Temporal aspects of suppression in distortion-product otoacoustic emissions

This study examined the time course of cochlear suppression using a tone-burst suppressor to measure decrement of distortion-product otoacoustic emissions (DPOAEs). Seven normal-hearing subjects with ages ranging from 19 to 28 yr participated in the study. Each subject had audiometric thresholds ≤ 15 dB HL [re ANSI (2004) Specifications for Audiometers] for standard octave and inter-octave frequencies from 0.25 to 8 kHz. DPOAEs were elicited by primary tones with f(2)?= 4.0 kHz and f(1)?= 3.333 kHz (f(2)/f(1)?= 1.2). For the f(2), L(2) combination, suppression was measured for three suppressor frequencies: One suppressor below f(2) (3.834 kHz) and two above f(2) (4.166 and 4.282 kHz) at three levels (55, 60, and 65 dB SPL). DPOAE decrement as a function of L(3) for the tone-burst suppressor was similar to decrements obtained with longer duration suppressors. Onset- and setoff- latencies were ≤ 4 ms, in agreement with previous physiological findings in auditory-nerve fiber studies that suggest suppression results from a nearly instantaneous compression of the waveform. Persistence of suppression was absent for the below-frequency suppressor (f(3)?= 3.834 kHz) and was ≤ 3 ms for the two above-frequency suppressors (f(3)?= 4.166 and 4.282 kHz).     

Reliability of distortion-product otoacoustic emissions and their relation to loudness

The reliability of distortion-product otoacoustic emission (DPOAE) measurements and their relation to loudness measurements was examined in 16 normal-hearing subjects and 58 subjects with hearing loss. The level of the distortion product (L(d)) was compared across two sessions and resulted in correlations that exceeded 0.90. The reliability of DPOAEs was less when parameters from nonlinear fits to the input/output (I/O) functions were compared across visits. Next, the relationship between DPOAE I/O parameters and the slope of the low-level portion of the categorical loudness scaling (CLS) function (soft slope) was assessed. Correlations of 0.65, 0.74, and 0.81 at 1, 2, and 4 kHz were observed between CLS soft slope and combined DPOAE parameters. Behavioral threshold had correlations of 0.82, 0.83, and 0.88 at 1, 2, and 4 kHz with CLS soft slope. Combining DPOAEs and behavioral threshold provided little additional information. Lastly, a multivariate approach utilizing the entire DPOAE I/O function was used to predict the CLS rating for each input level (dB SPL). Standard error of the estimate when using this method ranged from 2.4 to 3.0 categorical units (CU), suggesting that DPOAE I/O functions can predict CLS measures within the CU step size used in this study (5).     

Human cochlear tuning estimates from stimulus-frequency otoacoustic emissions

Two objective measures of human cochlear tuning, using stimulus-frequency otoacoustic emissions (SFOAE), have been proposed. One measure used SFOAE phase-gradient delay and the other two-tone suppression (2TS) tuning curves. Here, it is hypothesized that the two measures lead to different frequency functions in the same listener. Two experiments were conducted in ten young adult normal-hearing listeners in three frequency bands (1-2 kHz, 3-4 kHz and 5-6 kHz). Experiment 1 recorded SFOAE latency as a function of stimulus frequency, and experiment 2 recorded 2TS iso-input tuning curves. In both cases, the output was converted into a sharpness-of-tuning factor based on the equivalent rectangular bandwidth. In both experiments, sharpness-of-tuning curves were shown to be frequency dependent, yielding sharper relative tuning with increasing frequency. Only a weak frequency dependence of the sharpness-of-tuning curves was observed for experiment 2, consistent with objective and behavioural estimates from the literature. Most importantly, the absolute difference between the two tuning estimates was very large and statistically significant. It is argued that the 2TS estimates of cochlear tuning likely represents the underlying properties of the suppression mechanism, and not necessarily cochlear tuning. Thus the phase-gradient delay estimate is the most likely one to reflect cochlear tuning.     

Transient-evoked stimulus-frequency and distortion-product otoacoustic emissions in normal and impaired ears

Transient-evoked stimulus-frequency otoacoustic emissions (SFOAEs), recorded using a nonlinear differential technique, and distortion-product otoacoustic emissions (DPOAEs) were measured in 17 normal-hearing and 10 hearing-impaired subjects using pairs of tone pips (pp), gated tones (gg), and for DPOAEs, continuous and gated tones (cg). Temporal envelopes of stimulus and OAE waveforms were obtained by narrow-band filtering at the stimulus or DP frequency. Mean SFOAE latencies in normal ears at 2.7 and 4.0 kHz decreased with increasing stimulus level and were larger at 4.0 kHz than latencies in impaired ears. Equivalent auditory filter bandwidths were calculated as a function of stimulus level from SFOAE latencies by assuming that cochlear transmission is minimum phase. DPOAE latencies varied less with level than SFOAE latencies. The ppDPOAEs often had two (or more) peaks separated in time with latencies consistent with model predictions for distortion and reflection components. Changes in ppDPOAE latency with level were sometimes explained by a shift in relative amplitudes of distortion and reflection components. The pp SFOAE SPL within the main spectral lobe of the pip stimulus was higher for normal ears in the higher-frequency half of the pip than the lower-frequency half, which is likely an effect of basilar membrane two-tone suppression.     

Level dependence of distortion-product otoacoustic emissions measured at high frequencies in humans

Given that high-frequency hearing is most vulnerable to cochlear pathology, it is important to characterize distortion-product otoacoustic emissions (DPOAEs) measured with higher-frequency stimuli in order to utilize these measures in clinical applications. The purpose of this study was to explore the dependence of DPOAE amplitude on the levels of the evoking stimuli at frequencies greater than 8 kHz, and make comparisons with those data that have been extensively measured with lower-frequency stimuli. To accomplish this, DPOAE amplitudes were measured at six different f2 frequencies (2, 5, 10, 12, 14, and 16 kHz), with a frequency ratio (f2/f1) of 1.2, at five fixed levels (30 to 70 dB SPL) of one primary (either f1 or f2), while the other primary was varied in level (30 to 70 dB SPL). Generally, the level separation between the two primary tones (L1 > L2) generating the largest DPOAE amplitude (referred to as the "optimal level separation") decreased as the level of the fixed primary increased. Additionally, the optimal level separation was frequency dependent, especially at the lower fixed primary tone levels ( < or = 50 dB SPL). In agreement with previous studies, the DPOAE level exhibited greater dependence on L1 than on L2.     

Growth of suppression in humans based on distortion-product otoacoustic emission measurements

Distortion-product otoacoustic emissions (DPOAEs) were used to describe suppression growth in normal-hearing humans. Data were collected at eight f(2) frequencies ranging from 0.5 to 8 kHz for L(2) levels ranging from 10 to 60 dB sensation level. For each f(2) and L(2) combination, suppression was measured for nine or eleven suppressor frequencies (f(3)) whose levels varied from -20 to 85 dB sound pressure level (SPL). Suppression grew nearly linearly when f(3) ≈ f(2), grew more rapidly for f(3)?< f(2), and grew more slowly for f(3)?> f(2). These results are consistent with physiological and mechanical data from lower animals, as well as previous DPOAE data from humans, although no previous DPOAE study has described suppression growth for as wide a range of frequencies and levels. These trends were evident for all f(2) and L(2) combinations; however, some exceptions were noted. Specifically, suppression growth rate was less steep as a function of f(3) for f(2) frequencies ≤ 1 kHz. Thus, despite the qualitative similarities across frequency, there were quantitative differences related to f(2), suggesting that there may be subtle differences in suppression for frequencies above 1 kHz compared to frequencies below 1 kHz.     

Inferring basilar-membrane motion from tone-burst otoacoustic emissions and psychoacoustic measurements

The amplitude of otoacoustic emissions, which arise on the basilar membrane, is assumed to be proportional to basilar-membrane motion. It should then be possible to assess basilar-membrane motion on the basis of otoacoustic emissions. The present study provides support for this possibility by comparing basilar-membrane motion inferred from emissions to that inferred from psychoacoustic measures. Three psychoacoustic measurements believed to be associated with basilar-membrane motion were investigated: (1) pulsation threshold; (2) loudness functions derived from temporal integration; and (3) loudness functions derived from loudness matches between pure tones and multitone complexes. Results of the psychoacoustic measurements and of the tone-burst otoacoustic emissions led to very similar estimations of basilar-membrane motion. Accordingly, emissions could serve as an excellent tool--one that is objective, noninvasive, and rapid--for estimating relative basilar-membrane motion.     

Frequency specificity of distortion-product otoacoustic emissions produced by high-level tones despite inefficient cochlear electromechanical feedback

Distortion product otoacoustic emissions (DPOAEs) are thought to stem from the outer hair cells (OHCs) around the normally narrow place tuned to the primary tone stimuli. They are thus said to be frequency-specific: their local absence should accurately pinpoint local OHC damage. Yet the influence of impaired tuning on DPOAE frequency specificity is poorly documented. Mice with local damage to OHCs were examined. Their DPOAEs were frequency-specific in that audiometric notches were accurately tracked. The same cochleae were further impaired by ischemia or furosemide injection inducing strial dysfunction with flat loss of sensitivity and tuning, while the preexisting pattern of damaged OHCs remained unaltered. Despite the loss of cochlear activity, DPOAEs produced by high-level (> or =70 dB SPL) primaries remained large in about the same interval where they had been initially normal, i.e., that with nondamaged OHCs, albeit with a slight frequency shift, of -1.1 kHz on average. Thus, the ability of DPOAEs to map structurally intact OHCs cannot be a mere consequence of cochlear tuning as it largely persists in its absence. The key element for this correct mapping is likely part of intact OHC structures (e.g., stereocilia bundles) and must have some tuning of its own.     

Evidence for basal distortion-product otoacoustic emission components

Distortion-product otoacoustic emissions (DPOAEs) were measured with traditional DP-grams and level/phase (L/P) maps in rabbits with either normal cochlear function or unique sound-induced cochlear losses that were characterized as either low-frequency or notched configurations. To demonstrate that emission generators distributed basal to the f(2) primary-tone contribute, in general, to DPOAE levels and phases, a high-frequency interference tone (IT) was presented at 1/3 of an octave (oct) above the f(2) primary-tone, and DPOAEs were re-measured as "augmented" DP-grams (ADP-grams) and L/P maps. The vector difference between the control and augmented functions was then computed to derive residual DP-grams (RDP-grams) and L/P maps. The resulting RDP-grams and L/P maps, which described the DPOAEs removed by the IT, supported the notion that basal DPOAE components routinely contribute to the generation of standard measures of DPOAEs. Separate experiments demonstrated that these components could not be attributed to the effects of the 1/3-oct IT on f(2), or DPOAEs generated by the addition of a third interfering tone. These basal components can "fill in" the lesion estimated by the commonly employed DP-gram. Thus, ADP-grams more accurately reveal the pattern of cochlear damage and may eventually lead to an improved DP-gram procedure.     

L1,L2 maps of distortion-product otoacoustic emissions from a moth ear with only two auditory receptor neurons

The tympanal organ of the moth Empyreuma affinis emits physiologically vulnerable distortion-product otoacoustic emissions. To assess the nature of underlying mechanical nonlinearities, we measured L1,L2 maps by varying both stimulus levels. Two types of maps were found: (1) Maps containing dominant islands centered at the L1=L2 diagonal as it is typical for saturating nonlinearities that can be described by Boltzmann functions. In contrast to maps published for mammals and frogs, the shape of such islands includes sharp ridges at L1 or L2 levels close to 70 dB sound pressure level. This could be produced by a strongly asymmetric operating point of the respective transfer functions, consistent with the fact that the auditory sensory cells are not hair cells but primary mechanoreceptors with a single cilium. The saturating map components could be selectively reduced by acoustic suppression. (2) Maps where separated islands were less conspicuous but in which the dominant feature consisted of contour lines which were orthogonal to the L1=2L2 diagonal and could be generated by an expansive nonlinearity. Maps showing strong islands were found for f2 frequencies between 26.7 and 45 kHz, maps without strong islands for f2 between 42 and 57.5 kHz. This suggests a frequency-dependent change regarding the involved mechanical nonlinearities.     

Characterizing distortion-product otoacoustic emission components across four species

Distortion-product otoacoustic emissions (DPOAEs) were measured as level/phase (L/P) maps in humans, rabbits, chinchillas, and rats with and without an interference tone (IT) placed either near the 2f(1)-f(2) DPOAE frequency place (f(dp)) or at one-third of an octave above the f(2) primary tone (1/3-oct IT). Vector differences between with and without IT conditions were computed to derive a residual composed of the DPOAE components removed by the IT. In humans, a DPOAE component could be extracted with the expected steep phase gradient indicative of reflection emissions by ITs near f(dp). In the laboratory species, ITs near f(dp) failed to produce any conclusive evidence for reflection components. For all species, 1/3-oct ITs extracted large DPOAE components presumably generated at or basal to the IT-frequency place that exhibited both distortion- and reflection-like phase properties. Together, these findings suggested that basal distortion components could assume reflection-like phase behavior when the assumptions of cochlear-scaling symmetry, the basis for shallow phase gradients for constant f(2)/f(1) ratio sweeps, are violated. The present results contradict the common belief that DPOAE components associated with steep or shallow phase slopes are unique signatures for reflection emissions arising from f(dp) or distortion emissions generated near f(2), respectively.     

Cochlear compression: effects of low-frequency biasing on quadratic distortion product otoacoustic emission

Distortion product otoacoustic emissions (DPOAEs) are generated from the nonlinear transduction n cochlear outer hair cells. The transducer function demonstrating a compressive nonlinearity can be estimated from low-frequency modulation of DPOAEs. Experimental results from the gerbils showed that the magnitude of quadratic difference tone (QDT, f2-f1) was either enhanced or suppressed depending on the phase of the low-frequency bias tone. Within one period of the bias tone, QDT magnitudes exhibited two similar modulation patterns, each resembling the absolute value of the second derivative of the transducer function. In the time domain, the center notches of the modulation patterns occurred around the zero crossings of the bias pressure, whereas peaks corresponded to the increase or decrease in bias pressure. Evaluated with respect to the bias pressure, modulated QDT magnitude displayed a double-modulation pattern marked by a separation of the center notches. Loading/unloading of the cochlear transducer or rise/fall in bias pressure shifted the center notch to positive or negative sound pressures, indicating a mechanical hysteresis. These results suggest that QDT arises from the compression that coexists with the active hysteresis in cochlear transduction. Modulation of QDT magnitude reflects the dynamic regulation of cochlear transducer gain and compression.     

Tone-burst-evoked otoacoustic emissions from normal-hearing subjects

Tone-burst-evoked otoacoustic emissions were measured as a function of tone-burst sound pressure level and frequency in normally hearing ears. Although the spectral and temporal properties varied across individual ears, there was a close correspondence between stimulus and response spectra. Both the spectral and latency characteristics of tone-burst-evoked emissions are consistent with the hypothesis that they are generated at sites along the cochlear partition corresponding to their frequency.     

Recovery of distortion-product otoacoustic emissions after a 2-kHz monaural sound-exposure in humans: effects on fine structures

A better understanding of the vulnerability of the fine structures of distortion-product otoacoustic emissions (DPOAEs) after acoustic overexposure may improve the knowledge about DPOAE generation, cochlear damage, and lead to more efficient diagnostic tools. It is studied whether the DPOAE fine structures of 16 normal-hearing human subjects are systematically affected after a moderate monaural sound-exposure of 10 min to a 2-kHz tone normalized to an exposure level L(EX,8h) of 80 dBA. DPOAEs were measured before and in the following 70 min after the exposure. The experimental protocol allowed measurements with high time and frequency resolution in a 1/3-octave band centered at 3 kHz. On average, DPOAE levels were reduced approximately 5 dB in the entire measured frequency-range. Statistically significant differences in pre- and post-exposure DPOAE levels were observed up to 70 min after the end of the sound exposure. The results show that the effects on fine structures are highly individual and no systematic change was observed.     

Physiopathological significance of distortion-product otoacoustic emissions at 2f1-f2 produced by high- versus low-level stimuli

Distortion product otoacoustic emissions emitted by the cochlea at 2f1-f2 in response to pairs of pure tones at f1 and f2 (DPOAE) form a class of otoacoustic emissions and as such, are viewed as a reliable tool for screening outer hair cell (OHC) dysfunctions on a pass/fail basis. However, the persistence of residual DPOAEs from impaired cochleae at high stimulus levels has suggested that above 60-70 dB SPL, instead of reflecting "active" cochlear motion, DPOAEs might represent another "passive" modality: they would thus become unsuitable for analyzing cochlear function. The present work reports the consequences on high- vs low-level DPOAEs of three types of cochlear impairments involving OHCs: progressive OHC degeneration of genetic origin in CD1 mice, complete cochlear ischemia in gerbils, and furosemide injection vs ischemia-reperfusion in gerbils. An alternative to the "active-passive" model was used wherein regardless of stimulus level, cubic DPOAEs are produced by N (probably OHC-borne) nonlinear elements driven by input I and modulated by a function F3 of their operating point o; thus, DPOAE proportional to NI3F3(o). When OHCs degenerated, thereby implying a decrease of N, DPOAE levels also decreased regardless of the stimulus level up to 80 dB SPL, in line with the previous formula but at variance with the prediction of the active-passive concept. Instead of affecting N, the other two experiments impaired the efficiency of the cochlear feedback loop as a result of its electrical drive being decreased by strial dysfunction. As it is well accepted that the impaired basilar-membrane motion, although greatly reduced at low levels, tends to catch up with a normal one at higher levels, it was assumed the same was true with I so that DPOAE levels had to be, and indeed were little affected at high levels while plummeting at low levels, without any need for invoking two modalities for DPOAE generation. Finally, comparisons of furosemide vs ischemia effects revealed additional influences on DPOAEs, possibly accounted for by function F3(o). These results lead to the proposal that although high-level DPOAEs are expected to be poor audiometric indicators, they seem well adapted to assessing the functional integrity of nonlinear elements in OHCs, i.e., presumably their mechanoelectrical transduction channels.     

Swept-tone transient-evoked otoacoustic emissions

Transient-evoked otoacoustic emissions (TEOAE) are responses generated within the inner ear in response to acoustic stimuli and are indicative of normal cochlear function. They are commonly acquired by averaging post-stimulus acoustic responses recorded near the eardrum in response to brief stimuli such as clicks or tone pips. In this study a new long duration stimulus consisting of a frequency swept tone is introduced for the acquisition of TEOAEs. Like stimulus frequency generated OAEs, swept-tone responses contain embedded OAEs. With swept-tone analysis, OAEs can be recovered by convolving it with a time reversed swept-tone signal resulting in time-compression. In addition, higher order nonlinear OAE responses were removed from the linear TEOAE. The results show comparable phase and time-frequency properties between the click and swept-tone evoked OAEs. Swept-tone acquisition of TEOAEs has beneficial noise properties, improving the signal to noise ratio by 6 dB compared to click evoked responses thus offering testing time savings. Additionally, swept-tone analysis removed synchronized spontaneous OAE activity from the recordings of subjects exhibiting such responses in conventional click TEOAEs. Since swept-tone stimulus consists of a single frequency component at any instantaneous moment, its analysis also provides for direct comparison with stimulus-frequency OAEs and click evoked OAEs.     

Comparing stimulus-frequency otoacoustic emissions measured by compression, suppression, and spectral smoothing

Stimulus-frequency otoacoustic emissions (SFOAEs) have been measured in several different ways, including (1) nonlinear compression, (2) two-tone suppression, and (3) spectral smoothing. Each of the three methods exploits a different cochlear phenomenon or signal-processing technique to extract the emission. The compression method makes use of the compressive growth of emission amplitude relative to the linear growth of the stimulus. The emission is defined as the complex difference between ear-canal pressure measured at one intensity and the rescaled pressure measured at a higher intensity for which the emission is presumed negligible. The suppression method defines the SFOAE as the complex difference between the ear-canal pressure measured with and without a suppressor tone at a nearby frequency. The suppressor tone is presumed to substantially reduce or eliminate the emission. The spectral smoothing method involves convolving the complex ear-canal pressure spectrum with a smoothing function. The analysis exploits the differing latencies of stimulus and emission and is equivalent to windowing in the corresponding latency domain. Although the three methods are generally assumed to yield identical emissions, no equivalence has ever been established. This paper compares human SFOAEs measured with the three methods using procedures that control for temporal drifts, contamination of the calibration by evoked emissions, and other potential confounds. At low stimulus intensities, SFOAEs measured using all three methods are nearly identical. At higher intensities, limitations of the procedures contribute to small differences, although the general spectral shape and phase of the three SFOAEs remain similar. The near equivalence of SFOAEs measured by compression, suppression, and spectral smoothing indicates that SFOAE characteristics are not mere artifacts of measurement methodology.     

A review of otoacoustic emissions

Otoacoustic emissions measured in the external ear canal describe responses that the cochlea generates in the form of acoustic energy. For the convenience of discussing their principal features, emitted responses can be classified into several categories according to the type of stimulation used to evoke them. On this basis, four distinct but interrelated classes can be distinguished including spontaneous, transiently evoked, stimulus-frequency, and distortion-product otoacoustic emissions. The present review details the findings that have been described for each emission type according to this classification schema. Additionally, the known features of emitted responses are discussed for both normally hearing and hearing-impaired humans and experimental animals, and with respect to their potential clinical applications. The findings reviewed here clearly indicate that future studies of otoacoustic emissions will significantly increase our understanding of the basic mechanisms of cochlear function while, at the same time, provide a new and important clinical tool.     

Influence of in situ, sound-level calibration on distortion-product otoacoustic emission variability

Standing waves can cause errors during in-the-ear calibration of sound pressure level (SPL), affecting both stimulus magnitude and distortion-product otoacoustic emission (DPOAE) level. Sound intensity level (SIL) and forward pressure level (FPL) are two measurements theoretically unaffected by standing waves. SPL, SIL, and FPL in situ calibrations were compared by determining sensitivity of DPOAE level to probe-insertion depth (deep and "shallow") for a range of stimulus frequencies (1-8 kHz) and levels (20-60 dB). Probe-insertion depth was manipulated with the intent to shift the frequencies with standing-wave minima at the emission probe, introducing variability during SPL calibration. The absolute difference in DPOAE level between insertions was evaluated after correcting for an incidental change caused by the effect of ear-canal impedance on the emission traveling from the cochlea. A three-way analysis of variance found significant main effects for stimulus level, stimulus frequency, and calibration method, as well as significant interactions involving calibration method. All calibration methods exhibited changes in DPOAE level due to the insertion depth, especially above 4 kHz. However, SPL demonstrated the greatest changes across all stimulus levels for frequencies above 2 kHz, suggesting that SIL and FPL provide more consistent measurements of DPOAEs for frequencies susceptible to standing-wave calibration errors.     

Comparison of distortion-product otoacoustic emission growth rates and slopes of forward-masked psychometric functions

Slopes of forward-masked psychometric functions (FM PFs) were compared with distortion-product otoacoustic emission (DPOAE) input/output (I/O) parameters at 1 and 6 kHz to test the hypothesis that these measures provide similar estimates of cochlear compression. Implicit in this hypothesis is the assumption that both DPOAE I/O and FM PF slopes are functionally related to basilar-membrane (BM) response growth. FM PF-slope decreased with signal level, but this effect was reduced or reversed with increasing hearing loss; there was a trend of decreasing psychometric function (PF) slope with increasing frequency, consistent with greater compression at higher frequencies. DPOAE I/O functions at 6 kHz exhibited an increase in the breakpoint of a two-segment slope as a function of hearing loss with a concomitant decrease in the level of the distortion product (L(d)). Results of the comparison between FM PF and DPOAE I/O parameters revealed only a weak correlation, suggesting that one or both of these measures may provide unreliable information about BM compression.