Inner hair cell response patterns: implications for low-frequency hearing.

Inner hair cell (IHC) responses to tone-burst stimuli were measured from three locations in the apical half of the guinea pig cochlea. In addition to the measurement of ac receptor potentials, average intracellular voltages, reflecting both ac and dc components of the receptor potential, were computed and compared to determine how bandwidth changes with level. Companion phase measures were also obtained and evaluated. Data collected from turn 2, where best frequency (BF) is approximately 4000 Hz, indicate that frequency response functions are asymmetrical with steeper slopes above the best frequency of the cell. However, in turn 4, where BF is around 250 Hz, the opposite behavior is observed and the steepest slopes are measured below BF. The data imply that cochlear filters are generally asymmetrical with steeper slopes above BF. High-pass filtering by the middle ear serves to reduce this asymmetry in turn 3 and to reverse it in turn 4. Apical response patterns are used to assess the degree to which the middle ear transfer function, the IHC's velocity dependence and the shunting effect of the helicotrema influence low-frequency hearing in guinea pigs. Implications for low-frequency hearing in man are also discussed.     

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.     

Nonlinearities in cochlear receptor potentials and their origins

Using intracellular recording methods in vivo [P. Dallos, J. Neurosci. 5, 1591-1608 (1985)], various nonlinear characteristics of receptor potentials from hair cells located in the low-frequency region of the guinea pig cochlea have been examined. Patterns of saturation for ac and dc response components obtained from Fourier analysis and directly from averaged waveforms are studied. Growth patterns of lower harmonic components are investigated and the interesting nonmonotonic properties of even harmonics noted. The latter are seen in both inner and outer hair cell responses, primarily with stimuli near the cells' best frequency. Fundamental ac and the dc potentials occasionally exhibit nonmonotonic growth. These patterns are studied and their occurrence in inner and outer hair cell responses considered.     

Use of phase contrast microscopy to determine the height of the organ of Corti in whole-mount preparations

A technique has been developed to measure the height of the organ of Corti (OC) in the whole-mount preparations of the cochlear duct. The technique corrects for variations in the microscope system, such as the magnification of the objective lens and the mechanical properties of the fine-focus knob, as well as the refractive index of the embedding medium and the angle of specimens with respect to the optical axis of the microscope. At 11 percentage locations from apex to base, the height of the OC in ten chinchilla cochleas was measured at three positions: (1) the lateral edge of the inner hair cell (IHC); (2) the medial edge of the first row outer hair cell (OHC1); and (3) the lateral edge of the third row outer hair cell (OHC3). These measurements were compared to measurements made on radial sections from five other cochleas, with very good agreement at IHC and OHC3, and fairly good agreement at OHC1. The height at OHC3 varied almost linearly with percentage distance along the OC, ranging from 96 microns (apical end) to 51 microns (basal end). The height at the OHC1 varied from 77 to 49 microns, but did not vary linearly. The height of the IHC was relatively constant, from 50 to 60 microns, except at the basal end, where it decreased to 42 microns.     

A variant temporal-masking-curve method for inferring peripheral auditory compression

Recent studies have suggested that the degree of on-frequency peripheral auditory compression is similar for apical and basal cochlear sites and that compression extends to a wider range of frequencies in apical than in basal sites. These conclusions were drawn from the analysis of the slopes of temporal masking curves (TMCs) on the assumption that forward masking decays at the same rate for all probe and masker frequencies. The aim here was to verify this conclusion using a different assumption. TMCs for normal hearing listeners were measured for probe frequencies (f(P)) of 500 and 4000 Hz and for masker frequencies (f(M)) of 0.4, 0.55, and 1.0 times the probe frequency. TMCs were measured for probes of 9 and 15 dB sensation level. The assumption was that given a 6 dB increase in probe level, linear cochlear responses to the maskers should lead to a 6 dB vertical shift of the corresponding TMCs, while compressive responses should lead to bigger shifts. Results were consistent with the conclusions from earlier studies. It is argued that this supports the assumptions of the standard TMC method for inferring compression, at least in normal-hearing listeners.     

A nonlinear filter-bank model of the guinea-pig cochlear nerve: rate responses

The aim of this study is to produce a functional model of the auditory nerve (AN) response of the guinea-pig that reproduces a wide range of important responses to auditory stimulation. The model is intended for use as an input to larger scale models of auditory processing in the brain-stem. A dual-resonance nonlinear filter architecture is used to reproduce the mechanical tuning of the cochlea. Transduction to the activity on the AN is accomplished with a recently proposed model of the inner-hair-cell. Together, these models have been shown to be able to reproduce the response of high-, medium-, and low-spontaneous rate fibers from the guinea-pig AN at high best frequencies (BFs). In this study we generate parameters that allow us to fit the AN model to data from a wide range of BFs. By varying the characteristics of the mechanical filtering as a function of the BF it was possible to reproduce the BF dependence of frequency-threshold tuning curves, AN rate-intensity functions at and away from BF, compression of the basilar membrane at BF as inferred from AN responses, and AN iso-intensity functions. The model is a convenient computational tool for the simulation of the range of nonlinear tuning and rate-responses found across the length of the guinea-pig cochlear nerve.     

Further evaluation of a model of loudness perception applied to cochlear hearing loss.

This paper describes further tests of a model for loudness perception in people with cochlear hearing loss. It is assumed that the hearing loss (the elevation in absolute threshold) at each audiometric frequency can be partitioned into a loss due to damage to outer hair cells (OHCs) and a loss due to damage to inner hair cells (IHCs) and/or neurons. The former affects primarily the active mechanism that amplifies the basilar membrane (BM) response to weak sounds. It is modeled by increasing the excitation level required for threshold, which results in a steeper growth of specific loudness with increasing excitation level. Loss of frequency selectivity, which results in broader excitation patterns, is also assumed to be directly related to the OHC loss. IHC damage is modeled by an attenuation of the calculated excitation level at each frequency. The model also allows for the possibility of complete loss of IHCs or functional neurons at certain places within the cochlea ("dead" regions). The parameters of the model (OHC loss at each audiometric frequency, plus frequency limits of the dead regions) were determined for three subjects with unilateral cochlear hearing loss, using data on loudness matches between sinusoids presented alternately to their two ears. Further experiments used bands of noise that were either 1-equivalent rectangular bandwidth (ERB) wide or 6-ERBs wide, centered at 1 kHz. Subjects made loudness matches for these bands of noise both within ears and across ears. The model was reasonably accurate in predicting the results of these matches without any further adjustment of the parameters.     

Chinchilla auditory-nerve responses to low-frequency tones

Single unit activity was recorded in the auditory nerves of chinchillas. Period histograms were constructed for responses to tones with frequencies 30-1000 Hz. For low-frequency tones at near-threshold levels, peak period histogram phases for low- and medium-best-frequency (BF) neurons (less than or equal to kHz) ranged from synchronous with condensation at the eardrum to 90 degrees leading it. At near-threshold (but high absolute) levels, high-BF (greater than or equal to 8 kHz) neurons responded in phase with rarefaction. At even higher levels, period histograms for responses of high-BF neurons tended to become bimodal, with one of the modes lagging rarefaction by 90 degrees. Using cochlear microphonics as an indicator of basilar membrane (BM) displacement, at threshold levels, response phase of low- and medium-BF neurons fall within a range between displacement and velocity of the BM toward scala vestibuli. High-BF neurons respond, at threshold (but high) intensities, in phase with BM displacement toward scala tympani. The rates of growth of frequency sensitivity in responses of low-BF (+ 18 dB/oct) and high-BF (+ 12 dB/oct) neurons are consistent with preferred response phases corresponding to BM SV velocity and ST displacement, respectively. At supra-threshold levels high-BF neurons may fire preferentially to both scala tympani displacement and scala vestibuli velocity. These results support the notion that, for high-intensity, low-frequency stimuli, OHC hyperpolarization can induce excitation of the dendrites innervating IHCs.     

Cochlear nonlinearity between 500 and 8000 Hz in listeners with normal hearing

Cochlear nonlinearity was estimated over a wide range of center frequencies and levels in listeners with normal hearing, using a forward-masking method. For a fixed low-level probe, the masker level required to mask the probe was measured as a function of the masker-probe interval, to produce a temporal masking curve (TMC). TMCs were measured for probe frequencies of 500, 1000, 2000, 4000, and 8000 Hz, and for masker frequencies 0.5, 0.7, 0.9, 1.0 (on frequency), 1.1, and 1.6 times the probe frequency. Across the range of probe frequencies, the TMCs for on-frequency maskers showed two or three segments with clearly distinct slopes. If it is assumed that the rate of decay of the internal effect of the masker is constant across level and frequency, the variations in the slopes of the TMCs can be attributed to variations in cochlear compression. Compression-ratio estimates for on-frequency maskers were between 3:1 and 5:1 across the range of probe frequencies. Compression did not decrease at low frequencies. The slopes of the TMCs for the lowest frequency probe (500 Hz) did not change with masker frequency. This suggests that compression extends over a wide range of stimulus frequencies relative to characteristic frequency in the apical region of the cochlea.     

Low-frequency characteristics of human and guinea pig cochleae

Previous physiological studies investigating the transfer of low-frequency sound into the cochlea have been invasive. Predictions about the human cochlea are based on anatomical similarities with animal cochleae but no direct comparison has been possible. This paper presents a noninvasive method of observing low frequency cochlear vibration using distortion product otoacoustic emissions (DPOAE) modulated by low-frequency tones. For various frequencies (15-480 Hz), the level was adjusted to maintain an equal DPOAE-modulation depth, interpreted as a constant basilar membrane displacement amplitude. The resulting modulator level curves from four human ears match equal-loudness contours (ISO226:2003) except for an irregularity consisting of a notch and a peak at 45 Hz and 60 Hz, respectively, suggesting a cochlear resonance. This resonator interacts with the middle ear stiffness. The irregularity separates two regions of the middle ear transfer function in humans: A slope of 12 dB/octave below the irregularity suggests mass-controlled impedance resulting from perilymph movement through the helicotrema; a 6-dB/octave slope above the irregularity suggests resistive cochlear impedance and the existence of a traveling wave. The results from four guinea pig ears showed a 6-dB/octave slope on either side of an irregularity around 120 Hz, and agree with published data.     

Psychophysical tuning curves and auditory thresholds after hair cell damage in the chinchilla

Chinchillas were treated with kanamycin sulfate (150--200 mg/kg/day) to produce high-frequency hearing loss extending to about 4.0 kHz. Thresholds and psychophysical tuning curves (PTCs) were obtained before and after treatment, utilizing a shuttlebox avoidance procedure, and cochlear hair cells were evaluated under phase contrast microscopy. Hair cell loss resulting from kanamycin treatment varied from restricted lesions of the outer hair cells (OHCs) in the cochlear base, with no loss of inner hair cells (IHCs), to more extensive lesions involving both OHCs and IHCs. Threshold shift of at least 40 dB was always associated with OHC loss. PTCs obtained from frequency regions exhibiting 40--50 dB of threshold shift were normal in shape. With threshold shift in excess of 50 dB, PTCs were progressively distorted, with truncation of the tip segment and in some cases increased sensitivity of the tail segment. The results suggest that the threshold of optimally functional IHCs after kanamycin-induced OHC loss is about 40 dB higher than normal. Threshold shift in excess of 40 dB may represent IHC damage. IHCs are capable of transducing the fine-frequency information necessary for generating normally sharp PTCs in the absence of OHCs. However, with threshold shift in excess of approximately 50 dB, this frequency resolution is increasingly compromised.     

Simulations of tonotopically mapped speech processors for cochlear implant electrodes varying in insertion depth

It has been claimed that speech recognition with a cochlear implant is dependent on the frequency alignment of analysis bands in the speech processor with characteristic frequencies (CFs) at electrode locations. However, the most apical electrode location can often have a CF of 1 kHz or more. The use of filters aligned in frequency to relatively basal electrode arrays leads to the loss of lower frequency speech information. This study simulates a frequency-aligned speech processor and common array insertion depths to assess this significance of this loss. Noise-excited vocoders simulated processors driving eight electrodes 2 mm apart. Analysis filters always had center frequencies matching the CFs of the simulated stimulation sites. The simulated insertion depth of the most apical electrode was varied in 2-mm steps between 25 mm (CF 502 Hz) and 17 mm (CF 1851 Hz) from the cochlear base. Identification of consonants, vowels, and words in sentences all showed a significant decline between each of the three more basal simulated electrode configurations. Thus, if implant processors used analysis filters frequency-aligned to electrode CFs, patients whose most apical electrode is 19 mm (CF 1.3 kHz) or less from the cochlear base would suffer a significant loss of speech information.     

DPOAE suppression tuning: cochlear immaturity in premature neonates or auditory aging in normal-hearing adults?

Previous work has shown that distortion product otoacoustic emission (DPOAE) suppression tuning curves (STCs) recorded from premature neonates are narrower than adult STCs at both low and high frequencies. This has been interpreted to indicate an immaturity in cochlear function prior to term birth. However, an alternative explanation for this finding is that adult DPOAE STCs are broadened and reflect cochlear hair cell loss in normal-hearing adults due to aging, and natural exposure to noise and ototoxins. This alternative hypothesis can be tested by studying suppression tuning in normal-hearing school-aged children. If normal-hearing children, who have not aged significantly or been exposed to noise/ototoxins, have DPOAE suppression tuning similar to adults, the auditory aging hypothesis can be ruled out. However, if children have tuning similar to premature neonates and dissimilar from adults, it implicates aging or other factors intrinsic to the adult cochlea. DPOAE STCs were recorded at 1500, 3000, and 6000 Hz using optimal parameters in normal-hearing children and adults. DPOAE STCs collected previously from premature neonates were used for age comparisons. In general, results indicate that tuning curves from children are comparable to adult STCs and significantly different from neonatal STCS at 1500 and 6000 Hz. Only the growth of suppression was not adultlike in children and only at 6000 Hz. These findings do not strongly support the auditory aging hypothesis as a primary explanation for previously observed neonatal-adult differences in DPOAE suppression tuning. It suggests that these age differences are most likely due to immaturities in the neonatal cochlea. However, nonadultlike suppression growth observed in children at 6000 Hz warrants further attention and may be indicative of subtle alternations in the adult cochlea at high frequencies.     

A parametric study of cochlear input impedance

In this paper various aspects of the cat cochlear input impedance Zc (omega) are implemented using a transmission line model having perilymph viscosity and a varying cross-sectional scalae area. These model results are then compared to the experimental results of Lynch et al. [J. Acoust. Soc. Am. 72, 108-130 (1982)]. From the model, the following observations are made about the cochlear input impedance: (a) Scalae area variations significantly alter the model Zc (omega); (b) the use of anatomically measured area improves the fits to the experimental data; (c) improved agreement between model and experimental phase is obtained when perilymph viscosity and tapering are included in the cochlear model for frequencies below approximately 150 Hz; (d) when model scalae tapering and perilymph viscosity are chosen to match physiological conditions, the effect of the helicotrema impedance on Zc (omega) is insignificant; and (e) the cochlear map, which is defined as the position of the basilar membrane peak displacement as a function of stimulus frequency, can have an important effect on Zc (omega) for frequencies below 500 Hz. A nonphysiological cochlear map can give rise to cochlear standing waves, which result in oscillations in Zc (omega). Scalae tapering and perilymph viscosity contribute significantly to the damping of these standing waves. These observations should dispel the previous notion that Zc (omega) is determined solely by parameters of the cochlea close to the stapes, and the notion that Zc (omega) is dominated by the helicotrema at low frequencies.     

Ipsilateral masking between acoustic and electric stimulations

Residual acoustic hearing can be preserved in the same ear following cochlear implantation with minimally traumatic surgical techniques and short-electrode arrays. The combined electric-acoustic stimulation significantly improves cochlear implant performance, particularly speech recognition in noise. The present study measures simultaneous masking by electric pulses on acoustic pure tones, or vice versa, to investigate electric-acoustic interactions and their underlying psychophysical mechanisms. Six subjects, with acoustic hearing preserved at low frequencies in their implanted ear, participated in the study. One subject had a fully inserted 24 mm Nucleus Freedom array and five subjects had Iowa/Nucleus hybrid implants that were only 10 mm in length. Electric masking data of the long-electrode subject showed that stimulation from the most apical electrodes produced threshold elevations over 10 dB for 500, 625, and 750 Hz probe tones, but no elevation for 125 and 250 Hz tones. On the contrary, electric stimulation did not produce any electric masking in the short-electrode subjects. In the acoustic masking experiment, 125-750 Hz pure tones were used to acoustically mask electric stimulation. The acoustic masking results showed that, independent of pure tone frequency, both long- and short-electrode subjects showed threshold elevations at apical and basal electrodes. The present results can be interpreted in terms of underlying physiological mechanisms related to either place-dependent peripheral masking or place-independent central masking.     

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.     

The breaking of cochlear scaling symmetry in human newborns and adults

Scaling symmetry appears to be a fundamental property of the cochlea as evidenced by invariant distortion product otoacoustic emission (DPOAE) phase above ～1-1.5 kHz when using frequency-scaled stimuli. Below this frequency demarcation, phase steepens. Cochlear scaling and its breaking have been described in the adult cochlea but have not been studied in newborns. It is not clear whether immaturities in cochlear mechanics exist at birth in the human neonate. In this study, DPOAE phase was recorded with a swept-tone protocol in three, octave-wide segments from 0.5 to 4 kHz. The lowest-frequency octave was targeted with increased signal averaging to enhance signal-to-noise ratio (SNR) and focus on the apical half of the newborn cochlea where breaks from scaling have been observed. The results show: (1) the ear canal DPOAE phase was dominated by the distortion-source component in the low frequencies; thus, the reflection component cannot explain the steeper slope of phase; (2) DPOAE phase-frequency functions from adults and infants showed an unambiguous discontinuity around 1.4 and 1 kHz when described using two- and three-segment fits, respectively, and (3) newborns had a significantly steeper slope of phase in the low-frequency portion of the function which may suggest residual immaturities in the apical half of the newborn cochlea.     

Speech recognition as a function of high-pass filter cutoff frequency for people with and without low-frequency cochlear dead regions

Regions in the cochlea with no (or very few) functioning inner hair cells and/or neurons are called "dead regions" (DRs). The recognition of high-pass filtered nonsense syllables was measured as a function of filter cutoff frequency for hearing-impaired people with and without low-frequency (apical) cochlear DRs. The diagnosis of any DR was made using the TEN(HL) test, and psychophysical tuning curves were used to define the edge frequency (f(e)) more precisely. Stimuli were amplified differently for each ear, using the "Cambridge formula." For subjects with low-frequency hearing loss but without DRs, scores were high (about 78%) for low cutoff frequencies, remained approximately constant for cutoff frequencies up to 862 Hz, and then worsened with increasing cutoff frequency. For subjects with low-frequency DRs, performance was typically poor for the lowest cutoff frequency (100 Hz), improved as the cutoff frequency was increased to about 0.57f(e), and worsened with further increases. These results indicate that people with low-frequency DRs are able to make effective use of frequency components that fall in the range 0.57f(e) to f(e), but that frequency components below 0.57f(e) have deleterious effects. The results have implications for the fitting of hearing aids to people with low-frequency DRs.     

Interaural correlations in normal and traumatized cochleas: length and sensory cell loss

Sizable intraspecies variations have been found in both the length of the organ of Corti (OC) and the amount of damage resulting from exposure to a particular ototraumatic agent. These variations have made it difficult to address certain research questions such as the susceptibility of the previously injured ear to further damage. If intra-animal correlation is high, the variability problem could be circumvented by using the two ears from a given animal for different aspects of the same study. Therefore, correlation coefficients were calculated for OC length and for percentage of missing inner (IHCs) and outer hair cells (OHCs) in a large sample of chinchillas which included controls and animals which had been exposed to noise or treated with ionizing radiation. The correlation coefficients were +0.96 for OC length, +0.93 for IHC loss, and +0.97 for OHC loss.     

Effects of electrical polarization on inner hair cell receptor potentials

Ac and dc receptor potential components in response to tone-burst stimuli were measured from inner hair cells in the third cochlear turn of the guinea pig. Comparisons were sought between conditions when constant polarizing current was injected into the cell through the recording electrode and when there was no extrinsic current. Hyperpolarization of the cell increased all responses, while depolarization decreased them. The input-output functions were vertically translated by current injection. The extent of translation was a function of current level. In addition, the amount of current-induced change was frequency dependent. Largest changes were seen at low frequencies and the current-induced change tended toward a constant high-frequency asymptote between 1-2 kHz. Changes in the dc response component were considerably in excess of those for the fundamental ac response. The frequency-dependent effects are quantified with the aid of a hair cell circuit model [P. Dallos, Hear. Res. 14, 281-291 (1984)]. It is assumed that the quantity altered by polarizing current (actually by the transmembrane voltage) is the resistance of the cell's basolateral membrane.