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

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

Middle-ear response in the chinchilla and its relationship to mechanics at the base of the cochlea

The responses of the malleus and the stapes to sinusoidal acoustic stimulation have been measured in the middle ears of anesthetized chinchillas using the M?ssbauer technique. With "intact" bullas (i.e., closed except for venting via capillary tubing), the vibrations of the tip of the malleus reach a maximal peak velocity of about 2 mm/s in responses to 100-dB SPL tones in the frequency range 500-6000 Hz; vibration velocity diminishes toward lower frequencies with a slope of about 6 dB/oct. Opening the bulla widely increases the responses to low-frequency stimuli by as much as 16 dB. At low frequencies, malleus response sensitivity with either open or intact bullas far exceeds all previous measurements in cats and matches or exceeds such measurements in guinea pigs. Whether measured in open or intact bullas, phase-versus-frequency curves closely approximate those predicted from the magnitude-versus-frequency curves by minimum phase theory. The stapes responses are similar to those of the malleus, except that stapes response magnitude is lower, on the average, by 7.5 dB at frequencies below 2 kHz and 10.7 dB at 2 kHz and above. Comparison of the responses of the middle ear with those of the basilar membrane at a site 3.5 mm from the stapes indicates that, at frequencies below 150 Hz, the basilar membrane displacement is proportional to stapes acceleration. At frequencies between 150 and 2000 Hz, basilar membrane displacement is proportional to stapes velocity.     

Effect of current stimulus on in vivo cochlear mechanics

In this paper, the influence of direct current stimulation on the acoustic impulse response of the basilar membrane (BM) is studied. A positive current applied in the scala vestibuli relative to a ground electrode in the scala tympani is found to enhance gain and increase the best frequency at a given location on the BM. An opposite effect is found for a negative current. Also, the amplitude of low-frequency cochlear microphonic at high sound levels is found to change with the concurrent application of direct current stimulus. BM vibrations in response to pure tone acoustic excitation are found to possess harmonics whose levels relative to the fundamental increase with the application of positive current and decrease with the application of negative current. A model for outer hair cell activity that couples changes in length and stiffness to transmembrane potential is used to interpret the results of these experiments and others in the literature. The importance of the in vivo mechanical and electrical loading is emphasized. Simulation results show the somewhat paradoxical finding that for outer hair cells under tension, hyperpolarization causes shortening of the cell length due to the dominance of voltage dependent stiffness changes.     

Basilar membrane mechanics at the base of the chinchilla cochlea. I. Input-output functions, tuning curves, and response phases

Basilar membrane (BM) velocity was measured at a site 3.5 mm from the basal end of the chinchilla cochlea using the M?ssbauer technique. The threshold of the compound action potential recorded at the round window in response to tone bursts was used as an indicator of the physiological state of the cochlea. The BM input-output functions display a compressive nonlinearity for frequencies around the characteristic frequency (CF, 8 to 8.75 kHz), but are linear for frequencies below 7 and above 10.5 kHz. In preparations with little surgical damage, isovelocity tuning curves at 0.1 mm/s are sharply tuned, have Q10's of about 6, minima as low as 13 dB SPL, tip-to-tail ratios (at 1 kHz) of 56 to 76 dB, and high-frequency slopes of about 300 dB/oct. These mechanical responses are as sharply tuned as frequency-threshold curves of chinchilla auditory nerve fibers with corresponding CF. There is a progressive loss of sensitivity of the mechanical response with time for the frequencies around CF, but not for frequencies on the tail of the tuning curve. In some experiments the nonlinearity was maintained for several hours, in spite of a considerable loss of sensitivity of the BM response. High-frequency plateaus were observed in both isovelocity tuning curves and phase-frequency curves.     

Columella footplate motion and the cochlear microphonic potential in the embryo and hatchling chicken

A piezoelectric (PZE) vibrator was used to mechanically drive the columella footplate and stimulate the cochlea of chicken embryos and hatchlings. Our objectives were to characterize the motion of the PZE driver and determine the relationship between columella footplate motion (displacement/ velocity) and the cochlear microphonic recorded from the recessus scala tympani (CMrst). At each frequency, displacement of the PZE driver probe tip was linearly related to the applied voltage over a wide range of attenuation levels (-60 to -20 dBre:50 Vp-p). The mean displacement across frequencies (100-4000 Hz) was 0.221+/-0.042 micromp-p for a constant applied voltage level of -20 dBre:50 Vp-p. Displacement was within 1.5 dB of the mean for this stimulus level at all frequencies except for 4000 Hz, where it was approximately 3 dB higher (p < 0.01). CMrst amplitudes in hatchlings were larger than amplitudes in embryos (p=0.003). For a given frequency, CM was linearly related to footplate displacement and velocity at both ages. The transform ratio of CMrst/A (CM amplitude/displacement) increased at approximately 6 dB/octave at frequencies between 100 and 1000 Hz in hatchlings suggesting that cochlear impedance (Zc) was resistive at these frequencies. In a large fraction of the embryos, Zc exhibited reactive behavior.     

Free-field audiogram of the Japanese macaque (Macaca fuscata)

The audiograms of three Japanese macaques and seven humans were determined in a free-field environment using loudspeakers. The monkeys and humans were tested using tones ranging from 8 Hz to 40 kHz and 4 Hz to 22.4 kHz, respectively. At a level of 60 dB sound pressure level the monkeys were able to hear tones extending from 28 Hz to 37 kHz with their best sensitivity of 1 dB occurring at 4 kHz. The human 60-dB hearing range extended from 31 Hz to 17.6 kHz with a best sensitivity of -10 dB at 2 and 4 kHz. These results indicate that the Japanese macaque has low-frequency hearing equal to that of humans and better than that indicated by previous audiograms obtained using headphones.     

Longitudinal endolymph movements and endocochlear potential changes induced by stimulation at infrasonic frequencies.

The inner ear is continually exposed to pressure fluctuations in the infrasonic frequency range (< 20 Hz) from external and internal body sources. The cochlea is generally regarded to be insensitive to such stimulation. The effects of stimulation at infrasonic frequencies (0.1 to 10 Hz) on endocochlear potential (EP) and endolymph movements in the guinea pig cochlea were studied. Stimuli were applied directly to the perilymph of scala tympani or scala vestibuli of the cochlea via a fluid-filled pipette. Stimuli, especially those near 1 Hz, elicited large EP changes which under some conditions exceeded 20 mV in amplitude and were equivalent to a cochlear microphonic (CM) response. Accompanying the electrical responses was a cyclical, longitudinal displacement of the endolymph. The amplitude and phase of the CM varied according to which perilymphatic scala the stimuli were applied to and whether a perforation was made in the opposing perilymphatic scala. Spontaneously occurring middle ear muscle contractions were also found to induce EP deflections and longitudinal endolymph movements comparable to those generated by perilymphatic injections. These findings suggest that cochlear fluid movements induced by pressure fluctuations at infrasonic frequencies could play a role in fluid homeostasis in the normal state and in fluid disturbances in pathological states.     

Frequency characteristics of the middle ear

For 68 temporal bones, frequency curves for the round window volume displacement have been measured for a constant sound pressure at the eardrum. Phase curves were measured for 33 of the specimens. The levels averaged amplitude curve is approximately flat below 1 kHz, where the round window volume displacement per unit sound pressure at the eardrum is 6.8 X 10(-5) mm3/Pa, and falls off by about 15 dB/oct at higher frequencies. For the 20 ears having the largest sound transmission magnitude at low frequencies, the corresponding amplitude curve is displaced about 5 dB towards higher levels. The phase of the round window volume displacement lags the eardrum sound pressure phase. In average for 33 temporal bones, the phase lag increases from zero at the lowest frequencies to pi near 2 kHz and to about 1.5 pi at 10 kHz.     

Interaction between adenosine triphosphate and mechanically induced modulation of electrically evoked otoacoustic emissions

It was shown previously that electrically evoked otoacoustic emissions (EEOAEs) can be amplitude modulated by low-frequency bias tones and enhanced by application of adenosine triphosphate (ATP) to scala media. These effects were attributed, respectively, to the mechano-electrical transduction (MET) channels and ATP-gated ion channels on outer hair cell (OHC) stereocilia, two conductance pathways that appear to be functionally independent and additive in their effects on ionic current through the OHC. In the experiments described here, the separate influences of ATP and MET channel bias on EEOAEs did not combine linearly. Modulated EEOAEs increased in amplitude, but lost modulation at the phase and frequency of the bias tone (except at very high sound levels) after application of ATP to scala media, even though spectral components at the modulation sideband frequencies were still present. Some sidebands underwent phase shifts after ATP. In EEOAEs modulated by tones at lower sound levels, substitution of the original phase values restored modulation to the waveform, which then resembled a linear summation of the separate effects of ATP and low-frequency bias. While the physiological meaning of this procedure is not clear, the result raises the possibility that a secondary effect of ATP on one or more nonlinear stages in the transduction process, which may have caused the phase shifts, obscured linear summation at lower sound levels. In addition, "acoustic enhancement" of the EEOAE may have introduced nonlinear interaction at higher levels of the bias tones.     

Constructing a cochlear transducer function from the summating potential using a low-frequency bias tone

A new method is developed to construct a cochlear transducer function using modulation of the summating potential (SP), a dc component of the electrical response of the cochlea to a sinusoid. It is mathematically shown that the magnitude of the SP is determined by the even-order terms of the power series representing a nonlinear function. The relationship between the SP magnitudes and the second derivative of the transducer function was determined by using a low-frequency bias tone to position a high-frequency probe tone at different places along the cochlear transducer function. Two probe tones (6 kHz and 12 kHz) ranging from 70 to 90 dB SPL and a 25-Hz bias tone at 130 dB SPL were simultaneously presented. Electric responses from the cochlea were recorded by an electrode placed at the round window to obtain the SP magnitudes. The experimental results from eight animals demonstrated that the SP magnitudes as a function of bias levels are essentially proportional to the second derivative of a sigmoidal Boltzmann function. This suggests that the low-frequency modulated SP amplitude can be used to construct a cochlear transducer function.     

Finite element cochlear models and their steady state response

Numerical cochlear models are constructed by means of a finite element approach and their frequency and spatial responses are calculated. The cochlea is modelled as a coupled fluid-membrane system, for which both two- and three-dimensional models are considered. The fluid in the scala canals is assumed to be incompressible and the basilar membrane is assumed to be a locally reactive impedance wall or a lossy elastic membrane. With the three-dimensional models, the effects are examined of the spiral configuration of the cochlea, of the presence of the lamina and the ligament that narrows the coupling area between the two fluid canals (scala vestibuli and scala tympani), and of the extended reaction of the basilar membrane which cannot be included in case of the two-dimensional models. The conclusion is that these effects on the cochlear response and the inherent mechanism governing the cochlear behaviour are found to be rather secondary.     

Intensity discrimination with cochlear implants

Intensity difference limens were measured for various frequencies and intensities of sinusoidal and pulsatile electrical stimulation in monkeys with electrodes implanted in the scala tympani, scala vestibuli, modiolus, or middle ear. Difference limens decreased, as a function of initial stimulus intensity, from values of 1.5-3 dB near threshold to as low as 0.5 dB near the upper limit of the dynamic range. If sensation level was held constant, difference limens decreased as a function of frequency up to about 500 Hz, and then remained constant. They were similar across a variety of electrode placements and separations if differences in threshold and dynamic range were taken into account. However, difference limens measured in severely damaged ears were slightly smaller than those in moderately damaged ears. The near miss to Weber's law, characteristic of acoustic difference limens, was not seen with electrical stimuli. Differences limens for electrical stimuli were roughly one-half those for acoustic stimuli; thus, part of the deficit in dynamic range for electrical stimulation compared with acoustic stimulation is countered by the smaller intensity differences limens for electrical stimuli.     

Edge effects on frequency discrimination of tones presented in low- and high-pass noise backgrounds

Previous research has indicated that frequency discrimination performance is poorer for tones presented near the sharp spectral edge of a low-pass noise than for tones presented near the edge of a high-pass noise, or for tones in the same low-pass noise with high-pass noise added [Emmerich et al., J. Acoust. Soc. Am. 80, 1668-1672 (1986)]. The present study extends these findings in order to investigate how the steepness of the spectral edges of low- and high-pass maskers influences the discriminability of tones presented near these edges. Frequency discrimination was measured in each of three high- and low-pass noise backgrounds (which differed in the steepness of their filter skirts). The following results were obtained: (1) In the low-pass noise background, frequency discrimination performance improved as the filter skirt became more gradual; (2) in the high-pass noise background, performance first improved and then became poorer as the filter skirt became shallower; and (3) performance in low-pass noise was poorer than that in high-pass noise for the two steepest slopes employed (96 and 72 dB/oct) but not for the shallower slope (36 dB/oct). Results are discussed in the context of lateral suppression and edge pitch effects, and of a trade-off between possible edge effects and masking.     

Frequency-dependent self-induced bias of the basilar membrane and its potential for controlling sensitivity and tuning in the mammalian cochlea

A displacement-sensitive capacitive probe technique was used in the first turn of guinea pig cochleas to examine whether the motion of the basilar membrane includes a displacement component analogous to the dc receptor potentials of the hair cells. Such a "dc" component apparently exists. At a given location on the basilar membrane, its direction toward scala vestibuli (SV) or scala tympani (ST) varies systematically with frequency of the acoustic stimulus. Furthermore, it appears to consist of two parts: a small asymmetric offset response to each gated tone burst plus a progressive shift of the basilar membrane from its previous position. The mean position shift is cumulative, increasing with successive tone bursts. The amplitude of the immediate offset response, when plotted as a function of frequency, appears to exhibit a trimodal pattern. This displacement offset is toward SV at the characteristic frequency (CF) of the location of the probe, while at frequencies either above or below the CF the offset is relatively larger, and toward ST. The mechanical motion of the basilar membrane therefore appears to contain the basis for lateral suppression. The cumulative mean position shift, however, appears to peak toward ST at the apical end of the traveling wave envelope and appears to be associated with a resonance, not of the basilar membrane motion directly, but coupled to it. The summating potential, measured concurrently at the round window, shows a more broadly tuned peak just above the CF of the position of the probe. This seems to correspond to the peak at the CF of the mechanical bias. As the preparation deteriorates, the best frequency of the vibratory displacement response decreases to about a half-octave below the original CF. There is a corresponding decrease in the frequency of the peaks of the trimodal pattern of the asymmetric responses to tone bursts. The trimodal pattern also broadens. In previous experiments the basilar membrane has been forced to move in response to a low-frequency biasing tone. The sensitivity to high-frequency stimuli varies in phase with the biasing tone. The amplitudes of slow movement in these earlier experiments and in the present experiments are of the same order of magnitude. This suggests strongly that the cumulative shift toward ST to a high-frequency acoustic stimulus constitutes a substantial controlling bias on the sensitivity of the cochlea in that same high-frequency region. Its effect will be to reduce the slope of neural rate-level functions on the high-frequency side of CF.     

Level discrimination as a function of level for tones from 0.25 to 16 kHz

Difference limens for level (delta L in dB = 20 log [(p + delta p)/p], where p is pressure) were measured as a function of level for tones at 0.25, 0.5, 1, 2, 4, 8, 10, 12, 14, and 16 kHz. At each frequency, test levels encompassed the range from near threshold to 95 dB SPL in steps of 10 dB or smaller. The stimulus duration was 500 ms and the interstimulus interval was 250 ms. An adaptive two-alternative forced-choice procedure with feedback was used. Results for six normal listeners show individual differences among listeners, but the general trends seen in the average data clearly are present in the individual data and show the following. First, the delta Ls at all but the highest frequencies are generally smaller at high levels than at low levels. Second, the delta Ls at equal SPLs are largely independent of frequency up to about 4 kHz, but increase with frequency above 4 kHz. Third, at 8 and 10 kHz, the delta Ls are clearly nonmonotonic functions of level, showing consistent deterioration in the mid-level delta Ls relative to the low- and high-level delta Ls. The present data are discussed qualitatively in terms of current models of level discrimination.     

Comments on "Acoustic Transfer Characteristics in Human Middle Ears Studied by a SQUID Magnetometer Method" [J. Acoust. Soc. Am. 82, 1646-1654 (1987)

The study by Brenkman et al. [J. Acoust. Soc. Am. 82, 1646-1654 (1987)] of malleus umbo and anterior crus of stapes displacement in 14 human temporal bones shows a mean -7.3-dB/oct slope above 1.0 kHz for stapes displacement in response to a 80-dB SPL input at the eardrum. The slope they obtained for midfrequency (1.0-4.0 kHz) stapes displacement is significantly flatter than what was found previously [Gyo et al., Acta Otolaryngol. 103, 87-95 (1987); Gundersen, Prostheses in the Ossicular Chain (University Park, Baltimore, MD, 1971); Kringlebotn and Gundersen, J. Acoust. Soc. Am. 77, 159-164 (1985); Vlaming and Feenstra, Clin. Otolaryngol. 11, 353-363 (1986a)]; in these studies, stapes displacement rolled off at -12.0 to -14.9 dB/oct above 1.0 kHz. It appears that their mean midfrequency stapes displacement slope has been flattened by some unusual results in a small number of ears. Possible reasons for these results are discussed.     

Testing coherent reflection in chinchilla: Auditory-nerve responses predict stimulus-frequency emissions

Coherent-reflection theory explains the generation of stimulus-frequency and transient-evoked otoacoustic emissions by showing how they emerge from the coherent "backscattering" of forward-traveling waves by mechanical irregularities in the cochlear partition. Recent published measurements of stimulus-frequency otoacoustic emissions (SFOAEs) and estimates of near-threshold basilar-membrane (BM) responses derived from Wiener-kernel analysis of auditory-nerve responses allow for comprehensive tests of the theory in chinchilla. Model predictions are based on (1) an approximate analytic expression for the SFOAE signal in terms of the BM traveling wave and its complex wave number, (2) an inversion procedure that derives the wave number from BM traveling waves, and (3) estimates of BM traveling waves obtained from the Wiener-kernel data and local scaling assumptions. At frequencies above 4 kHz, predicted median SFOAE phase-gradient delays and the general shapes of SFOAE magnitude-versus-frequency curves are in excellent agreement with the measurements. At frequencies below 4 kHz, both the magnitude and the phase of chinchilla SFOAEs show strong evidence of interference between short- and long-latency components. Approximate unmixing of these components, and association of the long-latency component with the predicted SFOAE, yields close agreement throughout the cochlea. Possible candidates for the short-latency SFOAE component, including wave-fixed distortion, are considered. Both empirical and predicted delay ratios (long-latency SFOAE delay/BM delay) are significantly less than 2 but greater than 1. Although these delay ratios contradict models in which SFOAE generators couple primarily into cochlear compression waves, they are consistent with the notion that forward and reverse energy propagation in the cochlea occurs predominantly by means of traveling pressure-difference waves. The compelling overall agreement between measured and predicted delays suggests that the coherent-reflection model captures the dominant mechanisms responsible for the generation of reflection-source otoacoustic emissions.     

Speech coding in the auditory nerve: III. Voiceless fricative consonants

Responses of auditory-nerve fibers in anesthetized cats were recorded for synthetic voiceless fricative consonants. The four stimuli (/x/, /s/, /s/, and /f/) were presented at two levels corresponding to speech in which the levels of the vowels would be approximately 60 and 75 dB SPL, respectively. Discharge patterns were characterized in terms of PST histograms and their power spectra. For both stimulus levels, frequency regions in which the stimuli had considerable energy corresponded well with characteristic-frequency (CF) regions in which average discharge rates were the highest. At the higher level, the profiles of discharge rate against CF were more distinctive for the stimulus onset than for the central portion. Power spectra of PST histograms had large response components near fiber characteristic frequencies for CFs up to 3-4 kHz, as well as low-frequency components for all fibers. The relative amplitudes of these components varied for the different stimuli. In general, the formant frequencies of the fricatives did not correspond with the largest response components, except for formants below about 3 kHz. Processing schemes based on fine time patterns of discharge that were effective for vowel stimuli generally failed to extract the formant frequencies of fricatives.     

Dead regions and pitch perception

The perception of pitch for pure tones with frequencies falling inside low- or high-frequency dead regions (DRs) was examined. Subjects adjusted a variable-frequency tone to match the pitch of a fixed tone. Matches within one ear were often erratic for tones falling in a DR, indicating unclear pitch percepts. Matches across ears of subjects with asymmetric hearing loss, and octave matches within ears, indicated that tones falling within a DR were perceived with an unclear pitch and/or a pitch different from "normal" whenever the tones fell more than 0.5 octave within a low- or high-frequency DR. One unilaterally impaired subject, with only a small surviving region between 3 and 4 kHz, matched a fixed 0.5-kHz tone in his impaired ear with, on average, a 3.75-kHz tone in his better ear. When asked to match the 0.5-kHz tone with an amplitude-modulated tone, he adjusted the carrier and modulation frequencies to about 3.8 and 0.5 kHz, respectively, suggesting that some temporal information was still available. Overall, the results indicate that the pitch of low-frequency tones is not conveyed solely by a temporal code. Possibly, there needs to be a correspondence between place and temporal information for a normal pitch to be perceived.     

Audiogram of a striped dolphin (Stenella coeruleoalba)

The underwater hearing sensitivity of a striped dolphin was measured in a pool using standard psycho-acoustic techniques. The go/no-go response paradigm and up-down staircase psychometric method were used. Auditory sensitivity was measured by using 12 narrow-band frequency-modulated signals having center frequencies between 0.5 and 160 kHz. The 50% detection threshold was determined for each frequency. The resulting audiogram for this animal was U-shaped, with hearing capabilities from 0.5 to 160 kHz (8 1/3 oct). Maximum sensitivity (42 dB re 1 microPa) occurred at 64 kHz. The range of most sensitive hearing (defined as the frequency range with sensitivities within 10 dB of maximum sensitivity) was from 29 to 123 kHz (approximately 2 oct). The animal's hearing became less sensitive below 32 kHz and above 120 kHz. Sensitivity decreased by about 8 dB per octave below 1 kHz and fell sharply at a rate of about 390 dB per octave above 140 kHz.