Two-tone Suppression Research Articles

Nonlinear mechanics at the apex of the guinea-pig cochlea

A heterodyne laser interferometer was used to observe the sound-evoked displacement patterns of Reissner's membrane and various other structures in the apical turn of the guinea-pig cochlea. Most structures (including the basilar membrane) were similarly tuned, and had best frequencies in the 200–350Hz range. A distinct notch was usually observed ∼ 0.7 octaves above the best frequency, and amplitude- and phase-plateaus were observed at higher frequencies. In most other respects, however, the mechanical tuning resembled the frequency-threshold curves of low frequency cochlear nerve fibers. In five reasonably intact, in vivo preparations, the frequency of the mechanical sensitivity notch was intensity-dependent: Compressive nonlinearities were observed above ∼ 80 dB SPL on the low-frequency side of the notch, with antagonistically expansive nonlinearities on the high-frequency side. Two-tone suppression was observed in one of these preparations. Stimulus-related baseline position shifts were observed in another in vivo preparation. No such nonlinearities were observed in structurally damaged and/or > 1 hour post-mortem preparations. However, more robust nonlinearities were observed in all preparations at higher levels of stimulation (e.g. > 100–110 dB SPL). These high-level nonlinearities diminished only slowly after death, and gave rise to various effects, including time-dependent (i.e. adapting) and severely distorted (e.g. peak-split and/or dc-shifted) responses.

Two-tone suppression in a cochlear model

Two-tone rate suppression is a nonlinear property of the cochlea in which the total neural firing rate in the region most sensitive to a probe tone is reduced by the addition of a second (suppressor) tone at a different frequency. A cochlear model featuring a cascade of adaptive-Q filter sections was investigated to determine its ability to reproduce two-tone suppression. It was found that the adaptive-Q filter sections are adequate to reproduce two-tone suppression when the suppressor is located higher in frequency than the probe tone but are not adequate to reproduce suppression for a suppressor lower in frequency than the probe. A modification to the cochlear model, in which the output signal level is adjusted in response to the estimated peak signal levels in the regions of the cochlear filter tip and tail, was much more accurate in reproducing two-tone suppression behavior. A speech example is also presented, and the implications of two-tone suppression in applications of the cochlear model are discussed.< <ETX xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink">&gt;</ETX>

Two-tone suppression in a locally active nonlinear model of the cochlea.

In auditory nerve, inner-hair cell and basilar-membrane responses, it has been found that the response to one tone can be suppressed by another tone. This phenomenon, called two-tone suppression, is examined on the level of the basilar membrane with a locally active long-wave model of the cochlea in which the active mechanism is nonlinear. The model is solved in the frequency domain by means of a quasi-linear solution method. Several phenomena, such as difference in growth of suppression for low-side and high-side suppressors and critical dependence of the phase of the probe response on suppressor parameters, have been replicated. The attenuation hypothesis which states that the presence of a suppressor has the same effect on the probe response as attenuation of probe level is shown to be insufficient in explaining the experimental data. This model, in which suppression is simply reduction of power amplification due to saturation of the active mechanism, is more successful in this respect.

Representation of acoustic signals in the eighth nerve of the Tokay gecko: I. Pure tones

A systematic study of the encoding properties of 146 auditory nerve fibers in the Tokay gecko ( Gekko gecko, L) was conducted with respect to pure tones and two-tone rate suppression. Our aim was a comprehensive understanding of the peripheral encoding of simple tonal stimuli and their representation by temporal synchronization and spike rate codes as a prelude to subsequent studies of more complex signals. Auditory nerve fibers in the Tokay gecko have asymmetrical, V-shaped excitatory tuning curves with best excitatory frequencies that range from 200–5100 Hz and thresholds between 4–35 dB SPL. A low-frequency excitatory ‘tail’ extends far into the low-frequency range and two-tone suppression is present only on the high frequency side of the tuning curve. The response properties to pure tones at different loci within a tuning curve can differ greatly, due to evident interactions between the representations of temporal, spectral and intensity stimulus features. For frequencies below 1250 Hz, pure tones are encoded by both temporal synchronization and spike rate codes, whereas above this frequency a fiber's ability to encode the waveform periodicity is lost and only a rate code predominates. These complimentary representations within a tuning curve raise fundamental issues which need to be addressed in interpreting how more complex, bioacoustic communication signals are represented in the peripheral and central auditory system. And since auditory nerve fibers in the Tokay gecko exhibit tonal sensitivity, selective frequency tuning, and iso-intensity and iso-frequency contours that seem comparable to similar measures in birds and mammals, these issues likely apply to most higher vertebrates in general. The simpler wiring diagram of the reptilian auditory system, coupled with the Tokay gecko's remarkable vocalizations, make this animal a good evolutionary model in which to experimentally explore the encoding of more complex sounds of communicative significance.

Responses of peripheral auditory neurons to two-tone stimuli during development: II. Factors related to neural responsiveness

In an accompanying paper (Fitzakerley et al., 1994), it was demonstrated that there is a significant developmental correlation between the appearance of tuning and two-tone suppression. However, it was also found that some sharply tuned neurons meeting minimal adult standards did not exhibit suppression. Therefore, in order to investigate other factors that may be related to the demonstration of suppression in peripheral auditory neurons, the relationship of two-tone suppression with various parameters related to neural responsiveness was studied in perinatal kittens. A positive correlation was made between the observance of suppression and driven discharge rate, characteristic frequency (CF), and threshold, all properties which change significantly during the final stages of cochlear differentiation. In older animals, suppression was also observed in higher percentages of neurons having low spontaneous rates ( < 1 spk/s). Suppression was evoked less often by test tones placed below CF than above CF in neurons recorded from younger animals, and was generally produced by a narrower range of test tone intensities than those recorded from adults. As a result, the conventional description of suppression as observed in peripheral auditory neurons in mature animals must be extended to include these factors when responses of immature neurons are considered.

Responses of peripheral auditory neurons to two-tone stimuli during development: III. Rate facilitation

Approximately 25% of peripheral auditory neurons having low characteristic frequencies (CFs) and broad tuning, and recorded from immature animals, responded to two-tone stimuli with increases in discharge rate greater than predicted by linear summation of the responses to probe tones (facilitation), in contrast to the two-tone suppression observed in adult animals and in more sharply tuned immature neurons. Facilitation was not seen after 81 gestational days and was not observed when test tones produced a substantial increase in rate when presented alone. The fact that some neural responses were facilitated under conditions of two-tone stimulation during the final stages of cochlear differentiation provides additional evidence that signal transduction is fundamentally different in neonatal kittens than in adults. A linear model of basilar membrane mechanics coupled to nonlinear neural processes is proposed which can account for the production of facilitation.

Individual, sex, and ear differences in measures of overshoot and psychophysical two-tone suppression

Notched-noise overshoot and two-tone suppression were measured at 1000 Hz using standard procedures in 40 normal-hearing, psychoacoustically naive adults, counterbalanced for sex and listening ear. The threshold variability across listeners for the same condition often exceeded 30 dB. In the overshoot conditions, the signal was an average of 7 dB harder to detect when it was presented at the onset of a 500-ms masker (masker notch width: 1000 Hz) than when signal onset was delayed by 400 ms. Across listeners, this overshoot effect ranged from 1 to 17 dB. In the suppression conditions, for some listeners, the forward-masked signal was as much as 15 dB easier to detect when the tonal on-frequency masker (1000 Hz) and suppressor (1150 Hz) were presented together, than when the masker was presented alone, indicating suppression. For other listeners, however, presenting the masker and suppressor together increased thresholds by as much as 13 dB, indicating additional masking (negative suppression). The average amount of suppression was −1.0 dB. ANOVA tests shoed significantly more overshoot and less suppression in females than males, and significantly higher thresholds in left than right ears in the overshoot conditions. Results will be discussed in terms of possible individual, sex, and ear differences in efferent inhibition. [Work supported by NIH.]

Stimulus biasing: A comparison between cochlear hair cell and organ of corti response patterns

Responses from the organ of Corti (OC) fluid space and from individual hair cells are collected for short duration tone pips measured alone and in the presence of a 20 Hz bias tone. Because of the relatively long period of the acoustic bias signal, a probe can be selectively placed at precise locations within a single response period. Since bias effects produced during maximum basilar membrane velocity are negligible, this report documents changes associated with basilar membrane displacements to scala vestibuli and scala tympani. Hair cell response patterns are compared with those measured nearby in the OC to determine the degree to which inner (IHC) and outer hair cells (OHC) contribute to the gross cochlear potentials. It is shown that intracellular OHC and OC dc responses are strongly influenced by the bias while intracellular IHC dc responses are minimally affected. Although an association has been established between the cochlear microphonic and outer hair cell ac receptor potentials, the well correlated changes in the outer hair cell dc receptor potential and the organ of Corti summating potential suggest that gross cochlear potentials reflect dc as well as ac contributions from nearby OHCs. Since IHC responses are not influenced by the bias, they appear to contribute less than OHCs to extracellular potentials. These conclusions, however, are restricted to the moderately high input levels required to produce these effects (Durrant and Dallos, 1974) and to the central region of the cochlea where the recordings are made. Finally, the degree to which bias effects are contaminated by two-tone suppression is discussed.

Comparative analysis of spectro-temporal receptive fields, reverse correlation functions, and frequency tuning curves of auditory-nerve fibers.

The tuning properties of single auditory-nerve fibers (ANFs) are characterized with spectro-temporal receptive fields (STRFs), reverse correlation functions (revcors), and frequency tuning curves (FTCs). Measures of tuning and latency from the STRFs and revcors are largely comparable to the traditional measures of tuning from FTCs and measures of latency from peristimulus time histograms (PSTHs), but several important differences are found. As is well known, revcors can only characterize low (< 6 kHz) best frequency (BF) units, whereas STRFs are able to characterize all units studied (BFs ranging from 0.26-23 kHz), except for a few very low-BF examples. Whereas tuning bandwidth derived from revcor exceeds that measured from FTCs at all BFs and increases with sound level. STRF bandwidth is comparable to FTC bandwidth, except at low BFs, and is stable with sound level. The STRF may reflect nonlinear properties of auditory-nerve fibers such as refractoriness and two-tone suppression that are absent in the FTC and revcor characterizations. The principal drawback of the STRF is its narrow dynamic range.

Response to ‘‘Comment on ‘Two-tone suppression of inner hair cell and basilar membrane responses in the guinea pig’ ’’ [J. Acoust. Soc. Am. 94, 3509–3510 (1993)

This letter provides additional data concerning the nature of two-tone suppression when an above characteristic frequency (CF) tone suppresses the responses of hair cells (in the basal turn of the cochlea) stimulated by lower than characteristic frequency tones. It is shown that the phase of the ac receptor potential of the below CF probe tone undergoes a phase lag during suppression. This is the opposite direction from that which would occur during attenuation of the probe. These data are consistent with the changes that have been reported [Cheatham and Dallos, J. Acoust. Soc. Am. 94 (1993)] in turns two and three of the guinea pig cochlea. Other additional data are provided showing that the phase change of a probe tone having a frequency higher than CF is a function of whether the high-side supressor is excitatory or nonexcitatory for the hair cell. Nonexcitatory high-side suppression is attenuation-like, whereas the mutual suppression of two (close in frequency) excitatory tones are not like attenuation.

Adaptation of suppression as an explanation of enhancement effectsa)

Delaying the onset of a signal relative to the onset of a simultaneous notched masker often improves the ability of subjects to "hear out" the signal at both threshold and suprathreshold levels. Viemeister and Bacon [J. Acoust. Soc. Am. 71, 1502-1507 (1982)] suggested that such signal-enhancement effects might be attributable to adaptation of the suppression directed from the masker to the signal, thereby releasing the signal from suppression. In support of their hypothesis, Viemeister and Bacon reported that a masker, preceded by an enhancer having no component at the signal frequency, produced more forward masking than did the masker by itself. Here the masker enhancement described by Viemeister and Bacon, signal enhancement, and two-tone suppression were measured in the same six subjects. Parametric manipulations of the masker-enhancement stimulus produced results similar to those previously reported for parallel investigations of signal enhancement, indicating that the two types of enhancement are closely related effects. Although the present data reveal an inverse relationship between the amounts of suppression and enhancement, suggesting that the two processes may be interrelated, no support was obtained for the hypothesis that adaptation of suppression can account for enhancement.

The pathophysiology of presbyacusis: Does the aging cochlea need a jump start?

The Mongolian gerbil is used as an animal model to study the pathophysiology underlying presbyacusis. Gerbils are raised from birth in a quiet vivarium or are exposed to a long-duration wideband noise (0.5–4.0 kHz for 1–2 years at 85 dB SPL) at some time during their life. Quiet-aged ears have thresholds that are increased somewhat, especially above 4 kHz, but nonlinearities such as otoacoustic emissions and two-tone suppression are present and are largely unaffected by the aging process. Morphologically, hair cells in quiet-aged animals are highly conserved, whereas the lateral wall system degenerates, resulting in a decreased endocochlear potential (EP). Current injection to bolster the EP in these quiet-aged ears can enhance the response to low- and high-level stimuli. Noise-aged ears, while also showing increased thresholds, can be differentiated from their quiet-aged counterparts by a lack of nonlinear phenomena. Two-tone suppression is absent as are otoacoustic emissions. Thus, aging in quiet or in noise can have very different outcomes with regard to overall peripheral function, even when the respective audibility curves are similar. [Work supported by NIH P01 DC00422.]

Two-tone suppression and distortion production on the basilar membrane in the hook region of cat and guinea pig cochleae

Two-tone suppression and two-tone distortion were investigated at the level of the basilar membrane in the hook region of cat and guinea pig cochleae using a displacement-sensitive laser interferometric measurement system. The system allowed measurements to be performed at physiological stimulus levels in the cochlear region tuned to 30–35 kHz in cat and 29 kHz in guinea pig. The amplitude of vibration of the basilar membrane due to a probe tone at the characteristic frequency (CF) was attenuated during the presentation of a simultaneous suppressor tone either above or below CF. The amount of suppression depended on the intensities of both probe and suppressor, and the relationship of the suppressor frequency to the CF. Suppressors at frequencies more than an octave below the CF attenuated the responses to the CF probe at a rate of up to 1 dB/dB, with little variation based on suppressor frequency. As the suppressor frequency was increased above CF the rate of suppression decreased rapidly. The lowest suppressor intensity at which attenuation of the probe response was observed did not vary in direct proportion to the probe intensity. This suppression threshold often varied only a few dB SPL when the probe was varied over a 20 dB SPL range. In a few instances the rate of attenuation was as much as a factor of two greater at the lowest probe intensities than at higher intensities. It is noteworthy that suppression was found when the frequency of the suppressor was either above or below CF in the same preparation. Low frequency suppressor tones suppress basilar membrane motion at the CF when the basilar membrane undergoes displacement toward either scala. The maximum suppression occurs around 100 /gms after the peak excursions caused by the low frequency biasing tone. Two-tone distortion products were often observed even at stimulus levels below those causing two-tone suppression at the site studied. The cubic difference tone (CDT) was the most prominent of the distortion products. The level of the CDT component varied nonmonotonically with the level of either of the primary tones. Responses at the difference frequency between the two primaries were usually below the noise floor of the recording system. The existence of both two-tone distortion and two-tone suppression was dependent on the presence of a cochlear nonlinearity.

Two-tone suppression of inner hair cell and basilar membrane responses in the guinea pig

Recordings of receptor potentials from inner hair cells (IHCs) and the basilar membrane (BM) motion were made in pigmented guinea pigs. The acoustic stimuli were single tones near best frequency (BF) and two-tone complexes. Single tone input/output (I/O) functions had a saturating growth for the magnitude and their phase shifts were strongly dependent on the tone frequency relative to BF. For IHCs, a BF tone stimulus produced no phase shift in the ac receptor potential response. Phase lag or lead occurred for tones below or above BF, respectively. BM velocity I/O functions were not as compressively saturating as IHC ac I/O curves. BM phase shifts (in relation to BF) were similar to those of the IHCs. Two-tone suppression was observed in both IHC and BM response measures. Suppressor tones on the low-frequency side of BF produced complex suppression results, which were inconsistent with a simple attenuation model for suppression. The growth of suppression was faster than the attenuation from equivalent level reductions of the probe tone, and phase shifts were phase lead. Depending upon experimental conditions, phase change with suppression may be in the opposite direction from phase change observed from pure attenuation of the probe tone. High-frequency suppressors (relative to BF) are consistent with an attenuation model of suppression for the IHCs of the current study. High side suppression of basilar membrane velocity, however, differed from the IHCs in a systematic way. The phase change caused by suppression of BM velocity was always smaller than that of an equivalent reduction in the probe tone level.

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. This observation indicates that the influence of the suppressor tone on subsequent sensitivity to CF can occur with or without the simultaneous presentation of the CF tone.

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.

Additivity of threshold elevations produced by disruption of outer hair cell function

We present a simple model describing the additivity of hearing loss in the mammalian cochlea produced by disruption of the outer hair cell transduction processes. The validity of this model has been tested experimentally in the guinea-pig by inducing threshold elevations using two simultaneous cochlear manipulations, including acoustic overstimulation, two-tone suppression, low-frequency acoustic biasing of the cochlear partition and electrical stimulation of the medial olivo-cochlear system of efferent fibres. The results of these experiments suggest that the model presented is an adequate description, within the measurement error of our experiments, of the hearing losses produced.

Effects of OFF-BF tones on responses of chopper units in ventral cochlear nucleus. I. Regularity and temporal adaptation patterns.

1. We have recorded the responses of neurons in the anteroventral cochlear nucleus (AVCN) of barbiturate-anesthetized cats to pure tones [either at the unit's best frequency (BF) or at another frequency (OFF-BF)] and to two-tone combination stimuli. 2. The effects of OFF-BF input (either alone or presented simultaneously with a BF tone in a two-tone stimulus) on the response patterns of choppers may include not only rate inhibition but changes in the discharge regularity and the temporal adaptation properties of the spike trains. 3. In the majority of cases we studied (119 of 146 frequencies examined in 45 units), the discharge regularity of a response to an OFF-BF or two-tone stimulus is comparable with that of a "rate-matched" BF tone response. In a minority of cases (27 of 146 frequencies examined), however, OFF-BF input (either alone or in a two-tone stimulus format) changed the regularity compared with that of a rate-matched BF tone response. 4. In the majority of cases studied (139 of 171 frequencies examined in 53 units), the initial pattern of rate adaptation ["temporal adaptation pattern" (TAP)] was the same in response to a short tone burst at BF, to an OFF-BF tone burst, or to a pair of tones. The TAP can, however, be significantly altered by OFF-BF input, although this is a comparatively infrequent occurrence in our data sample (32 of 171 frequencies examined), from the response to BF tone to the response to the two-tone or OFF-BF stimulus, are as follows: sustained to slowly adapting; slowly adapting to transiently adapting, and transiently adapting to slowly adapting. Changes in the TAPs of chopper unit responses have been recorded from both regular and irregular choppers and cannot be accounted for on the basis of changes in sustained firing rate. These changes in the discharge regularity and TAP in the small minority of cases suggest that (at least in these cases) the inhibitory effect of OFF-BF input is not simply the result of two-tone suppression at the level of the auditory nerve fiber input. 5. We have observed that regular choppers may be transformed into irregular choppers by OFF-BF (rate inhibitory) input.(ABSTRACT TRUNCATED AT 400 WORDS)

Evidence that adaptation of suppression cannot account for auditory enhancement or enhanced forward masking.

Delaying the onset of a signal relative to the onset of a simultaneous notched masker often improves the ability of listeners to 'hear out' the signal at both threshold and suprathreshold levels. Viemeister & Bacon (J. acoust. Soc. Am., 71, 1502-1507 (1982)) suggested that such auditory enhancement effects could be accounted for if the suppression produced by the masker on the signal frequency adapted, thereby releasing the signal from suppression. In support of their hypothesis, Viemeister & Bacon reported that a masker preceded by an enhancer having no component at the signal frequency produced more forward masking than did the masker by itself. Here evidence is provided from five new experiments showing that adaptation of psychophysical two-tone suppression is inadequate to account either for auditory enhancement effects or for the enhanced forward masking demonstrated by Viemeister & Bacon.

Basilar membrane responses to two-tone and broadband stimuli.

The responses to sound of mammalian cochlear neurons exhibit many nonlinearities, some of which (such as two-tone rate suppression and intermodulation distortion) are highly frequency specific, being strongly tuned to the characteristic frequency (CF) of the neuron. With the goal of establishing the cochlear origin of these auditory-nerve nonlinearities, mechanical responses to clicks and to pairs of tones were studied in relatively healthy chinchilla cochleae at a basal site of the basilar membrane with CF of 8-10 kHz. Responses were also obtained in cochleae in which hair cell receptor potentials were reduced by systemic furosemide injection. Vibrations were recorded using either the Mössbauer technique or laser Doppler-shift velocimetry. Responses to tone pairs contained intermodulation distortion products whose magnitudes as a function of stimulus frequency and intensity were comparable to those of distortion products in cochlear afferent responses. Responses to CF tones could be selectively suppressed by tones with frequency either higher or lower than CF; in most respects, mechanical two-tone suppression resembled rate suppression in cochlear afferents. Responses to clicks displayed a CF-specific compressive nonlinearity, similar to that present in responses to single tones, which could be profoundly and selectively reduced by furosemide. The present findings firmly support the hypothesis that all CF-specific nonlinearities present in the auditory nerve originate in analogous phenomena of basilar membrane vibration. However, because of their lability, it is almost certain that the mechanical nonlinearities themselves originate in outer hair cells.