchilla cochlea with a characteristic frequency between 6.5 and 8.5 kHz. Three-component stimuli were amplitude-modulated sinusoids (AM) with modulation depth varied between 0.25 and 2 and modulation frequency varied between 100 and 2000 Hz. For five-component stimuli of equal amplitude, frequency separation between adjacent components was the same as that used for AM stimuli. An additional manipulation was to position either the first, third, or fifth component at the characteristic frequency (CF). This allowed the study of the basilar-membrane response to off-CF stimuli. CF suppression was as high as 35 dB for two-tone combinations, while for equal-amplitude stimulus components CF suppression never exceeded 20 dB. This latter case occurred for both two-tone stimuli where the suppressor was below CF and for multitone stimuli with the third component=CF. Suppression was least for the AM stimuli, including when the three AM components were equal. Maximum suppression was both level- and frequency dependent, and occurred for component frequency separations of 500 to 600 Hz. Suppression decreased for multicomponent stimuli with component frequency spacing greater than 600 Hz. Mutual suppression occurred whenever stimulus components were within the compressive region of the basilar membrane.     

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.     

Psychophysical suppression measured with bandlimited noise extended below and/or above the signal: effects of age and hearing loss

The objectives of this study were to measure suppression with bandlimited noise extended below and above the signal, at lower and higher signal frequencies, between younger and older subjects, and between subjects with normal hearing and cochlear hearing loss. Psychophysical suppression was assessed by measuring forward-masked thresholds at 0.8 and 2.0 kHz in bandlimited maskers as a function of masker bandwidth. Bandpass-masker bandwidth was increased by introducing noise components below and above the signal frequency while keeping the noise centered on the signal frequency, and also by adding noise below the signal only, and above the signal only. Subjects were younger and older adults with normal hearing and older adults with cochlear hearing loss. For all subjects, suppression was larger when noise was added below the signal than when noise was added above the signal, consistent with some physiological evidence of stronger suppression below a fiber's characteristic frequency than above. For subjects with normal hearing, suppression was greater at higher than at lower frequencies. For older subjects with hearing loss, suppression was reduced to a greater extent above the signal than below and where thresholds were elevated. Suppression for older subjects with normal hearing was poorer than would be predicted from their absolute thresholds, suggesting that age may have contributed to reduced suppression or that suppression was sensitive to changes in cochlear function that did not result in significant threshold elevation.     

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.     

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.     

Physiological mechanisms of psychophysical masking: observations from auditory-nerve fibers

Masking might be due either to the spread of the excitation produced by the masker to the place of the tone signal along the cochlea or to the suppression of the response to the signal by the masker. In order to identify the contributions of these two mechanisms to tone-on-tone masking, masked thresholds of auditory-nerve fibers were measured in anesthetized cats using the same stimulus paradigms and detection criteria as in psychophysics. Suppressive masking was identified by comparing thresholds for simultaneous masking with those for a nonsimultaneous masking technique resembling pulsation thresholds. These nonsimultaneous thresholds do not include the contribution of suppression to masking because suppression only occurs for stimuli that overlap in time. For each masker and signal frequency, the fibers with the lowest (or "best") masked thresholds had characteristic frequencies (CF) slightly on the opposite side of the masker frequency with respect to the signal frequency, consistent with the psychophysical phenomenon of off-frequency listening. Patterns of best masked thresholds against signal frequency resembled psychophysical masking patterns in that they showed a maximum for signal frequencies close to the masker, and a skew toward high frequencies. Masking was found to be both excitatory and suppressive, with the relative contribution of the two mechanisms depending on the frequency separation between signal and masker. Suppressive masking was large for signal frequencies well above the masker. For these conditions, simultaneous thresholds grew more rapidly with masker level than did nonsimultaneous thresholds, suggesting that the upward spread of masking is largely due to the growth of suppression rather than to that of excitation.     

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.     

Basilar membrane mechanics at the base of the chinchilla cochlea. II. Responses to low-frequency tones and relationship to microphonics and spike initiation in the VIII nerve

Low-frequency stimuli (40- to 1000-Hz tones) have been used to correlate the motion of the 8-to 9-kHz place of the chinchilla basilar membrane with the cochlear microphonics recorded at the round window and with the responses of auditory nerve fibers with appropriate characteristic frequency. At the lowest stimulus frequencies, maximum displacement of the basilar membrane toward scala tympani occurs in near synchrony with maximum rarefaction at the eardrum and maximum negativity at the round window; at higher frequencies, the mechanical and microphonic response phases progressively lag rarefaction, reaching - 240 deg at 1000 Hz. At most frequencies (40-1000 Hz) near-threshold neural responses, once corrected for neural travel-time and synaptic delays, somewhat lead (by some 40 deg) maximal scala tympani displacement and maximal negativity of the round window microphonics. The variation of sensitivity with frequency is similar for basilar membrane displacement and microphonic responses: Under open-bulla conditions, sensitivity is constant for frequencies between 100 and 1000 Hz; below 100 Hz, sensitivity decreases at rates close to 12 dB/oct toward lower frequencies. Neural response sensitivity matches BM displacement more closely than BM velocity.     

Rate and timing cues associated with the cochlear amplifier: level discrimination based on monaural cross-frequency coincidence detection.

The perceptual significance of the cochlear amplifier was evaluated by predicting level-discrimination performance based on stochastic auditory-nerve (AN) activity. Performance was calculated for three models of processing: the optimal all-information processor (based on discharge times), the optimal rate-place processor (based on discharge counts), and a monaural coincidence-based processor that uses a non-optimal combination of rate and temporal information. An analytical AN model included compressive magnitude and level-dependent-phase responses associated with the cochlear amplifier, and high-, medium-, and low-spontaneous-rate (SR) fibers with characteristic frequencies (CFs) spanning the AN population. The relative contributions of nonlinear magnitude and nonlinear phase responses to level encoding were compared by using four versions of the model, which included and excluded the nonlinear gain and phase responses in all possible combinations. Nonlinear basilar-membrane (BM) phase responses are robustly encoded in near-CF AN fibers at low frequencies. Strongly compressive BM responses at high frequencies near CF interact with the high thresholds of low-SR AN fibers to produce large dynamic ranges. Coincidence performance based on a narrow range of AN CFs was robust across a wide dynamic range at both low and high frequencies, and matched human performance levels. Coincidence performance based on all CFs demonstrated the "near-miss" to Weber's law at low frequencies and the high-frequency "mid-level bump." Monaural coincidence detection is a physiologically realistic mechanism that is extremely general in that it can utilize AN information (average-rate, synchrony, and nonlinear-phase cues) from all SR groups.     

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.     

Perception of across-frequency asynchrony and the role of cochlear delays

Cochlear filtering results in earlier responses to high than to low frequencies. This study examined potential perceptual correlates of cochlear delays by measuring the perception of relative timing between tones of different frequencies. A brief 250-Hz tone was combined with a brief 1-, 2-, 4-, or 6-kHz tone. Two experiments were performed, one involving subjective judgments of perceived synchrony, the other involving asynchrony detection and discrimination. The functions relating the proportion of "synchronous" responses to the delay between the tones were similar for all tone pairs. Perceived synchrony was maximal when the tones in a pair were gated synchronously. The perceived-synchrony function slopes were asymmetric, being steeper on the low-frequency-leading side. In the second experiment, asynchrony-detection thresholds were lower for low-frequency rather than for high-frequency leading pairs. In contrast with previous studies, but consistent with the first experiment, thresholds did not depend on frequency separation between the tones, perhaps because of the elimination of within-channel cues. The results of the two experiments were related quantitatively using a decision-theoretic model, and were found to be highly correlated. Overall the results suggest that frequency-dependent cochlear group delays are compensated for at higher processing stages, resulting in veridical perception of timing relationships across frequency.     

Synchrony-dependent autocorrelation in eighth-nerve-fiber response to rippled noise

Autocorrelograms and interval and delay histograms of the eighth-nerve-fiber response in cats to cosine noise were recorded. A good detectability level for the delay oscillations in the autocorrelograms was always found, when the fiber had a high value of the synchronization index at characteristic frequency (CF). In order to study their relationship, autocorrelograms for cosine noise stimulation were computed by the substitution of synchronization indices in the Poisson distribution formulas for higher-order intervals. The approach was made possible through a further exploration of Johnson's synchronization theory [D. H. Johnson, "The response of single auditory-nerve fibers in the cat to single tones: synchrony and average discharge rate," Ph. D. thesis, MIT, Cambridge, MA (1974)]. It was shown that computed autocorrelograms somewhat resembled experimental ones. The differences between them concerned the envelopes of the "onset" and "delay" oscillations, viz., in their constrictions and amplitudes. These constrictions were shown to be significant only in recordings at delays greater than or equal to 4/CF, corresponding to the dominant region for human repetition pitch.     

Two-tone suppression in auditory nerve of the cat: rate-intensity and temporal analyses

Responses to two-tone stimuli were recorded from auditory-nerve fibers in anesthetized cats. One tone, the suppressor, was set at a frequency above characteristic frequency and was fixed in intensity. A second tone was set at an excitatory frequency and was varied in intensity. The suppressor tone, when set at a sufficient level, always reduced the response to the excitatory tone by an amount equivalent to a fixed number of decibels, regardless of the excitatory tone's intensity. Estimates of suppression magnitude were derived from shifts in rate-intensity function obtained when the suppressor tone was present relative to the functions obtained for the excitatory tone alone. When suppressor-tone intensity was increased, suppression magnitude likewise increased. When the two tones were increasingly separated in frequency, either by varying the excitor or by varying the suppressor, suppression magnitude decreased monotonically. Suppression behaved in the same manner regardless of whether suppresor tone was excitatory or nonexcitatory. When frequency separation was small enough and when both tones were above the neuron's characteristic frequency, responses synchronized to low-order combination tones could be elicited. These responses usually possessed different rate-intensity characteristics and resulted in estimates of suppression magnitude which were spuriously low. When frequency separation is normalized with regard to position of traveling wave maxima within the cochlear duct, the magnitude of two-tone suppression for a given suppressor-tone intensity is seen to be frequency independent.