Relations between frequency selectivity and two-tone rate suppression in lizard cochlear-nerve fibers

Cochlear-nerve fibers innervating the apicial region of the alligator lizard basilar papilla show sharp frequency selectivity in response to single tones (measured with the frequency threshold contour, or FTC), and the phenomenon of two-tone rate suppression (TTRS) in response to two simultaneously presented tones (measured with the iso-TTRS contour, or ITC). The gross shapes of the FTCs, as characterized by the slopes of the sides and Q_10dB, vary systematically with the fiber's characteristic frequency (CF). ‘Fine-structural’ features are also found: below CF, notches (frequency regions of relatively high threshold) occur in the FTC at frequencies related to CF. Above CF, a break frequency, which varies with CF, divides the FTC into segments of different slope. Features of the ITC also vary with CF. The detailed shapes of the FTCs and ITCs are related: lobes of the ITC interdigitate with notches in the FTC; the side of the FTC with steepest slope is closely associated with the side of the ITC with steepest slope. The close relation that is observed between sharp frequency selectivity and TTRS suggests that both phenomena arise from a common cochlear mechanism.     

Responses of auditory nerve fibers to harmonic and mistuned complex tones

Responses of auditory nerve fibers were obtained to harmonic complex tones in which single components could be mistuned. Human listeners hear the harmonic tones as single sounds, but the same tones with one component mistuned are heard as two separate sounds. Fourier analysis of the temporal discharge patterns indicated that auditory nerve fibers typically responded to one or two stimulus components near the fibers' characteristic frequencies. At low stimulus levels, the discharge patterns could also exhibit low-frequency modulation that was produced by beating of two higher-frequency components. The same components were observed in the response spectra, whether those components were part of the original harmonic series or had been mistuned. The discharge patterns and response spectra were consistent with expectations based on previous studies of auditory nerve fibers with harmonic tones and other complex sounds. However, the discharge patterns differed dramatically from the discharge patterns elicited from inferior colliculus neurons by comparable stimuli.     

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.     

Time course of rate responses to two-tone stimuli in auditory nerve fibres in the guinea pig.

Peri-stimulus time histograms (PSTHs) were constructed from responses of auditory nerve fibres in anaesthetized guinea pigs. Acoustic stimuli consisted of pure tones, presented either as tone bursts, or in two-tone combinations in which a gated test tone was superimposed on a continuous excitatory tone at characteristic frequency (CF). The majority of the sample of fibres displayed two-tone rate suppression (2TRS). The suppression was either a monotonic or a non-monotonic function of the level of the superimposed test tone. Monotonic suppression of CF-driven rate occurred only for test tones at frequencies higher than CF, presented at levels up to the maximum available (approx. 100 dB SPL). For test tones below CF, 2TRS initially increased, then reverted towards excitation for higher levels of the test tone. Three levels were identified in non-monotonic, two-tone rate functions; (1) the threshold for rate suppression, (2) the maximally suppressing level and (3) the level (referred to as the balance point) at which average firing rate was restored to the background, CF-driven rate. PSTHs for two-tone responses obtained for test tone levels between the maximally-suppressing level and the balance point typically showed brief decrements (notches) in spike rate, at the onset and following the offset of the test tone. The latency, depth and duration of notches, however, depended on the level of the test tone, in a different manner for onset and offset. In some cases, without overt rate excitation above the probe-driven rate, the offset notch became more pronounced and of extended duration with increased level of the test tone, suggestive of adaptation to the test tone. Two-tone responses, in which rate exceeded the background, CF-driven rate, in general were preceded by a reduced onset notch and were followed by a longer-lasting depression of the background spike rate, typical of post-excitatory depression. Relative to responses obtained to the test tones presented alone, excitatory two-tone responses were of lower rate and were delayed by the onset notch. Onset notches sometimes preceded rate excitation in responses to single tones. Some features of the time course of rate suppression and excitation displayed in PSTHs for responses to one and two-tone stimuli seem inconsistent with current models of 2TRS.     

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.     

Masking and suppression in auditory nerve fibers of the goldfish, Carassius auratus.

The responses of single fibers of the auditory nerve of the goldfish (Carassius auratus) were recorded in response to two tones of different duration (20 ms 'signals' and 200 ms 'maskers') presented simultaneously or non-simultaneously. A single tone may produce excitation, adaptation, and suppression in auditory nerve fibers. For fibers with characteristic frequencies (CF) in the 200 to 400 Hz range, frequencies well above CF tend to produce suppression. If the net response to the masker tone is excitation, an added excitatory signal tone tends to increment the response in a way predictable from the rate-level function for the masker. A masker can attenuate the response to a signal as a result of a compressive and saturating response to the masker, and as a result of a low signal-to-masker ratio. If the net response to a masker tone is suppression, it effectively subtracts from signal excitation, causing 'suppressive masking.' In non-spontaneous fibers, suppression, additive excitatory effects, and adaptation can be revealed by responses to the signal in the absence of spike responses to the masker. In general, the ability of one tone (the masker) to reduce the response to a second tone (the signal) is greater in non-spontaneous fibers than in spontaneous fibers. These results also show that estimates of the frequency selectivity of many goldfish auditory nerve fibers will depend on whether the response of the fiber is defined by excitation, suppression, or both. The response of many fibers with CF in the 200-400 Hz region, as defined by excitation, can be masked or suppressed by a broad range of frequencies covering the effective hearing range of the goldfish.     

Tuning properties of turtle auditory nerve fibers: evidence for suppression and adaptation

Second-order reverse correlation (second-order Wiener-kernel analysis) was carried out between spike responses in single afferent units from the basilar papilla of the red-eared turtle and band limited white noise auditory stimuli. For units with best excitatory frequencies (BEFs) below approximately 500 Hz, the analysis revealed suppression similar to that observed previously in anuran amphibians. For units with higher BEFs, the analysis revealed dc response with narrow-band tuning centered about the BEF, combined with broad-band ac response at lower frequencies. For all units, the analysis revealed the relative timing and tuning of excitation and various forms of inhibitory or suppressive effects.     

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.     

Effects of intense pure tones on auditory temporal acuity

Gap detection thresholds (GDTs) were obtained from human listeners before and after exposure to a brief 0.4- or 1.7-kHz tone. The temporary threshold shift (TTS) produced 2 min after an exposure was approximately 10 dB. GDT stimuli were octave-band noises centered at one of three frequencies: the exposure frequency, one-half octave above the exposure frequency or one octave above the exposure frequency. GDTs were obtained at 35, 55, and 75 dB SPL at each center frequency. GDT and TTS recovery were monitored at logarithmically-spaced time intervals after the exposures. Following the 1.7-kHz exposure, shifts in post-exposure GDT were only obtained with the low-level stimulus conditions--the magnitude of GDT shift was correlated with the size of the TTS, and the shifts in GDT and absolute threshold required similar amounts of time to recover. Significant post-exposure shifts in GDT were also observed following the 0.4-kHz exposure. However, shifts were found at frequencies where there was no measurable TTS, and they required longer periods of time to recover than did absolute threshold.     

Characteristics of tone-pip response patterns in relationship to spontaneous rate in cat auditory nerve fibers

The responses of single auditory nerve (AN) fibers in the cat were recorded in response to 25 ms tone pips. Peristimulus time histograms (PSTH) of discharge patterns recorded from fibers with high spontaneous rates (high SRs), show that the discharge rate rapidly adapts to a much lower steady-state level over a 15 ms period with shorter times for units with best frequencies (CFs) greater than 5 kHz. The PSTHs of auditory nerve fibers with low SRs do not show this pattern of rapid adaptation. Differences between the high and low SR populations include higher thresholds, better tuning, and longer latency in the low SR population. The peak-to-steady-state discharge ratio is an increasing function of SR and CF; it varies from 1.0 for fibers with SR = 0 to over 8 for fibers with high SRs and CFs near 10 kHz. This ratio increases with increasing stimulus intensity and stimulus recovery time. The high SR population shows a number of responses to transients which are weak or absent in the low SR population. Increasing the recovery time shortened the latency of both high and low SR AN fibers by as much as 1 ms. A number of other response properties of AN fibers are also reported that are important when interpreting the responses of cochlear nucleus neurons to tone pips.     

Representation of a low-frequency tone in the discharge rate of populations of auditory nerve fibers

Discharge rates for populations of single auditory nerve fibers in response to 1.5 kHz tone bursts were measured in anesthetized cats. Separate plots of average rate vs. best frequency (rate-place profiles) were made for high, medium and low spontaneous rate (SR) auditory nerve fibers. At the lowest sound levels studied (34 dB SPL), all three SR groups show a peak in the rate-place profile centered around 1.5 kHz. At the highest sound levels studied (87 dB SPL), the average rates of the high and medium SR fibers are saturated across a wide range of best frequencies, but a peak around 1.5 kHz is maintained in the rate-place representation of the low SR fibers. These results show that in addition to the temporal information present in the discharge patterns of auditory nerve fibers, a rate-place representation of a single low-frequency tone exists in the auditory nerve over a wide range of sound levels.     

Responses of DCN-PVCN neurons and auditory nerve fibers in unanesthetized decerebrate cats to AM and pure tones: analysis with autocorrelation/power-spectrum

We investigated amplitude-modulated (AM) tone encoding behavior of dorsal and posteroventral cochlear-nucleus (DCN and PVCN) neurons and auditory nerve (AN) fibers in decerebrate unanesthetized cats. Some of the modulation transfer functions (MTFs) were narrowly-tuned band-pass functions; these included responses at moderate and high stimulus levels of DCN pause/build-type-III neurons and the following types of DCN and PVCN chopper neurons: chop-S and/or chop-type-I/III. Other MTFs were broad low-pass or complex functions. Chop-T neurons of the DCN and PVCN tended to exhibit low-pass or flat MTFs. The band-pass MTF neurons exhibited intrinsic oscillations (IOs) in responses to AM or pure tones. The IOs, which were detected in autocorrelation functions and power spectra, were closely correlated (r = 0.863) with the best envelope frequency (BEF). All of the AN fibers showed broad low-pass MTFs with some showing a rudimentary peak in the MTF. The MTFs of DCN-PVCN neurons and AN fibers showed, respectively: (1) BEFs ranging 50-500 Hz, and 400-1300 Hz; (2) upper cut-off frequencies ranging 200-1200 Hz, and 1600-3200 Hz. At stimulus levels of 60-85 dB SPL, maximum modulation gains were as high as 12 dB for DCN-PVCN neurons but were limited to below about 0 dB for AN fibers. The median dynamic ranges of DCN and PVCN neurons (51 and 42 dB, respectively) were substantially wider than those of the low and high spontaneous rate AN fibers (30 and 31 dB, respectively). The observation of higher modulation gain, wider dynamic range, and more narrowly-tuned MTF of DCN-PVCN neurons than AN fibers supports the concept that the capabilities to encode dynamic signals are enhanced in DCN-PVCN neurons compared with AN fibers.     

Coding of signals in noise by amphibian auditory nerve fibers

Rate-level (R-L) functions derived for pure-tones and pure-tones in broadband noise were obtained for auditory nerve fibers in the treefrog, Eleutherodactylus coqui. Normalized R-L functions for low-frequency, low-threshold fibers exhibit a horizontal rightward shift in the presence of broadband background noise. The magnitude of this shift is directly proportional to the noise spectrum level, and inversely proportional to the fiber's threshold. R-L functions for mid- and high-frequency fibers also show a horizontal shift, but to a lesser degree, consistent with their elevated thresholds relative to the low-frequency fibers. The implications of these findings for the processing of biologically significant sounds in the high levels of background noise in the animal's natural habitat are considered.     

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)     

Rapid adaptation depends on the characteristic frequency of auditory nerve fibers

When a tone burst is presented to the ear, the firing rate of single auditory nerve fibers is initially high, then rapidly declines toward a smaller value. The rate of this decline in gerbil is a complex function of stimulus frequency and intensity, and fiber characteristic frequency.     

Tuning and timing of excitation and inhibition in primary auditory nerve fibers

Information about the tuning and timing of excitation, adaptation and suppression in an auditory primary afferent axon can be obtained from the second-order Wiener kernel. Through the process of singular-value decomposition, this information can be extracted from the kernel and displayed graphically in separate two-dimensional images for excitation and inhibition(1). For low- to mid-frequency units, the images typically include checkerboard patterns. For all units they may include patterns of parallel diagonal lines. The former represent non-linearities in the phase-locked (ac) response of the unit; the latter reflect non-linear envelope-following (dc) responses. Examples of detailed interpretation are presented for three amphibian-papillar units from the American bullfrog. The second-order Wiener kernel itself is derived from second-order reverse correlation between spikes and a continuous, non-repeating, broad-band white-noise stimulus.     

Response patterns of auditory nerve fibers during temporary threshold shift

Temporary threshold shifts were studied in chinchillas exposed to noise (octave-band noise centered at 500 Hz, 95 dB SPL, 5 days duration) and the response properties of their auditory nerve fibers were measured. The threshold shifts of the fibers were approximately 35 to 65 dB; these values were equal to or slightly greater than those measured behaviorally. Most units had broad V-shaped tuning curves due to a greater loss in sensitivity near the characteristic frequency (CF) than in the low-frequency tail. In 17% of the units, the thresholds were actually lower in the tail than at CF, so that the tuning curves were W-shaped. The latencies of the fibers were within normal limits in terms of absolute intensity, but shorter than normal in terms of intensity relative to threshold. Other measures such as the spontaneous discharge rate, the discharge rate-intensity functions, and the firing patterns to tone bursts at CF appeared normal. These results indicate that neural response patterns during noise-induced temporary threshold shift are similar to those measured during permanent threshold shift.