Two-tone suppression of basilar membrane vibrations in the base of the guinea pig cochlea using "low-side" suppressors.

The responses of the basilar membrane (BM) in the basal section of the guinea pig cochlea were measured by laser interferometry. The stimuli were pairs of harmonically related tones, presented simultaneously. One tone, at the BM's characteristic frequency (CF) of about 17 kHz, was presented at a low intensity. The other tone, presented at various intensities, was a "low-side" suppressor, with a frequency of 0.2-8 kHz. As observed by many others, the suppressor tone, when presented at high enough intensity, reduced the magnitude of the CF component of BM displacement, sometimes dramatically. However, regardless of whether the CF component was suppressed or not, the sum of the displacement amplitudes of the CF and suppressor components was always greater than the displacement amplitude of the unsuppressed CF component. For suppressor frequencies up to 4 kHz, the suppression was both tonic and phasic, and synchronized to the suppressor period. For higher suppressor frequencies, principally tonic suppression was seen.

Further results with the 'uniquantal EPSP' hypothesis.

The hypothesis of Geisler (Brain Res. 212 (1981) 198-201), in which the different spontaneous-rate classes of primary auditory neurons were accounted for by the different sizes of uniquantal EPSPs relative to the gap between resting membrane and threshold potentials, was represented with an expanded model which included relative refractory effects. The spike rates generated by the expanded model, when plotted vs. estimated sound level, are qualitatively similar to those of experimentally obtained rate-level curves. The hypothesis is also consistent with recent ultrastructural data which suggest that average quantal-release rates for any particular primary auditory neuron are inversely related to its spontaneous rate. The model's recovery processes following spike generation (hazard functions) are also similar to those observed experimentally.

Temporal patterns of the responses of auditory-nerve fibers to low-frequency tones.

The temporal response patterns of auditory-nerve fibers to low-frequency tones were studied in anesthetized cats using period histograms. 'Peak-splitting' was observed mostly in fibers with lower characteristic frequencies (CF < 2 kHz) and with lower-frequency stimulation (< or = 500 Hz). The occurrence of peak-splitting, the number of peaks, and the time between the peaks were all dependent upon the stimulus frequency. The phases of responses, although complex functions of stimulus frequency, intensity, and the fiber's CF, clearly showed traveling-wave characteristics for all frequencies at or above 100 Hz. The amount of phase change with intensity was generally small for lower-frequency stimuli (< approximately 50 degrees), although larger phase changes (e.g., approximately 180 degrees) were occasionally seen with higher-frequency stimuli. At 50 and 100 Hz, the phase of neural responses in the basal region roughly corresponds to the maximum velocity of the basilar membrane towards scala tympani (as inferred from cochlear microphonic recordings).

Suppression in auditory-nerve fibers of cats using low-side suppressors. I. Temporal aspects.

Two-tone suppression was studied in the auditory nerve fibers of anesthetized cats, using low-frequency suppressors (50-2000 Hz). The response to the characteristic-frequency (CF) tone was suppressed in a phase-specific manner, attaining one or two minimums in 1 cycle of the suppressor (SUP) tone. The suppression phase-lead (i.e., the phase of maximum suppression leading the phase of response to the SUP tone) was about 1/4 cycle for lower-frequency suppressors (50, 100 and 200 Hz), and was close to 1/2 cycle for higher-frequency suppressors (500, 1000 and 2000 Hz). Both the phase of suppression and the suppression phase-lead are independent of fiber spontaneous rate (SR). Some fibers also show a secondary (minor) suppression at higher SUP intensities, which is always about 1/2 cycle away from the first (major) one. Fibers with higher CFs (> 2 kHz) are more likely to show a secondary suppression than those with lower CFs. The threshold difference between the major and minor suppressions is CF-dependent: lower CF fibers usually show differences of 10 dB or greater, while higher CF fibers show smaller differences. The secondary suppression is suppressor-frequency-dependent, usually restricted to lower-frequency suppressors (< or = 200 Hz). No fibers showed a secondary suppression with a SUP frequency 1000 Hz or greater. The phases of suppressions (both the major and minor suppressions) are not affected by the intensity of the CF tone. Non-excitatory, low-frequency suppressors can also give rise to significant suppression. The threshold of synchronization to the SUP tone in the two-tone part was usually the lowest, while the SUP-alone rate threshold was highest. The threshold of synchronization in the SUP-alone segment and threshold of suppression were in between. In some low-SR fibers, complete suppression can be seen.

Suppression in auditory-nerve fibers of cats using low-side suppressors. II. Effect of spontaneous rates.

The responses of auditory nerve fibers with different spontaneous rates were studied in anesthetized cats, using harmonically related characteristic frequency (CF) tone and suppressor (SUP) tone (50-2000 Hz) as stimuli. The relative-response index, defined as the ratio of the maximum response level in the two-tone segment to the response level in the CF-alone segment, at or near the intensity of maximum suppression (i.e., where the two-tone rate was lowest), was dependent on fiber's spontaneous rate (SR). For all the SUP frequencies used, lower-SR fibers almost always showed values less than unity, while high-SR fibers almost always gave values near or greater than unity. The phase of maximum suppression was not dependent upon fiber SR. In one experiment, a pair of low- and high-SR fibers with the same CF (12 kHz) were recorded consecutively in the same electrode penetration, and were studied with the same stimulus parameters. Their temporal responses showed dramatic temporal resemblances, with very similar phases of suppression and response. But the relative-response indexes were different. The similarities in the lower- and high-SR fibers support the idea that the basic response and suppression patterns in all fibers are formed at or before the inner hair cell (IHC) stage, while the differences suggest that processes more central than the IHC receptor potential are important in determining the magnitudes of suppression, particularly in the lower-SR fibers.

Suppression in auditory-nerve fibers of cats using low-side suppressors. III. Model results.

A phenomenological model which simulates auditory-nerve (AN) two-tone suppression was developed. The model uses the output of the outer hair cell (OHC) to control the gain of the cochlear amplifier, which presumably affects only frequencies near the characteristic frequency (CF). Among other things, the model can simulate basic AN suppression patterns including the 1/4 to 1/2 cycle relationships which exist between phase of suppression and phase of excitation to the suppressor (SUP) tone alone (Cai and Geisler, 1996a). Without any changes, it is also able to simulate the experimental low-frequency biasing data and the suppression of CF component by the low-frequency SUP tone in the OHC outputs (Cheatham and Dallos, 1994). These successful simulations of the suppression patterns support the basic assumption in the model, that the saturation of OHC transduction current produces two-tone suppression. However, the amplitude behavior of the model fits that obtained only from AN fibers with high spontaneous rates (and from inner hair cells (IHC)), but not fibers with lower spontaneous rates. It appears, therefore, that other unknown mechanism(s) operating at stages following the IHC potential are important in determining the magnitude of low-side suppression.

Long-term suppression of the responses of auditory nerve fibers to a characteristic-frequency tone by a low-frequency suppressor.

The classical two-tone suppression requires the characteristic-frequency (CF) tone and the suppressor (SUP) tone to act simultaneously. We report a novel phenomenon whereby the responses to the CF tone alone were 'suppressed' by a preceding low-side SUP tone. Increasing the repetition interval to about 3000 ms or longer eliminated such suppression. The magnitude of this 'long-term' suppression was not dependent upon fiber CF, but fibers with low spontaneous rates (SR) generally showed more suppression than high-SR fibers did. The suppression threshold was not dependent upon fiber SR. This suppression of the CF responses did not affect the phases of responses to either the CF or SUP tone, or the phase of suppression. This phenomenon is not due to adaptation or fatigue, but due to the presence of the preceding SUP tone. The efferent system, particularly the 'slow' effect, might be responsible for it.

Relationships between frequency-tuning and spatial-tuning curves in the mammalian cochlea.

The tuning curve of a single auditory-nerve fiber is a measure of the intensity levels producing that fiber's threshold response at each of a number of frequencies. For many purposes it is desirable to know cochlear responses as a function of cochlear location (spatial distance from the stapes). Using assumptions of uniformity, the relationships between auditory-nerve-fiber frequency-tuning curves, basilar-membrane frequency-response curves, and basilar-membrane spatial-response curves are obtained. From the spatial-response characteristics which are then inferred from neural frequency-tuning curves, it appears that the tuning properties of the apical cochlea are fairly uniform and differ from the tuning properties of the basal cochlea.

A cochlear model using feed-forward outer-hair-cell forces.

A linear (frequency-domain) model of the cat cochlea (implemented in both 1- and 2-dimensional versions) has been developed which uses outer hair cell (OHC) forces in a geometry which includes the longitudinal (base-to-apex) tilt of the outer hair cells (OHCs). When positive (contractile) real OHC force-constants are used, very large (50 + dB) response peaks along with very rapidly accumulating phase lags (which can reach -50 pi radians) are obtained. The wider the longitudinal segmentation, the broader the peaks and the less the phase accumulation; 71-microns segmentation produced the most realistic responses. These large response peaks are achieved by a small zone of negative resistance (ca. 1 mm) just basal to the response peak and the virtual 'zeroing' of the basilar membrane's effective impedance over the entire peak region (ca. 2.5 mm). To produce these peaks, the OHCs generate about 25-times the incoming acoustic power. Inclusion of low-pass filtering in the model's OHC representation produces, by contrast, very unrealistic notch-and-peak displacement complexes accompanied by very large phase lags, for all segmentation widths used. However, when phase reversals of OHC forces are also added, achieved by imbedding a resonant system within the tectorial membrane, very realistic peaks and phase functions are produced. More power must, however, be generated by the OHCs (about 70-times the incoming). The end result is output which mimics quite closely the living basilar membrane's responses to low-intensity high-frequency tones.

A realizable cochlear model using feedback from motile outer hair cells.

A physically realizable form of a recent cochlear model using feedback forces from motile outer hair cells [Geisler (1991) Hear. Res. 54, 105-117] has been developed. The model was computer-simulated in the frequency domain (necessarily linear). Its responses to pure tones are very realistic in terms of sharpness (Q10s of 3-5) and in terms of tip-to-tail ratios (50-60 dB). These large tips are due to the feedback forces, which act as negative resistances (energy-supplying elements) over restricted spatial ranges. Nyquist-criterion analysis indicates that the model is stable. The spatial patterns of the model's output also bear qualitative resemblances to several other phenomena observed in cochleas, both living and excised.

A model of stereociliary tip-link stretches.

A model of the tip-link stretches produced by angular deflections of the stereocilia of vertebrate acoustico-lateralis hair cells is presented. It is shown that tip-link stretch in the model is proportional to the angle of stereociliary deflection. By contrast, the stretch of a horizontal (e.g., row-to-row) link is proportional to the square of the angle of stereociliary deflection. Possible roles of these stretches in sensory transduction are discussed.

Two-tone suppression, excitation and the after effect in rate responses in auditory nerve fibres in the cat.

Responses were recorded from single, auditory nerve fibres in the anaesthetized cat. Acoustic stimuli consisted of two tones, one of which was at characteristic frequency (CF), the other (the suppressor) was at considerably lower frequency. Tones were presented in simultaneous and sequential configurations. For simultaneous presentations, well-known response properties were observed. The rising limb of the two-tone rate-intensity function closely matched that of the appropriately adapted response to the suppressor tone presented alone. Also, whether strongly suppressed relative to CF-driven rate, or equal to CF-driven rate, rate responses to the two-tone stimuli persisted unchanged when the CF tone was terminated and the suppressor tone continued alone. These results support the hypothesis that the suppressor tone has dual influences, suppressive and excitatory, that are distinct and additive. Peristimulus response histograms confirm in the cat that depression and slow recovery of sensitivity to CF may follow termination of the suppressor tone, as reported for the guinea pig [Hill, K.G. and Palmer, A.R. (1991) Hear. Res. 55, 167-176]. This delay in recovery of normal sensitivity to CF appeared to be directly related to the amount of excitation of the fibre that is attributable to the suppressor tone. A similar, delayed re-establishment of sensitivity also occurred in the response to a tone at CF, presented immediately following excitation by a suppressor tone. However, no delay occurred in the onset of response to the suppressor when preceded by the CF tone.(ABSTRACT TRUNCATED AT 250 WORDS)

Two-tone suppression by a saturating feedback model of the cochlear partition.

A model of a small strip of cochlear partition was computer simulated. The model is composed of two elements, approximations to the transfer functions of an inner hair cell (IHC) and an outer hair cell (OHC), respectively. The IHC element was insensitive to DC stimulation. Input was one or two sinusoids. One sinusoid, at the characteristic frequency (CF), was multiplied by the gain of the 'cochlear amplifier'. A second sinusoid, representing a tone with much lower frequency, was not affected by the amplifier gain. This gain was determined by the OHC transfer function. In one form of the model ('fixed-gain'), this gain was set at a fixed number determined from the furthest point reached on the OHC transfer function. This form of the model produced very realistic single-tone responses as well as showing 'two-tone suppression': that is, the IHC DC response produced by CF stimulation was reduced when the lower-frequency sinusoid, at suitable intensities, was added to the stimulus. When a DC component was added to the two-tone stimulus, the magnitude of this two-tone suppression was enhanced. In the second form of the model ('variable-gain'), the cochlear-amplifier gain varied throughout the stimulus cycle. Its value was re-calculated at each instant, determined by the point on the OHC transfer function current at that particular instant. This form of the model showed two-tone suppression only when a DC component was added to the two-tone stimulus.

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.

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.

A cochlear model using feedback from motile outer hair cells.

A model of cochlear vibrations based upon motile outer hair cells (OHCs) has been developed using physiologically demonstrated phenomena. Rapid longitudinally directed OHC forces are connected in such a way as to form a negative-feedback system. The responses at the higher frequencies (greater than 1 kHZ) are quite realistic: they have properly shaped amplitude curves with large tip-to-tail ratios (30-50 dB), Q10's of 2-6, and 'shoulders' at frequencies an octave below the resonant frequency. The phases are also quite realistic, though asymptoting at somewhat lower values (about -6 pi radians) than observed physiologically. The responses in the apical section are not so realistic. The form of the OHC force is physically unrealizable, but realizable forms are discussed.

Saturation of outer hair cell receptor currents causes two-tone suppression.

Zwicker [Biol. Cybern. 35, 243-250, (1979); J. Acoust. Soc. Am. 80, 163-176 (1986)] has previously proposed that many nonlinear phenomena in the mammalian cochlea can be explained by saturation of a positive feedback process which enhances mechanical sensitivity, although the site of the nonlinearity producing this saturation has so far remained obscure. In this paper we present evidence suggesting that the nonlinearity of mechano-electrical transduction in the outer hair cells is the dominant nonlinearity producing two-tone suppression in the mammalian cochlea. In particular, we show that: (i) suppression of the extracellular summating potential (SP), recorded from a particular place within the organ of Corti, has characteristics similar to the suppression of activity in the auditory-nerve; (ii) that SP suppression occurs at approximately constant basilar membrane displacement, inferred from the SP iso-response contours; and that (iii) the onset of SP suppression with suppressor tones on the tail of the frequency tuning curve closely parallels the onset of nonlinearity in the local cochlear microphonic. Since previous studies (Patuzzi et al., 1989) have demonstrated that the vibration of the basilar membrane at its characteristic frequency is very sensitive to changes in outer hair cell receptor current, we consider that interference in outer hair cell currents caused by nonlinearity in mechano-electrical transduction is an adequate explanation of two-tone suppression. This requires that outer hair cell receptor currents deviate from linearity at a suppressor tone level below that required to produce a significant DC receptor potential within the inner hair cells, and that the active process within the cochlea is distributed along a local region of the cochlea, basal of the vibration peak.

Estimation of eardrum acoustic pressure and of ear canal length from remote points in the canal.

Sound pressure distributions in the human ear canal, whether unoccluded or occluded with ear molds, were studied using a probe tube technique. On average, for frequencies below 6 kHz, the measuring probe tube had to be placed within 8 mm of the vertical plane containing the top of the eardrum (TOD), determined optically, in order to obtain sound pressure magnitudes within 6 dB of "eardrum pressure." To obtain that accuracy in all of the eight subjects studied, the probe had to be within 6 mm of the TOD. Since probe location relative to the drum has to be known, a purely acoustic method was developed which can be conveniently used to localize the probe-tip position, utilizing the standing wave property of the sound pressure in the ear canal. The acoustically estimated "drum location" generally lay between the optically determined vertical planes containing the TOD and the umbo. On average, the "drum location" fell 1 mm medial to the TOD. Of the 32 estimates made acoustically in various occluded and unoccluded conditions in 14 subjects, 30 estimates lay within a +/- 2-mm range of this average.

Evidence for expansive power functions in the generation of the discharges of 'low- and medium-spontaneous' auditory-nerve fibers.

Re-analysis of data from Geisler et al. [J. Acoust. Soc. Am. 77, 1102-1109, 1985] indicates that the slopes of the intensity versus discharge-rate curves of auditory nerve (AN) fibers decrease systematically with increasing spontaneous discharge rate. For 'high-spontaneous' fibers, the slope is usually less than 0.5 dB/dB, while for 'low-spontaneous' fibers the slopes reach values greater than 4.0 dB/dB. A two-stage model accounts for this behavior. The first stage is a static non-linearity based on the measured intensity-voltage characteristic of inner hair cells. The second stage, representing action-potential generation, is linear for high-spontaneous fibers, but a squaring function for low- and medium-spontaneous fibers. The output of the model displays realistic slopes for its various intensity-rate curves. There are suggestions that a nonlinearity of still higher power is needed to simulate accurately the behavior of AN fibers having the lowest spontaneous rates (less than 0.1/s). The model also accounts for other observed differences between the discharge patterns of the different fiber classes.

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.