Two-tone Suppression Research Articles

Two-tone suppression in inner hair cell responses: Correlates of rate suppression in the auditory nerve

Inner hair cell (IHC) recordings were made from second turn of the guinea pig cochlea where characteristic frequencies are approximately 4000 Hz. In order to compare IHC responses with rate suppression measured in the auditory nerve, suppressors were introduced that produced little or no response in the hair cell. The effects of a variable-frequency suppressor on a constant-frequency probe, placed near characteristic frequency, were also investigated since this paradigm is commonly used in single unit experiments. Resulting magnitude changes were measured in the fundamental component of the ac receptor potential and/or in the total de produced in the region of temporal overlap between the two stimulus inputs. This latter component is escecially important when considering how changes in IHC responses relate to decreases in discharge rate in single auditorynnerve fibers. Since the ac receptor potential is filtered by the hair cell's basolateral membrane, the dc component probably controls transmitter release at the characteristic frequency of these second-turn IHCs. Based on results from these and previous experiments, a proposal is advanced to explain the evolution of two-tone suppression in the peripheral auditory system. The paper also discusses the use of excitatory versus non-excitatory suppressors and includes a description of two-tone suppression areas at the mechanical, IHC and single unit levels. The explanation of low-side suppression areas is of special interest since hitherto they have been difficult to model (Kim, 1985).

Physiological correlates of off-frequency listening

Recordings are made from inner hair cells (IHC) in the second turn of the guinea pig cochlea where characteristics frequencies (CF) are approximately 4000 Hz. Results from experiments using two stimulus inputs suggest that the characterization of two-tone suppression at this more-basal recording location is similar to that reported for IHCs in the third cochlear turn (Cheatham and Dallos, 1989, 1990a, 1990b). For example, introduction of a suppressor causes IHC frequency response functions to become narrower with the smallest magnitude reductions occurring between 1 2 to 1 octave below CF. In this frequency region, where suppression is minimal, it was also observed that suppressor magnitude was reduced by the probe. In other words, the mutual suppression of probe and suppressor may contribute to the sharpening of these functions. Since the peak of the frequency response function shifts to a lower frequency in the presence of the suppressor, these results may provide a physiological correlate of the psychophysical phenomenon known as ‘off-frequency listening’.

Activity patterns of primary auditory-nerve fibres in chickens: Development of fundamental properties

We have examined the activity patterns of single auditory-nerve fibres in the chicken and tested for possible changes during post-hatching development. For this purpose, we recorded from fibres in the cochlear ganglion of chickens of two age groups (about P2 and P21) and investigated their spontaneous and sound-evoked activity patterns under nembutal-chloralhydrate anaesthesia. The spontaneous activity of primary auditory neurones was irregular, the average rates were between 20.5 (P2) and 23 (P21) spikes/s. Many low-frequency fibres from both age groups showed preferred intervals in their spontaneous activity. Tuning characteristics, including the range of characteristic frequencies, the presence of primary and two-tone suppression, the slopes of tuning-curve flanks and Q 10 dB values were similar to those previously reported for the starling and were statistically indistinguishable between the two age groups. However, there was a difference in fibre thresholds at the highest frequencies. Systematic differences were also present between the two age groups with regard to some characteristics of the rate-intensity functions. These data indicate that whereas the tuning properties of primary auditory fibres of the chicken cochlea are mature as early as post-hatching day 2, the intensity functions are not.

Auditory nerve of the normal and jaundiced rat. II. Frequency selectivity and two-tone rate suppression

This study is the continuation of the functional probing of the auditory periphery in the normal and jaundiced rat. Threshold tuning curves from normal rat auditory nerve fibers were comparable to those reported in other mammals. Life-long unconjugated hyperbilirubinemia does not appear to have a widespread, demonstrable effect on cochlear frequency selectivity and sensitivity as measured by the shapes of FTCs of single auditory nerve fibers. Most fibers from the jj Gunn rats had threshold tuning curves as sharp as those from control animals (Jj Gunn and Long-Evans). Any difference seems to lie in a greater threshold variability, particularly for the high-SR fibers, for the Gunn rat strain. Two-tone rate suppression, particularly above CF, was detected in most fibers from the three groups of rats. The optimal suppression frequency (SF) as a function of CF displayed the same progression. Suppression thresholds at any given CF were generally higher for high-SR fibers than for low-SR fibers for all three groups of animals.

A computational model of afferent neural activity from the cochlea to the dorsal acoustic stria

The first comprehensive computational model of the precortical mammalian auditory system to include afferent neural processing up to the level of the dorsal acoustic stria (DAS) is described. The model consists of two scissile stages simulating (1) the cochlea and auditory nerve (AN) and (2) the dorsal cochlear nucleus (DCN). The model derives its input from a 128-channel cochlear filterbank. Cochlear transduction, rectification, logarithmic compression, and two-tone suppression functions are performed at the first stage of the simulation. The 512 artificial neurons employed model the cell at the level of transmembrane potential and have interconnections that follow closely those reported in recent anatomical and physiological studies of the cat AN and DCN. The responses of the model to pure-tone stimuli (at various sound-pressure levels) and noise stimuli (at various levels and bandwidths) are reported in detail and compare well with published results. The model is being used to investigate the representation of initial English stop consonants (differing in voice-onset time) in the DAS; this work is briefly described.

Two-tone interaction in phase locking of cat cochlear nerve fibers.

Discharges in response to a combination of a best frequency (BF) tone and another harmonically unrelated frequency (F2) tone were recorded from single cochlear nerve fibers of cats. The effects of the F2 tone on discharge distribution within a BF period were analyzed. When F2 was close to BF, the F2 tone disturbed phase-locked firing to a BF tone without reduction of discharge rate. Phase locking to the BF tone was disturbed very little when F2 was far from BF and at the boundary of the response area, although discharge rate was reduced seriously by the “two-tone suppression.” The respective contributions of the BF and F2 tones to discharge elicitation were evaluated and it was concluded that when F2 is close to BF, serious disturbance in phase locking to the BF tone results mainly from the nonlinearity in the transduction process at the receptor site. Conversely, marked reduction in discharge rate by an F2 tone far from BF is mainly due to mechanical nonlinearity in the basilar membrane vibration.

Comparison of low- and high-side two-tone suppression in inner hair cell and organ of corti responses

Two-tone interactions were measured from inner hair cells and from the organ of Corti fluid space in the third turn of the guinea pig cochlea. At relatively low stimulus levels, a low-side suppressor caused frequency response functions to become broader. Phase changes exhibited a lag/lead transition around the characteristic frequency in harmony with the change in magnitude. These patterns are similar to those previously documented for a high-side suppressor (Cheatham and Dallos 1989) and suggest that suppression is not simply an attenuation phenomenon since level reductions for single-tone inputs produce response patterns which are mirror images of those obtained for the two-tone conditions. In contrast to the low-level results, data measured at moderately high stimulus levels indicate that the magnitude changes produced by both low- and high-side suppressors are qualitatively similar to changes generated by reducing the input sound level. In other words, ac frequency response functions become narrower, partially reversing the broadening of these functions which occurs as sound level increases. Companion phase measures, however, demonstrate that lowand high-side suppressors, in spite of producing similar changes in filter shape, do not produce similar changes in response phase. In fact, neither of the two-tone conditions produce response patterns similar to the one associated with reducing the input sound level.

Two-tone rate suppression in auditory-nerve fibers: Dependence on suppressor frequency and level

The growth of two-tone rate suppression with suppressor level was studied for auditory-nerve fibers in anesthetized cats. The level of a tone at the characteristic frequency (CF) was adjusted by an adaptive procedure (PEST) so that, when presented with a suppressor tone, the CF tone would produce a criterion discharge rate. Suppression (in dB) was defined as the CF-tone level that met criterion in the presence of a suppressor minus the level that met criterion in quiet. The growth of suppression with suppressor level was well characterized by a straight line whose slope (in dB-excitor/dB-suppressor) varied with suppressor frequency by as much as a factor of 10 in the same fiber. These slope differences were systematically related to the position of the suppressor frequency relative to the fiber CF: for below-CF suppressors, slopes ranged from 1 to 3 dB/dB, while, for above-CF suppressors, they were between 0.15 and 0.7 dB/dB. Slopes decreased rapidly with increasing suppressor frequency near the CF, but, for frequencies well below the CF, the slope reached a maximum that increased gradually with CF. These results resemble psychophysical data on the growth of masking and psychophysical suppression and pose difficulties for existing models of two-tone suppression.

Tuning and suppression in auditory nerve fibers of aged gerbils raised in quiet or noise

Mongolian gerbils were reared either in quiet or in a continuous noise field (85 dBA, 500–4000 Hz). The gerbils began the noise exposure at 8 months of age and, after the exposure, spent the remainder of their lives in the quiet vivarium with the quiet-aged group. The duration of the noise exposure was between 365 and 724 days. At the terminal experiment the ages of the animals varied between 24 and 43 months, with a mean age of about 36 months, an age representing the average life span of a gerbil in our colony. During the terminal experiment, tuning curves and boundaries of two-tone rate suppression were obtained from single fibers in the auditory nerve. Threshold shifts occurred in both groups of animals. The shift was largely confined to the tip of the tuning curve; i.e., the region around the characteristic frequency (CF) of the fiber. The CF shifts effectively reduced the tip-to-tail ratios of the tuning curves. Two-tone suppression areas above and below CF were present for all fibers in the quiet-aged animals, but were often absent for fibers in the noise-aged group. The presence of suppression was largely independent of fiber thresholds in both groups of animals. Indeed, fibers were found with clearly-defined suppression boundaries above and below CF despite threshold shifts of up to 60 dB. Moreover, in the noise-aged group suppression below CF was sometimes found without concomitant suppression above CF and vice versa, suggesting an independence between the two suppression areas. For fibers with CFs within the bandwidth of the noise, two-tone suppression above CF was always absent, even though suppression below CF was sometimes present. In sum, two-tone suppression was near normal in ears aged in quiet despite relatively large threshold shifts at the fiber CF. However, suppression, especially that above CF, was vulnerable to the effects of chronic noise. Taken with the results of other studies, our data suggest that the micromechanics of the cochlea are largely responsible for two-tone suppression, especially that above CF, and that different mechanisms may underlie suppression above and below CF.

Physiological models of masking and speech processing

Auditory models might be applied to speech coding either as objective evaluation measures, or as coder stages in coder/decoder systems. Both applications are based on the premise that these models accurately represent all the information that is relevant to auditory perception. In this talk, two fundamental problems that need to be worked out in order to make auditory models practically useful in speech coding are identified: the choice of a distance measure for comparing model outputs, and the design of the decoder. These ideas are illustrated using a model of peripheral auditory processing that is based on physiological recordings from auditory-nerve fibers, and predicts psychophysical performance in masking and discrimination for a variety of stimulus conditions. In this model, intensity difference limens in restricted regions of the frequency spectrum depend on overall spectral shape and sound level, so that the coding accuracy in different frequency bands would have to vary with time. Model outputs will be compared for natural and coded speech, and the role of nonlinear phenomena in the inner ear (such as two-tone suppression ) will be discussed. [Work supported by NIH Grant NS13126.]

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: 1. (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; 2. (ii) that SP suppression occurs at approximately constant basilar membrane displacement, inferred from the SP iso-response contours; and that 3. (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.

Inner hair cell responses to the 2f1-f2 intermodulation distortion product

Recordings of dc and ac receptor potentials from pigmented guinea pig inner hair cells indicate strong responses to the 2f1-f2 intermodulation tone when f1 and f2 are greater than the hair cell characteristic frequency and do not cause a response when given individually. The effective magnitude of this cubic distortion product (CDP) was about 25-30 dB below equal sound level primaries over a 20-30-dB range of their sound levels. The relative strength of the CDP declined at a rate greater than 180-dB/oct separation of the primaries. When magnitude of f1 or f2 was held constant, the growth of CDP was nonmonotonic, exhibiting a distinct maximum. With a constant level of f1 or f2, optimal CDP was produced when the level of f2 was 10-15 dB greater than f1. Strong two-tone suppression from the primaries has a role in shaping the CDP growth. The ac receptor potentials of the CDP show a 150 degrees-200 degrees phase shift when the primaries are increased over a 50-dB range. These results support the hypothesis of a propagated CDP in the cochlea and are consistent with the major features of related studies of human psychoacoustic experiments, afferent nerve neural rate functions, and ear canal distortion products.

Two-tone interactions in inner hair cell receptor potentials: AC versus DV effects

Two-tone suppression was studied in both ac and dc receptor potentials recorded from inner hair cells in the third turn of the guinea pig cochlea. Frequency response functions for the ac component obtained at moderate intensities indicate that frequency selectivity is enhanced when a high-side suppressor is added to the stimulus. This occurs because the largest reductions in magnitude take place well above and below the characteristic frequency (CF) of the cell. Changes near CF are relatively small. In contrast, frequency response functions for the dc receptor potential become broader in the presence of an excitatory suppressor. The significance of these findings for the processing of complex stimuli is considered.

The Auditory Behaviour of Flying Locusts

ABSTRACT The auditory behaviour of tethered locusts flying in a wind tunnel was investigated under controlled acoustic conditions. Reflection, attenuation and diffraction of ultrasound evoked by the locust’s physical presence caused pronounced distortions of the acoustic field. Interaural pressure variations were observed that account for directional hearing at high frequencies. Sound field measurements indicated only a minor influence of flight posture or wing position on the interaural pressure gradient. The locusts steered away from pulsed ultrasounds that simulated bat echolocation signals. The phonotactic response was measured as ruddering by the abdomen and hind legs, resulting in a yaw torque directed away from the sound source. Wingbeat frequency increased by 15% in response to ultrasonic stimulation. This behaviour is considered to be analogous to the bat avoidance behaviour of flying crickets. The avoidance response was observed for carrier frequencies higher than 10 kHz and for sound pressure levels (on average) higher than 45 dB SPL. Low-frequency stimuli (<10kHz) failed to elicit any phonotactic steering at any intensity used (up to 100dB SPL). Because of its relatively low threshold of reaction, this steering behaviour is thought to be part of an early-warning system adapted to the acoustic detection of echolocating predators. The avoidance response was suppressed when a 30 kHz (normally effective) tone was combined with a 5 kHz tone (which is ineffective alone). Two-tone suppression only occurred when the low-frequency component was 10–15 dB SPL higher than the high-frequency tone. The biological significance of two-tone suppression is discussed. The intensity-response characteristics, the frequency sensitivity and the two-tone suppression of the avoidance behaviour are discussed with respect to the auditory physiology of Locusta migratoria. The involvement of some identified auditory ascending interneurones in the avoidance behaviour is considered.

Outer hair cell receptor current and sensorineural hearing loss

It is argued in this paper that many nonlinear phenomena in audition and many types of sensorineural hearing loss can be explained by a disruption of the mechano-electrical transduction process at the apex of the outer hair cells. This is done using experimental data and a simple model of the active role of outer hair cells in cochlear mechanics based on our previous experiments with acoustic trauma. The causes of sensorineural loss addressed include acoustic trauma, aminoglycoside ototoxicity, intoxication with loop diuretics, hypoxia and Meniere's disease. The nonlinear phenomena discussed include loudness compression, two-tone suppression and modulation of cochlear sensitivity by very low-frequency tones. In every case considered the reduction in neural sensitivity was related to the reduction in outer hair cell receptor current in a quantitatively similar way. We conclude that the link is causal.

Lower boundaries of two-tone suppression regions in the guinea pig

Lower boundaries of two-tone suppression regions were determined in single fibres of the guinea pig with a tracking algorithm as described by Schmiedt (1982). For a suppressee at CF having a level of 20 dB above the threshold of the tip, suppression at the high-frequency (hf) side of the FTC could almost always be found. With the method used, the percentage of fibres in which suppression could be found at the low-frequency (lf) side of the FTC decreased with decreasing CF. Moreover, the occurrence of lf-suppression decreased for lower suppressee levels for fibres with CF ≈ 2–5 kHz. For each fibre the minimum level difference between lf-suppression boundary and tip threshold was larger than 20 dB, for the whole group of fibres the difference was 34 dB on average. The hf-suppression regions sometimes reached below the tip for fibres with CFs in the 4 kHz region. The frequency at the lowest level of the hf-suppression boundary, best suppression frequency or BSF, is related to the CF as: BSF = 0.55 + 1.13 CF. When the suppressee level increased, the lower boundary at the hf side shifted upwards with a rate > 1 dB/dB. On the whole the two-tone suppression data in the guinea pig agree with those found in other rodents.

Auditory nerve rate-level functions for two-tone stimuli: Possible relation to basilar membrane nonlinearity

Rate versus level functions are presented for auditory-nerve fiber responses to best frequency (BF) tones presented alone and in the presence of a constant level suppressor tone. The paper focuses on units with sloping saturation rate functions for BF tones presented alone. Two-tone rate functions are generally parallel to BF functions at firing rates below those in the sloping saturation region of the BF function. At rates in the sloping saturation range the two-tone function grows with a greater slope than that of the BF function until the two functions meet. This result is discussed in terms of current knowledge of two-tone suppression on the basilar membrane.

Inner hair cell responses to tonal stimulation in the presence of broadband noise.

The effects of broadband noise (BBN) on the tone-evoked de receptor potential from inner hair cells of guinea pigs were measured. The effects of the noise were: suppression of the receptor potential, no net change, or greater depolarization relative to the tone alone, evoked receptor potential. The effects appear to be consistent with a two-tone suppression hypothesis. The time course of the suppression effect is immediate and constant in time. This observation suggests no obvious involvement of a local feedback loop in outer hair cells or one depending on the efferent nerves. Inner hair cell "sensitivity" is a variable in the magnitude of the suppression. Comparison of masked, tone-evoked de receptor potential intensity functions to responses from auditory-nerve fibers (taken from the literature for experiments using a similar paradigm) differentiates the phenomena of suppression and adaptation in the auditory periphery.

Two-tone suppression in inner hair cell responses

In an attempt to characterize certain aspects of two-tone suppression (2TS), ac receptor potentials were recorded from mammalian inner hair cells (IHC) in the third turn of the guinea pig cochlea. By comparing magnitude and phase changes occurring during suppression with predictions made on the basis of level-dependent responses to single-tone inputs, it is possible to determine whether 2TS is mimicked by simply attenuating stimulus intensity. Results indicate that the effects of suppression are not simulated by simple input attenuation for low probe levels which produce responses below saturation. In these situations, the suppressor causes a decrease in the magnitude of the ac receptor potential with the largest deviations measured at the characteristic frequency (CF) of the cell. Thus, frequency response functions become broader. Response phase goes through a lag/lead transition at CF, also opposite to the results expected by simply decreasing input to the cell. At higher probe levels, within the saturation region, the magnitude reductions produced during 2TS are largest for stimulus frequencies well below and well above CF. This effect partially reverses the broadening of frequency response functions seen at moderate intensities with possible benefits for the processing of complex stimuli at conversational levels. Although the magnitude data obtained at high probe levels are consistent with the attenuation hypothesis, the companion phase measures did not show the expected lead/lag transition through CF since phase changes were generally lags. Consequently, the high-level suppression data suggest that 2TS may reduce input to the IHC but in a way which is not equivalent to the attenuation of a single-input stimulus.

Contribution of GABAergic inhibition to the response characteristics of auditory units in the avian forebrain.

1. We tested the contribution of GABAergic inhibition to the response characteristics of 213 neurons in the auditory telencephalon of chronically prepared nonanesthetized chickens. Extracellular recordings were obtained with multibarrel glass electrodes containing a tungsten wire. Auditory stimuli consisted of tones, two-tone combinations, and noise bursts presented either free field or via earphones. 2. Response properties of the neurons were studied both before and during iontophoretic application of GABA, glutamate, bicuculline methiodide (BIC), and acetylcholine. 3. During BIC application excitatory responses were facilitated. With the exception of transient off-responses, which occasionally appeared only in the BIC condition, the temporal response patterns to tone stimuli at the units' best frequency usually were unaltered. In no case was an inhibitory response component to binaurally presented pure tones antagonized by BIC. 4. BIC iontophoresis enlarged the isointensity-response areas of the vast majority of neurons in the structures of the auditory forebrain lying postsynaptic to the thalamorecipient layer L2. This effect was not obtained when neurons were depolarized to perithreshold levels with glutamate. 5. Two-tone stimulation resulted in a suppression of the excitatory response to a neuron's best frequency when the second frequency lay outside the excitatory response area. In lamina L2, the frequency range inducing two-tone suppression was narrow, and the suppressive effect was not antagonized by BIC. In the postsynaptic layers, frequencies up to three octaves from the neurons' best frequency induced two-tone suppression that was sensitive to BIC. In addition, these neurons also displayed a BIC-insensitive suppression similar to the one seen in layer L2. 6. Neurons displaying no or only a poor response to white-noise stimulation strongly responded to this wide-band stimulus during BIC iontophoresis. 7. Neurons without tone responses usually displayed clear response areas to tones during BIC application. Iontophoretic application of acetylcholine, but not glutamate, also induced such tone responses. Two-tone combinations with frequencies lying within the response areas observed in the BIC condition elicited excitatory responses after full recovery from the BIC application. 8. During BIC iontophoresis nonmonotonic intensity-response functions were converted to monotonic functions in most of the neurons studied. 9. A model of GABAergic inhibitory interactions is proposed that is based on two independent GABAergic systems.(ABSTRACT TRUNCATED AT 400 WORDS)