Transient emission suppression tuning curve attributes in relation to psychoacoustic thresholda) Erika M. Zettnerb) and Richard C. Folsom Department of Speech and Hearing Sciences, University of Washington, JG-15, Seattle, Washington 98195
共Received 13 July 2002; revised 15 January 2003; accepted 21 January 2003兲 Ipsilateral suppression characteristics of transiently evoked otoacoustic emissions 共TEOAEs兲 are described in relation to psychoacoustic threshold at 4000 Hz and the presence or absence of spontaneous otoacoustic emissions in 41 adults with normal hearing. TEOAE amplitudes were measured in response to 4000-Hz tonebursts presented in linear blocks at 40 and 50 dB SPL while puretone suppressors were introduced at a variety of frequencies and levels ipsilateral to and simultaneously with the tonebursts. Suppressors close to the toneburst frequency were most effective in decreasing the amplitude of the TEOAEs, while those more remote in frequency required significantly greater intensity for a similar amount of suppression. Consequently, characteristic tuning curve shapes were obtained. Tuning-curve tip levels were closely associated with the level of the toneburst and tip frequencies occurred at or above the toneburst frequency. Tuning-curve widths (Q10), however, varied significantly across subjects with similar psychoacoustic thresholds in quiet determined by a two-alternative forced-choice method. The results suggest that a portion of that variability may be explained by the presence or absence of spontaneous otoacoustic emissions in an individual ear. © 2003 Acoustical Society of America. 关DOI: 10.1121/1.1560191兴 PACS numbers: 43.64.Jb, 43.64.Kc 关BLM兴
I. INTRODUCTION
One of the main correlates of sensorineural hearing loss and, more specifically, outer hair cell dysfunction is a decrease in frequency resolution 共Bonding, 1979; Liberman and Dodds, 1984; Moore, 1986兲. A loss of frequency resolution is thought to contribute to speech perception difficulties in those with hearing loss 共Festen and Plomp, 1983; Stelmachowicz et al., 1985兲. We have used a noninvasive measure of peripheral frequency resolution, the suppression of otoacoustic emissions 共OAEs兲, to provide greater insight into the mechanisms for the auditory processes responsible for frequency resolution and sensitivity. Ipsilateral OAE suppression is a consequence of normal cochlear function and occurs at the preneural, mechanical stage of auditory transduction within the cochlea 共Cooper and Rhode, 1992; Patuzzi et al., 1984; Robles et al., 1991; Ruggero et al., 1992; Sellick and Russell, 1979兲. In addition, while suppression-tuning curves 共STCs兲 are not identical, they have been compared to psychoacoustic measures of frequency resolution 共Abdala et al., 1996; Zwicker and Wesel, 1990兲. Ipsilateral suppression of all types of OAEs in humans has been demonstrated 关reviewed by Harris and Glattke 共1992兲兴 with the majority of investigations reporting the suppression of distortion product OAEs 共DPOAE兲. These rea兲
This article is based on a dissertation submitted by the first author to the Graduate School of the University of Washington in partial fulfillment of the requirements for the Doctor of Philosophy degree. Portions of this work were presented in ‘‘Transient emission suppression tuning curves as a function of psychoacoustic threshold,’’ poster presentation at the Association for Research in Otolaryngology Midwinter Research Meeting, St. Petersburg Beach, Florida, February 1999. b兲 Correspondence to: School of Hearing, Speech, and Language Sciences, Ohio University, Athens, OH 45701. Electronic mail:
[email protected] J. Acoust. Soc. Am. 113 (4), Pt. 1, April 2003
ports measured emission suppression tuning curves under experimental conditions that can be assumed to have changed psychoacoustic threshold, but which did not all report threshold. These studies used the temporary ototoxic effects of salicylates, furosemide and noise 共Howard et al., 2002; Long et al., 1991; Martin et al., 1998; Zettner et al., 1996兲. Unexpectedly sharper tuning of DPOAE suppression was reported during salicylate toxicity 共Zettner et al., 1996兲. In addition, Martin et al. 共1998兲 used furosemide in rabbits to temporarily induce hearing loss and reported a trend for sharper DPOAE STCs during periods when cochlear function was disrupted. Similarly, Howard et al. 共2002兲 showed that DPOAE STCs were sharper during temporary, noiseinduced, DPOAE-level reductions in rabbit ears. Under the effects of salicylates, spontaneous OAE 共SOAE兲 STCs were shifted down in level, that is, lower suppression levels were needed to suppress the SOAE by the criterion amount but tuning was unchanged 共Long et al., 1991兲. Relevant work by Abdala 共2001兲 showed sharper DPOAE tuning in premature infants as compared to term infants and adults. DPOAE bandpass filter measures 共f2/f1 ratio sweeps兲 have also not succeeded in demonstrating changes in tuning following aspirin ingestion 共Brown et al., 1993兲. Since broader tuning would be expected with degraded or immature cochlear function, these studies argue for an alternate interpretation of STCs as estimations of cochlear tuning. Both the production and the suppression of each type of OAE are thought to reflect the same underlying mechanism. However, qualitative differences exist between STCs of each OAE type. STCs of DPOAEs, for example, often exhibit ‘‘double-tipped’’ curves and other shape irregularities not characteristic of other measures of frequency resolution 共Kummer et al., 1995; Taschenberger and Manley, 1998兲.
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© 2003 Acoustical Society of America
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There is increasing evidence that tuning curves obtained by suppressing DPOAEs represent the suppression of distortions generated at more than one site on the cochlear partition. This may explain at least some of the irregularities seen in DPOAE tuning curve shapes and highlights problems in estimating frequency resolution of a particular ear using DPOAE suppression 共Siegel et al., 2000; Stover et al., 1996; Talmadge et al., 1999兲. Suppression of transiently evoked OAEs 共TEOAEs兲 does not exhibit this complexity in tuning curve shape and may argue for a localized site for TEOAE generation 共Folsom et al., 1995; Kemp and Chum, 1980; Tavartkildadze et al., 1994; Wilson, 1980兲. While a precise correspondence is not expected between OAE and psychoacoustic threshold or tuning measures, there are a number of associations that have been reported. First, SOAEs are often associated with frequencies of threshold minima 共i.e., increased threshold sensitivity兲 共Burns et al., 1984; Long and Tubis, 1988兲. Second, sharper psychoacoustic tuning curves have been reported not only at SOAE frequencies 共Bright, 1985兲 but also a generalized sharpening effect of SOAEs on psychoacoustic tuning may occur at some frequencies 共Micheyl and Collet, 1994兲. Third, Micheyl and Collet also showed that ears with lower level overall TEOAE responses demonstrated sharper tuning at 2000 Hz. And fourth, presence of SOAEs has been shown to increase amplitude and latency of TEOAEs as well as dominate the spectral characteristics of TEOAEs 共Kulawiac and Orlando, 1995; Prieve and Falter, 1995兲. Given the evidence for an association between OAE, tuning, and threshold, there is sufficient rationale to investigate possible associations between TEOAEs STCs, psychoacoustic threshold, and SOAE. The broad goal of this work was to provide a clearer understanding of normal inner ear processes that contribute to low psychoacoustic threshold and sharp frequency resolution. The assumptions underlying this goal were 共1兲 that both threshold and frequency resolution are largely outer hair cell mediated characteristics resulting from frequency specific amplification to cochlear partition motion, 共2兲 that OAEs are by-products of the amplification provided by the outer hair cells, and 共3兲 that TEOAEs are generated by mechanisms within a confined region on the organ of Corti directly related to the frequency of the stimulus. The specific goal for this work was to investigate the relation between TEOAE STCs and psychoacoustic thresholds at 4000 Hz. TEOAE STCs in 41 adults with normal hearing were analyzed for tuning-curve width, tip level, and sideband slopes in relation to psychoacoustic threshold and TEOAE amplitude at the same frequency in the same group of ears. It was hypothesized that if TEOAE STCs accurately reflect properties of cochlear tuning, then broader curves were expected in ears with lower OAEs and poorer behavioral thresholds. Furthermore, since SOAEs probably contribute to certain aspects of TEOAEs, the potential for a generalized effect of synchronized time-domain averaged SOAEs 共SSOAEs兲 on suppression tuning curve characteristics was also investigated 共Kulawiec and Orlando, 1995; Prieve and Falter, 1995; Probst et al., 1986兲. 2032
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II. METHODS A. Participants
Forty-five participants between the ages of 20 and 48 years 共mean 31.07 years兲 were recruited without regard for gender or presence of SSOAE. All were screened by interview and video otoscopy for negative audiologic and otologic history, clear ear canals, and normal appearing tympanic membranes. The test ear was randomly selected. The criterion response amplitude of ⬎7 dB signal/noise using a 50 dB SPL toneburst 共described below兲 was necessary to conduct suppression experiments in order to provide sufficient response level for amplitude manipulation. In two subjects this criterion was not met with the first randomly tested ear, but was met in the opposite ear. Four subjects did not have adequate response amplitude in either ear and were not included in further testing. Of the 41 subjects remaining, 5 were male and 36 were female. Twenty-nine left ears were tested and 45% of these had SSOAEs. Twelve right ears were tested and 50% of these had SSOAEs. Presence of SSOAEs was determined by visual inspection of responses in the frequency domain display of emissions equipment described below. Tympanometry was used to confirm that middle-ear pressure was between ⫺25 and ⫹25 daPa and compliance was between 0.4 and 1.5 ml at the time of testing. In addition, standard audiometric thresholds were obtained for each of the 41 subjects to confirm normal hearing thresholds 共i.e., ⭐25 dB HL兲. Test sessions were conducted with participants seated in a recliner in a sound-treated booth and lasted approximately 2 h. B. Instrumentation and stimuli
A test frequency of 4000 Hz was chosen because it was hypothesized that greater variance in psychoacoustic threshold would be seen across subjects at the higher frequencies, thus increasing the probability that a relation between STC characteristics across threshold would be revealed. Further, this frequency was chosen to avoid noise below 1000 Hz often encountered when measuring TEOAEs and to avoid the microphone response roll-off beyond approximately 5500 Hz. 1. Psychoacoustic threshold
Psychoacoustic thresholds for a 4000-Hz tone were determined using a microcomputer interfaced with signal generation, modification instrumentation, and a participant response box. A 500-ms 4000-Hz tone was generated digitally by a Data Translation 共DT2821兲 D/A board. The 4000-Hz tone was then high-pass filtered at 3400 Hz and low-pass filtered at 5000 Hz. It was cosine ramped with a rise-fall time of 16 ms and duration of 468 ms. This signal was digitally attenuated 共Wilsonics, PATT兲, passed through a dual filter in series 共Kemo VBF8兲, amplified, and impedance matched. The signal was then delivered to the ear with an Etymotic ER-1 insert-phone fitted with a foam tip. Psychoacoustic threshold for this stimulus was obtained for each subject in a two-alternative forced-choice 共2AFC兲 paradigm using a oneup, two-down adaptive procedure 共Levitt, 1971兲 and halving the step size upon each reversal as delineated by parameter E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
estimation sequential testing 共PEST兲 rules 共Taylor and Creelman, 1967兲. Threshold was defined as the mean of ten reversals from the 2AFC procedure. 2. Otoacoustic emission measures
Three otoacoustic emission measures were recorded using the ILO92 system and TEOAE software 共Version 6, Otodynamics-Ltd.兲. These included 共1兲 SSOAEs, 共2兲 toneburst evoked TEOAEs 共described below兲, and 共3兲 a TEOAE STC generated by suppressing the TEOAE response with puretones presented ipsilaterally and simultaneously with the toneburst. This toneburst was an eight-cycle 50 dB SPL toneburst centered at 4000 Hz that was generated using ILO92 software stimulus generation options (frequency ⫽4000 Hz, length in cycles⫽8, amplitude⫽100, multiplex ⫽1). The toneburst was presented in linear-stimulus blocks of four identical tonebursts in terms of phase and amplitude. The low-level linear toneburst series minimized the potential for stimulus artifact. In addition, confirmation of complete toneburst cancellation was determined by complete suppression of OAEs in each ear with at least one suppressor tone. Calibration of the toneburst was carried out in each ear prior to the acquisition of each averaged response of 260 stimulus blocks by using the ‘‘check-fit’’ procedure of the ILO92 testing sequence. The two-receiver probe assembly supplied by Otodynamics for distortion-product emission recording was used in all conditions. Micropore tape applied over the probe assembly and pinna held the probe assembly in place for the duration of the session. The first receiver of the probe assembly delivered the toneburst. The second receiver delivered puretone suppressors used in tuning curve measurements. A cancellation procedure was necessary to eliminate the suppressor tone from the ear canal response before response averaging took place. Cancellation of the suppressor tone was achieved by intercepting the output of the microphone, electrically introducing a second puretone 共cancellation tone兲, and adjusting its level and phase to be 180° out of phase with the suppressor tone as verified visually on an oscilloscope. The cancellation tone was generated by splitting the suppressor tone and routing it to a custom-built phase shifter. This intercepted and ‘‘suppressor-cancelled’’ response was then averaged. Adjustments in the cancellation were always necessary after suppressor frequency and amplitude changes. Fine adjustments in phase and intensity were occasionally necessary to maintain adequate cancellation during averaging. A synthesizer/function generator 共Hewlett-Packard, Model 3325A兲 generated the suppressor tones and a programmable attenuator 共Tucker Davis, PA4兲 served to attenuate the tones. Suppressor tones were calibrated in each ear canal by using the spectrum analyzer option of the ILO92 DPOAE software to read the suppressor SPL at the plane of the probe. Frequency and intensity values were controlled manually. Suppressor frequencies were presented individually at 41-oct intervals from one octave below 4000 Hz to 21 oct above and at 18-oct steps around the tip of the tuning curve. Five to seven of the frequencies listed in Table I were selected for each curve depending on the ability to define a J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
TABLE I. List of suppressor frequencies used to construct the tuning curves. Distance in octaves relative to the probe frequency are listed. Octave interval
Frequency 共Rounded to the nearest Hz兲
⫺1 ⫺3/4 ⫺5/8 ⫺1/2 ⫺3/8 ⫺1/4 ⫺1/8
2000 2378 2594 2828 3084 3363 3668
Probe
4000
1/8 1/4 3/8 1/2
4362 4757 5187 5657
tuning curve tip in an individual ear. At a minimum, the goal was to adequately define the tip region, and then obtain points on both the low-and high-frequency sides that occurred at least 10 dB above the tip of the tuning curve. The tip of the tuning curve most often occurred within a 41 oct above the toneburst frequency so that suppressors up to a 21 oct above 4000 Hz adequately defined the high-frequency side of the tuning curves. Each suppressor frequency was presented in 5 or 10 dB SPL increments up to a maximum of 90 dB SPL. The stopping rules for increasing the level of the suppressor tone were 共1兲 when the emission level was below the noise floor, 共2兲 when the suppressor tone reached 90 dB SPL, or 共3兲 if harmonic distortion from the suppressor occurred 共visible in the averaged emission response window兲. Distortion occurred for low-frequency suppressors and was revealed as either noise 共uncorrelated energy兲 or emission 共correlated energy兲. Such responses were not included in further data analysis. The suppressor tone level in the ear canal was verified prior to and following each test session using the Otodynamics calibration-tones function. C. Data analyses
Suppression tuning curves were plotted off-line. Response amplitudes were defined as the dB SPL of a ⫾500-Hz band around the toneburst frequency 共i.e., 3500– 4500 Hz兲 occurring from 2.5 to 20 ms regardless of whether a SSOAE occurred in this frequency region. Thus, energy recorded outside the 4000-Hz response region was not considered in the analysis but SSOAE energy within the response region could have contributed to the response. A SSOAE occurred within this region in four subjects 共014, 038, 042, and 043兲 and all but one of these had response levels within one standard deviation of the mean. The OAE response level relative to an unsuppressed control response within the 1000-Hz-wide band was used to plot the rate 共or growth兲 of suppression at each suppressor frequency 关Fig. 1共a兲兴. Suppressor levels producing 1–10 dB of suppression for each frequency were plotted as a function of suppressor frequency, thus forming iso-suppression curves or tuning curves. A typical data set including 1 to 10 dB iso-suppression curves is shown in Fig. 1共b兲. Tuning curve tips were identified as the suppressor frequency requiring the lowest sound pressure level to suppress
E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
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FIG. 1. 共a兲 Sample set of seven suppression-rate curves from a representative subject 共029兲. The parameter is suppressor frequency. Points are plotted relative to an unsuppressed control response. Suppressor tones below 4000 Hz are shown with filled symbols, suppressor tones above 4000 Hz with open symbols, and the suppressor tone at 4000 Hz with asterisks. Dashed lines indicate noise levels relative to the response level. A horizontal line intersects each curve at the criterion level reduction of 6 dB. Vertical arrows at each of these points of intersection indicate the suppressor level causing the criterion level reduction. These suppressor levels were used to construct the tuning curve 关shown with a thick line in 共b兲兴. 共b兲 Typical iso-suppression curves 共subject 029兲 from 1 to 10 dB of suppression of a transiently evoked otoacoustic emission using a 4000-Hz toneburst at 50 dB SPL and puretone suppressors. Each line represents an equal amount of suppression effect across suppressor frequency. The criterion of 6 dB 共thick line兲 was used for measuring tuning curve width (Q10) and side slopes. Suppression of 1 and 10 dB was not obtained at the highest frequency 共5187 Hz兲 in this subject. Shown on a linear scale for easier visualization of individual curves. SSOAEs were present at 1306 Hz at ⫺18.2 dB SPL and at 1880 Hz at ⫺25.7 dB SPL.
the emission by the criterion of 6 dB. This criterion represented a halving of the TEOAE pressure and ensured that a significant amount of suppression was achieved. Further, this allows more direct comparison with neural tuning curves which have been frequently reported using a 6-dB criterion. Q10 values were calculated by dividing the bandwidth of the 6-dB isosuppression curve 10 dB up from the tip of the curve by the toneburst frequency 共4000 Hz兲. III. RESULTS A. Psychoacoustic thresholds
Psychoacoustic thresholds ranged from ⫺3.65 to 29.9 dB SPL (mean⫽6.43 dB SPL ⫾6.5). These correspond to thresholds better than 25 dB HL and within the range of normal hearing defined as better than 25 dB HL 共or 34.5 dB SPL兲. These data are listed in Table II. A one-tailed t-test showed that the average psychoacoustic threshold for ears without SSOAEs (mean⫽8.12 dB SPL) was not statistically different than ears with SSOAEs (mean⫽4.83 dB SPL) (t ⫽1.66; df⫽39; p⫽0.052). In addition, there was no clear relationship between threshold and SSOAE frequency and
the two subjects whose SSOAEs were within 150 Hz of the test frequency 共4000 Hz兲 demonstrated psychoacoustic thresholds within one standard deviation from the mean.
B. Otoacoustic emission responses
Representative transient OAE responses to the toneburst from three participants are shown in Fig. 2 and demonstrate the range of response levels and bandwidths observed in this study. In all cases, unsuppressed emission spectra were localized to the 4000-Hz frequency region. This is consistent with previously published data of toneburst evoked otoacoustic emissions 共Norton and Neeley, 1987; Xu et al., 1994兲. The average OAE response level was ⫺1.76 dB SPL 共⫾4.9 dB兲 and ranged from ⫺9.3 to 9.7 dB SPL 共Table II兲. Twenty-one of the 41 participants 共51%兲 had at least one SSOAE in the ears tested, and the remaining subjects had no measurable SSOAEs. Ears with SSOAEs demonstrated an average overall OAE response level of 1.05 dB SPL 共⫾4.1 dB兲, while ears without SSOAEs had an average OAE re-
TABLE II. Quantitative data 共means and standard deviations兲 from the study are presented for all participants and then separately for subjects with synchronized spontaneous otoacoustic emissions 共SSOAE兲 and without SSOAEs. Data are presented for the age of participants, psychoacoustic threshold 共dB SPL兲 at 4000 Hz using a two-alternative forced-choice paradigm, otoacoustic emission response level 共dB SPL兲 to a 50-dB SPL 4000-Hz toneburst, as well as transiently evoked otoacoustic emission suppression tuning curve characteristics 关tuning curve sharpness (Q10), tip level 共dB SPL兲, and slope of the lowand high-frequency sides 共dB/oct兲兴.
All participants N⫽41 Without SSOAE n⫽20 With SSOAE n⫽21
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Age
Psychoacoustic threshold
OAE level
Q10
Tip level
Low side slope
High side slope
mean sd
31.07 7.5
6.43 6.5
⫺1.76 4.9
4.44 1.3
49.22 7.8
⫺50.11 16.0
169.37 64.9
mean sd
30.05 7.7
8.12 7.8
⫺4.70 4.0
4.69 1.1
51.30 6.8
⫺51.66 13.1
163.58 69.1
mean sd
32.15 7.2
4.83 4.6
1.05 4.1
4.19 1.5
47.21 8.6
⫺48.64 17.5
174.89 63.6
J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
FIG. 2. Representative transient-evoked otoacoustic emission responses from three subjects to a 4000-Hz linear toneburst series presented at 50 dB SPL. Time waveforms 共0- to 20-ms window兲 on the left side of the figure are shown with the corresponding FFT to the right of the waveform. Overall response levels and S/N ratios are indicated above each of the time waveforms. Each response obtained contained 260 averages. Responses shown were measured using an ILO88/92 system 共Otodynamics Ltd兲. Frequencies and levels of synchronized spontaneous otoacoustic emissions 共not shown in response兲 for these ears are given below the time waveforms.
sponse level of ⫺4.70 dB SPL 共⫾4.0 dB兲. This difference was statistically significant (t⫽4.56; df⫽39; p⬍0.01, onetailed t-test兲.
C. Suppression tuning curves
Forty-one STCs were analyzed quantitatively for Q10 , tip frequency, tip level, and slopes of the low- and highfrequency tuning curve sides. STCs shown in Fig. 3 were arbitrarily sorted by tip level 共30–39.9, 40– 49.9, 50–59.9, and 60– 69.9 dB SPL兲. Twenty-nine 共71%兲 of the curves had tip levels between 40 and 59 dB SPL. Tuning curves were always single-tipped which occurred at or up to 41 oct above the toneburst frequency 共4000– 4757 Hz兲. The mean tip level was 49.22 dB SPL 共⫾7.8兲 with no significant difference between ears exhibiting SSOAEs and those without 共Table II兲 (t⫽1.67; df⫽39; p⫽0.098). The average Q10 was 4.44 共⫾1.3兲. The difference in Q10 between ears without SSOAEs was not statistically different from ears with SSOAEs (t ⫽1.24; df⫽39; p⫽0.11). All curves exhibited steeper highfrequency than low-frequency slopes (mean⫽169.37 dB/oct and ⫺50.11 dB/oct, respectively兲. These data are shown in relation to Q10 in Fig. 4. Steeper slopes are indicated by more
FIG. 4. Slopes 共dB/oct兲 of both high-frequency sides 共open circles兲 and low-frequency sides 共filled diamonds兲 of all tuning curves shown in Fig. 3 are plotted as a function of Q10 . The linear regression of Q10 on the low frequency slope was significant (p⬍0.01), but not on the high frequency slope.
positive values on the high frequency side 共open circles兲 and by more negative values on the low-frequency side 共filled diamonds兲. D. Suppression rate of growth
Representative iso-frequency or suppression-rate growth curves are shown in Fig. 1 from a typical participant 共#029兲. Suppressors lower in frequency than the toneburst produced little or no effect at low levels but showed a substantial suppressive effect beyond a critical level, which varied depending on its frequency. Suppressors higher in frequency than the toneburst gradually increased in effectiveness 共greater than 2 dB of suppression兲 beginning at very low suppressor levels 共⬍20 dB SPL兲 and into higher levels 共80 dB SPL兲. The slope of each frequency curve was estimated using a linear fit (R2 was 0.90 or better兲 and represented the rate of growth of suppression. Only points greater than 2 dB of suppression were included to avoid inclusion of data points showing normal fluctuations of response amplitude. Figure 5 shows the estimated slope of the input/output curves as a function of frequency pooled across all subjects since there was no difference in the rate of suppression for ears with versus without SSOAEs at any frequency (p⬎0.05 for each frequency兲. The rate and variability of suppression across tuning curves was greatest at lower frequencies and gradu-
FIG. 3. Otoacoustic emission suppression tuning curves for all subjects (n⫽41) arbitrarily sorted by tip level. Panel 共a兲 shows tuning curves 共⫺6 dB iso-suppression curves兲 with tip levels between 30 and 39.5 dB SPL; 共b兲 tip levels 40 to 49.5 dB SPL; 共c兲 tip levels 50 to 59.5 dB SPL; and 共d兲 tip levels 60 to 69.5 dB SPL. The toneburst was a 4000-Hz 50 dB SPL toneburst for all tuning curves. J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
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FIG. 5. Estimated rate 共growth兲 of suppression 共dB/dB兲 for each suppressor frequency used to construct the tuning curves. This was obtained by measuring the slope of a regression line fit to the iso-suppression curves 共refer to Fig. 1兲 from 2 dB of suppression. The open circles indicate individual data and the thick vertical lines show standard deviations.
ally decreased in the higher frequencies. For example, at 2378 Hz the mean rate of suppression was 0.71 dB/dB 共⫾0.35兲 and at 5187 Hz the mean rate of suppression was 0.01 dB/dB 共⫾0.08兲. E. Effect of toneburst level
The TEOAE suppression paradigm was tested using a 40 dB SPL toneburst in addition to the 50 dB SPL stimulus in 8 of the original 41 subjects in order to demonstrate the feasibility of using lower stimulus levels and to compare STCs from this study to other studies using DPOAE at multiple stimulus levels. This subgroup exhibiting ⬎7 dB S/N OAE responses to a 40 dB SPL toneburst were retested using this reduced stimulus level. Figure 6 shows the tuning curves obtained at this lower level which are matched with a tuning curve using the higher level toneburst from the same ear. Asterisks indicate the level of each SSOAE identified. Overall, use of a 40 dB SPL toneburst did not result in significantly sharper tuning curves 共mean Q10⫽5.47⫾2.27) than for a 50 dB SPL toneburst 共mean Q10⫽4.69⫾1.78) (t ⫽0.764; df⫽14; p⫽0.228, one-tailed test兲. Sharper tuning was measured in three subjects, broader tuning in one subject and essentially no difference was measured in four subjects. However, tip level was significantly lower using the 40-dB SPL toneburst 共mean 35.25 dB SPL兲 than the 50-dB SPL toneburst 共mean 46.44 dB SPL兲 (t⫽3.03; df⫽14; p⬍0.01). This represents a mean tip-level difference of 11.19 dB 共⫾5.6兲 and corresponded closely with the 10-dB difference in toneburst levels. In five cases, tip frequency was unchanged with use of the 40 dB SPL toneburst, in two cases it was lower, and one it was higher than when a 50 dB SPL toneburst was used. F. Threshold versus OAE response level
Figure 7共a兲 shows the relation between emission response levels and psychoacoustic threshold for ears with ver2036
J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
FIG. 6. TEOAE suppression tuning curves from eight subjects for whom both high- and low-toneburst levels were used. Thin lines indicate suppression tuning curves obtained using a 50 dB SPL 4000-Hz toneburst whereas thick lines indicate a 40 dB SPL toneburst was used. Asterisks indicate frequencies and corresponding amplitudes of synchronized spontaneous otoacoustic emissions. Secondary axis indicates SSOAE level in dB SPL.
sus without SSOAEs. Overall, higher toneburst evoked OAE response levels were obtained when SSOAEs were present 共filled squares versus open diamonds兲 (average⫽1.05 dB SPL versus ⫺4.70 dB SPL兲. In both groups the highest OAE response levels were obtained when psychoacoustic threshold was low and levels decreased with increased thresholds. This relation was significant in both groups (r⫽⫺0.640, df ⫽20, p⬍0.01 with SSOAE; r⫽⫺0.490, df⫽19, p⬍0.05 without SSOAE兲. G. Q10 versus threshold
Figure 7共b兲 shows the relation of tuning curve sharpness (Q10) as a function of psychoacoustic threshold in ears with and without SSOAEs. A wide range of Q10 values was measured across subjects, ranging from 2.29 to 7.84. In addition, there was substantial overlap in Q10 values across the two groups, particularly at lower thresholds. Only a few ears E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
FIG. 7. 共a兲 Transient OAE response levels to a 50 dB SPL toneburst as a function of psychoacoustic threshold for a 4000-Hz tone in ears with synchronized spontaneous otoacoustic emissions 共SSOAE兲 共filled squares兲 and ears without SSOAEs 共open diamonds兲. 共b兲 Tuning-curve sharpness (Q10) as a function of psychoacoustic threshold for a 4000-Hz tone obtained using a two-alternative forced-choice paradigm. Ears with SSOAEs 共filled squares兲. Ears without SSOAEs 共open diamonds兲. 共c兲 OAE response levels to a 50 dB SPL 4000-Hz toneburst as a function of Q10 in ears with SSOAEs 共filled squares兲 and ears without SSOAEs 共open diamonds兲. Solid trend lines shown for subjects with SSOAEs, dotted trends lines shown for subjects without SSOAEs. Asterisks indicate significant regression analyses.
were tested with thresholds above approximately 10 dB SPL, and none of these had SSOAEs. Q10 was significantly correlated with threshold from the group without SSOAE (r ⫽0.645, df⫽19, p⬍0.01). Statistical significance was maintained with removal of the outlying data point at 29 dB SPL (r⫽0.460, df⫽18, p⬍0.05). An opposite trend was observed in ears with SSOAEs, that is higher Q10 was observed with lower thresholds (r⫽⫺0.031; df⫽17; p⫽0.904). J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
FIG. 8. Suppression tuning curve tip level in relation to 共a兲 psychoacoustic threshold, 共b兲 Q10 , and 共c兲 OAE response level. Data from ears with synchronized spontaneous otoacoustic emissions 共SSOAE兲 are shown with filled squares; ears without SSOAEs are shown with open diamonds. Asterisks indicate where significant regression analyses were obtained.
H. Q10 versus OAE response level
Figure 7共c兲 shows that the pattern for Q10 versus OAE response level also seemed to depend on presence or absence of SSOAEs. Without SSOAEs, Q10 values were significantly higher when OAE response levels were low (r⫽⫺0.503, df⫽19; p⬍0.05). This contrasted with ears with SSOAEs where low Q10 values tended to occur with low OAE response levels (r⫽0.302; df⫽20; p⫽0.184). I. Tip level
Tuning curve tip level was examined in relation to three parameters: psychoacoustic threshold, Q10 , and OAE re-
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sponse level 共Fig. 8兲. Tip level and psychoacoustic threshold were not related in a meaningful way in either group 关Fig. 8共a兲兴. However, tip level was significantly related to Q10 in ears with SSOAEs, such that lower tip levels were associated with higher Q10 values (r⫽⫺0.599; df⫽20; p⬍0.01) 关Fig. 8共b兲兴. A clear relationship between Q10 and tip level in ears without SSOAEs was not found. Lastly, the data from ears without SSOAEs suggest that lower tip levels occurred when OAE response levels were high 关Fig. 8共c兲兴 (r ⫽⫺0.443; df⫽19; p⫽0.051). No relation was seen between OAE response level and tip levels in ears with SSOAEs (r⫽⫺0.297; df⫽20; p⫽0.192). IV. DISCUSSION
matched by an average downward shift in tip level by 11.19 dB without a significant change in tuning 共Fig. 6兲. This contrasts with findings from Kummer et al. 共1995兲 and Harris et al. 共1992兲 who reported a decrease in DPOAE tuning curve width with lower primary tone levels. In the current study, tip frequencies of the 6-dB isosuppression curves occurred at and sometimes as much as 41 oct above the stimulus frequency 共4000 Hz兲. And, increasing the suppression criterion from 1 to 10 typically resulted in a downward frequency shift in the tuning curve tip 关see Fig. 1共b兲 for an example兴, a trend that Kummer et al. 共1995兲 has also reported. This shift down in tip frequency with increasing suppression criterion has been noted in basilar membrane vibration measures as well 共Rhode, 1978; Sellick et al., 1982兲.
A. General characteristics of TEOAE STCs
Tuning curves obtained by ipsilateral simultaneous suppression of toneburst evoked OAE were qualitatively similar to previously published neural and psychoacoustic tuning curves 共e.g., Liberman and Dodds, 1984; Vogten, 1974兲. TEOAE STCs were asymmetrical, V-shaped, and in many cases, exhibited a low-frequency tail. Characteristics of the STCs in this study are comparable to human TEOAE STCs previously published and are similar to STCs using other types of emissions as well 共Kemp and Chum, 1980; Wilson, 1980; Kummer et al., 1995; Abdala et al., 1996兲. In addition, the shapes of the suppression rate curves were consistent with previously published TEOAE suppression experiments 共e.g., Zwicker and Wesel, 1990兲, with DPOAE suppression experiments 共e.g., Abdala, 1998; Kummer et al., 1995兲 and SOAE suppression experiments 共e.g., Rabinowitz and Widin, 1984兲. Overall, however, the rate of suppression at each frequency appeared lower 共Fig. 5兲 compared to previously published data especially below the toneburst frequency 共Abdala, 1998; Kummer et al., 1995兲. The average Q10 for the 6-dB isosuppression tuning curves in this study was 4.44 共⫾1.3兲 and ranged from 2.88 to 7.84. These values compare well with previously published works in humans at similar frequencies and levels to those used in the current study. Folsom et al. 共1995兲 reported an average Q10 in five adults of 3.52 共range 2.56 – 4.44兲 for TEOAE STCs using a nonlinear 70-dB SPL toneburst at 4000 Hz. There are a few studies that offer Q10 measures of DPOAE STCs in humans using frequencies similar to those in the current study. Specifically, Kummer et al. 共1995兲 reported Q10 values between about 3.0 and 5.3 at 4000 Hz 共f1 and f2 levels of 55 and 40 dB SPL, respectively兲. Abdala 共1998兲 and Abdala et al. 共1996兲 reported Q10 values between approximately 2.5 and 4.25 at 3000 Hz and between 3.0 and 4.5 at 6000 Hz 共65 and 50 dB SPL for f1 and f2 stimulus levels兲. And, Harris et al. 共1992兲 obtained an average Q10 of 2.97 using slightly higher stimulus levels in the 4000-Hz region. Studies using laboratory animals, including those of the barn owl and rabbit, have also shown Q10 values in the same range at this frequency 共Martin et al., 1998; Taschenberger et al., 1998兲. Seventy-one percent 共71%兲 of the TEOAE STCs using a 50 dB SPL stimulus had tip levels within 10 dB of the stimulus level. A decrease in the stimulus level by 10 dB was 2038
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B. Contributions of SSOAEs to TEOAE STCs
One objective of this study was to examine effects of SOAE on TEOAE STC attributes since SOAEs are known to affect amplitude, spectral, and latency characteristics of TEOAEs 共Kulawiec and Orlando, 1995; Prieve and Falter, 1995兲. Furthermore, STCs obtained by suppressing DPOAEs and SOAEs often exhibit a multipeaked and irregular fine structure 共Bargones and Burns, 1988; Kummer et al., 1995; Zettner et al., 1996兲. This fine structure may be the result of complex interactions between the suppressor tones and emissions. For example, multiple SOAEs in an ear have been shown to interact with each other by generating additional DPOAE in addition to demonstrating reciprocal suppression 共Burns et al., 1984兲. In addition, externally presented tones can release SOAEs from suppression 共Rabinowtz and Widin, 1984兲. Whether presence of additional SOAEs specifically influence characteristics of DPOAE STCs is not clear. While Kummer et al. 共1995兲 did not find a consistent effect of SOAEs on STC shape, they did report a number of shape irregularities when SOAEs were present. And, Abdala et al. 共1996兲 reported a greater proportion of multipeaked DPOAE STC in infant ears, which can exhibit greater numbers of SOAE 共Burns et al., 1992兲. In contrast, Harris et al. 共1992兲 reported that presence of SOAE did not appear to affect rate of suppression nor characteristics of the tuning curves. The TEOAE STCs in the current study did not demonstrate shape irregularities often demonstrated by DPOAE and SOAE generated STCs. Though TEOAE STCs obtained in this study appeared unaltered in shape by SSOAEs, their presence did influence the relation of Q10 with OAE response. Ears without SSOAEs showed significantly greater tuning when OAE response level was low. This was in contrast to ears with SSOAEs tended to exhibit greater STC sharpness when OAE response level was high. This suggests that presence of any SSOAE may influence tuning curve sharpness. Since finer tuning and high-level emissions are both expected to be associated with low thresholds, it was reasonable to expect that high level OAEs would be associated with sharper suppression tuning, regardless of presence or absence of SOAEs. Thus, the results found for subjects without SOAEs are unexpected and an adequate explanation for this finding is lacking. E. M. Zettner and R. C. Folsom: TEOAE suppression tuning curves
An error in categorizing subjects on the basis of presence or absence of SSOAE may have occurred for subjects who did not have readily identifiable SSOAE. It is possible that some of these subjects had low level SSOAE below the noise floor of the recording. The likelihood for this kind of misclassification increased in subjects with lower psychoacoustic thresholds as this could have indicated a minimum in their threshold microstructure often associated with SOAE 共Long and Tubis, 1988兲. C. Relation of psychoacoustic threshold to TEOAE STC parameters
Psychophysical measures of frequency resolution have shown a wide range of frequency resolution characteristics across ears with similar thresholds 共Tyler, 1986; Bergman et al., 1992兲. As a peripheral response, the OAE STC excludes processing across much of the auditory system that could contribute to the variability of psychophysical measures 共reviewed by Moore, 1986兲. Nevertheless, a wide range in tuning was also observed for the subjects in this study with relatively similar psychoacoustic thresholds. Unlike neural or psychophysical methods, OAE STCs are shaped by individual output impedances of the middle ear. However, as output impedance functions are broadly tuned, it is not probable that this was a significant source of variability on the TEOAE STC width values observed in this study. The methodology used for calibration of the suppressor tones was also a possible source for variability in tuning curve characteristics seen in this study. Since the stimuli were calibrated in each ear at the plane of the probe rather than at the tympanic membrane, individual frequencydependent ear canal properties would have resulted in suppressors at different frequencies reaching the cochlea at different levels. While the same error would have existed for both the 4000-Hz tone burst and the suppressors at and close to 4000 Hz, the amount of error at other frequencies may have varied across subjects and contributed to measurable differences in suppression tuning. It was also reasonable to speculate that the participants with similar thresholds in this study did not represent a homogeneous group. West and Evans 共1990兲, for example, showed that psychophysical tuning curves are sometimes broader before measurable changes in behavioral thresholds occur. Thus, some of the Q10 variability across subjects with similar threshold may have indicated a real difference in frequency resolution characteristics of individual ears. Despite evidence for a common active cochlear process underlying evoked otoacoustic emission generation and auditory frequency selectivity, little work has been published that directly tested this association. Micheyl and Collet 共1994兲 investigated the relation between frequency resolution and the level of evoked OAE in subjects without SOAEs and found sharper psychoacoustic tuning curves 共at 2000 Hz兲 in ears with lower OAE response levels. This finding is similar to results in the present study at 4000 Hz. That is, in ears without SSOAEs, sharper STCs were obtained when OAE response level to the toneburst was low 关Fig. 7共c兲兴. This contradicts with the notion that large OAEs and sharper tuning result from a more active cochlear amplifier and that smaller J. Acoust. Soc. Am., Vol. 113, No. 4, Pt. 1, April 2003
OAEs result when there is decreased activity. This may reflect the same process influencing the paradoxically sharper tuning that some researchers have reported during salicylate ototoxicity, temporary noise-induced hearing loss, and application of furosemide 共Howard et al., 2002; Martin et al., 1998; Zettner et al., 1996兲. D. Site of suppressive effects
There is evidence to suggest that TEOAE are composed of intermodulation distortion energy generated over a widely distributed area of the cochlear partition. Withnell et al. 共2000兲, for example, found that damage to the basal region of the cochlea produced changes in the amplitude and latency characteristics of low frequency TEOAE. Temporal patterns of TEOAE from normal and noise-induced impaired human cochlea studied by Avan et al. 共1993兲 also indicate that energy may be generated by regions as far as 1 to 1.5 oct from its tuned location on the basilar membrane and contribute to the overall response. Therefore, intermodulation distortion may add to TEOAE energy generated locally. The extent to which one component dominates the emitted energy may be determined by individual physical cochlear characteristics. On the other hand, a puretone suppressor stimulates a discrete location and its suppressive effects are local. While TEOAE energy may come from a distributed region, the suppression-tuning curve reflects a suppression effect 共or synchronization effect as described by Neumann et al., 1997兲 occurring at a characteristic frequency. Therefore, even though TEOAE may consist of energy generated over a widely distributed area of the cochlear partition, STC can be interpreted as indicating tuning at a localized place on the partition. V. CONCLUSIONS
OAE suppression seems to provide a direct and noninvasive means for studying initial auditory stages of frequency resolution otherwise relatively inaccessible in humans. Many of the TEOAE STC characteristics described in this study were qualitatively similar to tuning curves obtained using DPOAEs and with other auditory responses. Yet, findings in this study and DPOAE STCs from other studies contradict with expected results. That is, the quantitative characteristics were not always related to psychoacoustic threshold and OAE response level in a clear and meaningful way. The presence of SSOAEs often existed with results distinct from the results from ears without SSOAEs. Specifically, in ears without SSOAEs, poorer psychoacoustic thresholds were associated with sharper tuning, whereas poorer thresholds were associated with broader tuning when SSOAEs were present. Further, the relation between Q10 and OAE response level and tuning curve tip level also depended on the presence or absence of SSOAEs. At least in ears without SSOAEs, frequency selectivity appeared better in ears with lower OAE response levels. These issues must be resolved in order to interpret the information gained from the suppression of otoacoustic emissions as measures of peripheral frequency resolution.
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ACKNOWLEDGMENTS
This research was supported by NIDCD Grant No. PO1.DC00520 and NIDCD Training Grant No. T32DC00033-06. The authors gratefully acknowledge two anonymous reviewers for their careful reading and useful suggestions. The authors would also like to thank Li Xu, Ph.D., for graphical assistance, numerous discussions, and readings of early versions of this document.
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