C urrent proposals for the identification

J Am Acad Audiol 9 : 315-331 (1998) Objective Evaluation of Aided Thresholds Using Auditory Steady-State Responses Terence W. Picton* Andree Durieux-Smiths Sandra C. Champagnet JoAnne Whittinghamt Linda M. Morant Christian Gigueret Yves Beauregardt Abstract Auditory steady-state responses to amplitude-modulated tones with modulation frequencies between 80 and 105 Hz can be recorded when multiple stimuli are presented simultaneously through a soundfield speaker and amplified using a hearing aid. Responses were recorded at carrier frequencies of 500, 1000, 2000, and 4000 Hz in a group of 35 hearing-impaired children using hearing aids. The physiologic responses were recorded at intensities close to the behavioral thresholds for sounds in the aided condition, with average differences between the physiologic and behavioral thresholds of 17, 13, 13, and 16 db for carrier frequencies 500, 1000, 2000, and 4000 Hz. The technique shows great promise as a way to assess aided thresholds objectively in subjects who cannot reliably respond on behavioral testing. Key Words: Auditory steady-state responses, evoked potential audiometry, hearing aids Abbreviations : ABR =auditory brainstem response, MASTER= multiple auditory steadystate responses, OAE = otoacoustic emission C urrent proposals for the identification and treatment of hearing-impaired children (NIH Consensus Committee, 1993 ; Joint Committee on Infant Hearing, 1994) recommend that hearing-impaired infants should be detected within the first few months of life and that treatment should be initiated by the age of 6 months. Several methods have been proposed and evaluated for detecting hearing impairment in infants. These include the use of auditory brainstem responses (ABRs) (e.g., Hyde et al, 1990 ; Durieux-Smith et al, 1991 ; Galambos et al, 1994) and otoacoustic emissions (OAEs) (e.g., Smurzynski et al, 1993 ; White and Behrens, 1993). Once the hearing-impaired infant has been detected, however, very little is recommended *Rotman Research Institute at Baycrest Centre for Geriatric Care, University of Toronto, Toronto, Ontario ; tprogram in Audiology and Speech-Language Pathology, University of Ottawa, Ottawa, Ontario Reprint requests : Terence W. Picton, Rotman Research Institute, Baycrest Centre for Geriatric Care, 3560 Bathurst Street, Toronto, Ontario, Canada M6A 2E1 about treatment other than that it should be available. The initial treatment of a hearing-impaired infant will involve the fitting of hearing aids. In older children and adults, who can respond easily to audiometric testing, hearing aids can be selected and adjusted according to their subjective responses to sounds. The "functional gain" of the hearing aid for any particular stimulus can be calculated as the difference between the thresholds for that stimulus with and without the aid (Hawkins and Haskell, 1982). Since an infant cannot provide reliable behavioral responses to auditory stimuli, functional gain cannot be measured. Objective techniques such as real-ear probe-tube measurements can also be used (Harford, 1980 ; Seewald et al, 1985 ; Moodie et al, 1994). These assess real-ear coupler differences and real-ear "insertion gain," which is determined with the hearing aid in place and is equivalent to functional gain (Dillon and Murray, 1987). These real-ear measures, however, are only useful if one knows the actual unaided audiometric thresholds of the patient so that the hearing aid can be adjusted to match

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 prescriptive targets (Stelmachowicz and Lewis, 1988). Furthermore, the placement of a probe tube in babies and uncooperative patients can be challenging. An objective method to measure the benefits of a hearing aid in patients where behavioral thresholds and real-ear measurements are difficult to obtain would be very helpful. Auditory evoked potentials have been used in the past to assess hearing aids. Most reports considered using the click-evoked ABR to assess how well a hearing aid is working (Kileny, 1982 ; Hecox, 1983 ; Mahoney, 1985 ; Beauchaine et al, 1988). The general aim was to adjust the hearing aid until the latency of the ABR wave V decreased to within normal range. These procedures were limited since the click ABR is mainly related to the high-frequency gain and since the correlation between wave V latency and loudness is low, particularly when there is a sloping hearing loss (Serpanos et al, 1997). Many technical problems have been reported in the use of ABR for the evaluation of amplification. Since the click is very brief, it can be significantly distorted both in the soundfield speaker and in the hearing aid. The resultant stimulus artifacts can obscure the interpretation of the response (Kileny, 1982 ; Hall and Ruth, 1985 ; Mahoney, 1985). Other investigators have used the amplitude intensity function of the unaided clickevoked ABR to predict the optimal gain for a hearing aid (Kiessling, 1982 ; Davidson et al, 1990). However, this approach is problematic since the amplitude of the ABR is only loosely correlated with loudness. In general, hearing aids handle rapidly changing acoustic stimuli (such as those used to evoke the ABR) differently from more continuous stimuli such as speech, and it is difficult to predict the steady-state characteristics of hearing aids from onset responses (Gorga et al, 1987). The auditory steady-state responses (Galambos et al, 1981 ; Rickards and Clark, 1984 ; Stapells et al, 1984) offer several advantages over transient evoked potentials like the ABR. A steady-state response is evoked by regularly repeating stimuli. After the initial few stimuli, the response stabilizes and thereafter contains constituent frequency components that remain constant in amplitude and phase over time (Regan, 1989). In the auditory system, these responses can be evoked by amplitude-modulated tones, which are frequency specific and stable over time. They are therefore unlikely to be distorted by amplification in either a soundfield speaker or a hearing aid. The most widely recorded of the auditory steady-state responses is the 40-Hz potential initially described by Galambos et al (1981). The best modulation rates for audiometric purposes, however, may be between 75 and 110 Hz, because at these rates the responses are not significantly affected by sleep (Cohen et al, 1991) and can be reliably recorded in infants (Aoyagi et al, 1993; Rickards et al, 1994 ; Lins et al, 1996). Several papers have reported that these rapid steady-state responses can be recorded down to near-threshold intensities in both normal and hearingimpaired subjects (Aoyagi et al, 1994 ; Rance et al, 1995 ; Lins et al, 1996). One particular advantage of the steadystate approach is that responses to several amplitude-modulated stimuli can be recorded simultaneously without any loss in the amplitude of the response (tins and Picton, 1995 ; John et al, 1998). The multiple-response technique derives from one used in the visual system to record responses to different regions of the visual field (Regan and Cartwright, 1970 ; Regan, 1989). In the auditory system, several carrier frequencies are presented simultaneously with each carrier amplitude modulated according to its own signature frequency. The recorded response then contains activity at each of the signature modulation frequencies. This technique makes it possible to record the responses to four (or eight) stimuli in the same time that it takes to record one. The multiple auditory steady-state response (MASTER) technique should therefore allow for the rapid assessment of threshold at multiple audiometric frequencies. This paper investigates the possible use of the MASTER technique in the assessment of aided thresholds in sound field. Three groups of subjects were evaluated for this report. Normal subjects were studied in two experiments. The first investigated whether estimated thresholds were similar when stimuli were presented alone or in combination. The second determined whether the responses could be accurately recorded in normal subjects without hearing aids using soundfield speakers rather than earphones. This experiment was designed to make sure that the responses were not distorted by the soundfield speakers. The second group of subjects consisted of children with hearing aids who were able to cooperate with behavioral testing. The recordings in these subjects investigated whether steady-state responses could accurately assess thresholds when sounds were amplified using hearing aids. A third group of 316

Objective Evaluation of Aided Thresholds/Picton et al subjects consisted of three hearing-impaired children who were fit with hearing aids but who were unable to yield reliable behavioral responses to sound : two hearing-impaired infants in whom treatment with hearing aids was being initiated and a developmentally delayed child in whom amplification was being used on a trial basis. These initial studies evaluated the feasibility of using this technique with these populations. Subjects METHOD Three groups of subjects participated in these experiments: 1. Normal subjects participated in the first two experiments. The first used 10 subjects (6 female) with normal hearing (less than 20 db HL at all frequencies between 500 and 4000 Hz). These subjects varied in age between 13 and 40 (mean 29) years. The second experiment used 10 female subjects with normal hearing. The age range of these subjects was between 23 and 43 (mean 31) years. These subjects were coded as N1-N10 ("normal"). 2. The second group of subjects consisted of 35 children with moderate hearing impairment who were using hearing aids and were being followed by the Audiology Department at the Children's Hospital of Eastern Ontario. These subjects were coded as A1-A35 ("aided"). The age range of these subjects was between 11 and 17 years with a mean age of 15. There were 14 female subjects and 21 male subjects. Only one ear of each subject was tested. This was selected as the ear with the best pure-tone average. In the case of symmetric losses, one ear was randomly selected. The untested ear was occluded with a foam plug. In all, 15 left ears and 20 right ears were tested. The unaided puretone average calculated for the frequencies 500, 1000, 2000 Hz varied between 23 and 78 db with a mean of 56 db HL. The audiometric configuration was flat (threshold differences between 500 and 2000 or 4000 Hz being less than 30 db) in 26 cases and sloping in 9 cases. 3. A small third group of subjects included three children who were being fitted with hearing aids and who could not provide reliable responses to sounds. These subjects were coded XI-X3 ("extra"). Two of the subjects were newly identified hearingimpaired infants under 1 year of age who were being fitted with hearing aids in the Audiology Program at the Children's Hospital of Eastern Ontario. One infant (X1) was seen at 51/2 months of age. ABR results showed 60 db HL thresholds to click stimulation for each ear. Immittance audiometry was incomplete, but bone-conduction ABRs indicated that the hearing loss was most likely sensorineural in origin. OAEs were absent bilaterally. Binaural amplification was recommended. This infant's left ear was tested to assess aided thresholds. The second infant (X2) was assessed at 8 months of age. She was born prematurely, developed respiratory distress syndrome, and was on assisted ventilation for several days in the neonatal period. Click ABR thresholds of 30 db nhl were obtained for each ear. Otoscopic examination indicated no signs of middle ear effusion. However, OAEs were consistently absent. Auditory steady-state responses for the right ear showed consistent responses at 1000, 2000, and 4000 Hz with thresholds at 50, 70, and 40 db SPL but no responses at 500 Hz at intensities as high as 80 db SPL. We concluded that this child had a mild sensorineural hearing loss with better thresholds in the higher frequencies (which might explain the low click ABR thresholds) and initiated low-gain amplification on a trial basis. This infant's right ear was tested to assess aided thresholds. In addition, this third group included a 9-year-old girl (X3) with severe developmental delay and seizures. The etiology of her disorder was not known. Magnetic resonance imaging showed cerebral atrophy and some periventricular demyelination. The child's course did not fit with any known leukoencephalopathic syndrome and the findings were therefore attributed to cerebral dysgenesis, possibly related to prenatal brain damage. There was severe visual dysfunction, perhaps caused by cortical blindness. This girl had been seen on several occasions in Audiology because of a suspicion of a bilateral sensorineural hearing loss. No consistent behavioral responses to narrow bands of noise, warble tones, and speech, presented at levels of up to 80 db HL, had ever been noted in sound field. The click ABR showed an abnormal waveform

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 morphology with a possible wave V identified in the right ear at 80 db nhl. Transient and distortion-product OAEs were consistently absent in the presence of normal middle ear pressure and tympanic membrane mobility. Trial amplification was initiated but it was impossible to evaluate how well this child was hearing with the hearing aids. This child's right ear was tested to assess aided thresholds. Stimuli The stimuli were sinusoidally amplitudemodulated tones. The carrier frequencies of these tones were 500, 1000, 2000, and 4000 Hz. The depth of modulation was 100 percent for each of the stimuli. Each carrier frequency had its own signature modulation frequency: 80.9, 88.9, 96.9, and 104.8 Hz for the 500-, 1000-, 2000-, and 4000-Hz carrier frequencies, respectively. The four stimuli were summed together and presented simultaneously (Fig. 1). In certain situations, we elected to present only one or two of the stimuli. The timing of both stimulation and recording was exactly synchronized in order for the fre- Carrier Modulation Time Frequency 500 80.9 1000 88.9 2000 96.9 aooo loan ~_., ~.,go,-~ Combined Stimulus 0 30 msec 0 5000 Hz Figure 1 Stimuli used to obtain multiple auditory steady-state responses. The left side of the figure represents the acoustic waveforms seen in the time domain over the first 30 msec of the stimulus buffer. Each carrier frequency is amplitude modulated by its signature modulation frequency- The four different signals are then added together to form the combined stimulus that is presented to the subject. On the right of the figure are shown the amplitude spectra for these signals (measured over the full stimulus buffer) and displayed between 0-5000 Hz. For each stimulus, the spectrum shows energy at the carrier frequency and at two side bands separated from the carrier frequency by the modulation frequency. The spectrum of the combined stimulus represents the sum of the four different amplitude spectra. L quency analysis to detect the appropriate responses (John et al, 1998). The stimuli were therefore adjusted so that there was an integer number of both the carrier frequency and the modulation frequency within a 754-msec buffer. Two identical buffers were then created and we rotated through one of these buffers every time a 754-msec "section" was recorded. The output of the digital analog converter was then amplified in a Madsen Micro 5 Audiometer and presented to the subject through either a TDH39 earphone or a Madsen FF73 soundfield speaker. When the presentation was sound field, the nontested ear was occluded with a foam plug. Testing was carried out in a single-walled audiometric test room (Industrial Acoustics Company). The acoustic environment of such a room is quasi free field (ISO, 1989). The ambient noise levels in the room complied with the specifications of ANSI S3.1 (1991) for audiometric testing conditions with ears not covered. During the test, the subjects were seated comfortably in an armchair located near the center of the room and at approximately 1.25 meters from the loudspeaker. The subject's head faced the loudspeaker (0 azimuth) at all times. The heights of the loudspeaker and subject were adjusted so that the center head position was always on the speaker axis. The test stimuli were calibrated using the procedures outlined in Walker et al (1984), ISO DP 8253/2 (1989), Beynon and Munro (1995), and ANSI S3.6 (1996) for quasi free field conditions. The sound field was determined for each FM stimulus with the test subject and subject's armchair absent. Sound pressure level (SPL) was measured at the reference test point and at six neighboring positions : 15 cm to the left and right of, 15 cm above and below, and 10 cm anterior and posterior to the reference point. The stimuli were measured using a Bruel and Kjaer Model 2209 sound level meter with a 1-inch Model 4145 condenser microphone. The mean of the seven SPL measurements was used as the calibrated level for each stimulus. The 1000- and 2000-Hz stimuli had a level 5 db greater than the 500- and 4000-Hz stimuli for an equivalent electrical input to the speaker. For simplicity, the figures will identify the stimuli using only one SPL. At "60 db SPL," the 500- and 4000-Hz tones were 60 db SPL and the 1000- and 2000-Hz tones 65 db SPL. Correct intensities were used in the calculations of mean thresholds and in the statistical evaluations. The standard deviation of the seven SPL measurements was used to estimate the spatial 318

Objective Evaluation of Aided Thresholds/Picton et al variability of the sound field for each stimulus. Our standard deviations were very similar to those reported by Beynon and Munro (1995) in another typical audiometric room under the same measurement conditions, except for the smaller standard deviation in our study at 4000 Hz. Beynon and Munro (1995) suggested using two standard deviations as an estimate of the error in threshold measurement arising from the soundfield variability. For our stimuli, this error was about ±3.7 db (500 Hz), -3.4 db (1000 Hz), ±2.3 db (2000 Hz), and ±1.8 db (4000 Hz). one subject, the artifact rejection procedure was turned off and extra averaging performed to attenuate the electrical noise. Analysis The averaged 12-second sweep was transformed into the frequency domain using a Fast Fourier Transform (FFT). The resultant Fourier coefficients at the modulation frequencies were then converted into measurements of amplitude and phase (John et al, 1998). The ampli- Recordings All subjects were encouraged to relax during the recording and most were able to drowse or sleep. The babies were tested when they were asleep. Subject X3 was tested while awake. Electroencephalographic signals were recorded between the vertex and the posterior midline neck halfway between the inion and the vertebra prominens. A ground electrode was placed on the lateral neck. In babies, the neck electrodes were not easy to maintain ; the reference electrode was therefore placed on the mastoid ipsilateral to the ear being tested and the ground electrode on the forehead. The recordings were amplified and filtered with a bandpass of 10 to 300 Hz. The signals were then analog-digital converted and entered into continuously rotating buffers that had durations exactly equal to the 754-msec duration of the digital analog buffer used for stimulus generation. The signal recorded in each analog-digital buffer was considered a "section." Each section contained 512 samples. Sixteen sections were concatenated together to form a full recording sweep of 12.06 seconds (8192 samples). The number of sweeps necessary to identify a response varied with the signal-to-noise levels of the recording. Usually between 32 and 64 sweeps were recorded. This lasted 6 to 15 minutes (depending on the number of artifacts). The use of recording sections allowed for artifact rejection over the section rather than over an entire sweep. In most subjects, a section was rejected if it contained any potentials with amplitudes greater than 40 RV. If a section was rejected, that part of the recording sweep was filled in with the next recorded data. The number of sections rejected was between 0 and 25 percent. When artifacts were more frequent, the artifact rejection procedure criterion was increased to 50 or 60 p,v (depending on the amplitude of the subject's alpha rhythm). In Time Frequency Polar Plots 0 80.9 88.9 96.9 104.8 Hz 754 msec 340 Hz 500 w ] 50 nv ] 50 nv Figure 2 Analysis of the steady-state responses. The responses were recorded and averaged using a sweep consisting of 16 sections, each section lasting 754 msec. The waveform at the top of this figure represents activity recorded over a period of one section. In order to make this time waveform visually tractable, we have averaged together each of the 16 sections that make up one averaged recorded sweep. Small levels of high-frequency activity represent the responses to the stimulus modulations (61, 67, 73, and 79 cycles per sweep). These responses ride upon higher amplitude slow waves that represent the residual EEG noise after the averaging. The time domain data were converted to the frequency domain using a Fast Fourier Transform based upon the 12.06-second recording sweep (16 sections). The amplitude spectrum shows the residual background noise in the low frequencies as well as recognizable responses at the specific (signature) modulation frequencies of the four different stimuli. These have been indicated with the arrows. There is also a small peak in the response at 180 Hz that represents the third harmonic of line noise. Although this spectrum provides only amplitude data, the frequency transform provides both amplitude and phase. These measurements are used at the signature frequencies in the polar plots shown at the bottom of the figure. In these plots, the amplitude of the responses is shown by the distance of the center of the circle from the origin. The phase of the response is shown by the angle made with the x-axis and the confidence limits of the mean response shown with the circle. If the origin is not included within these confidence limits, then one can be reasonably sure (p <.05) that the response is significantly different from noise.

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 tudes reported in this paper are baseline-topeak amplitudes and the phases are cosineonset phase. Figure 2 shows sample data from one subject. It is difficult to recognize the response in the time domain. The frequency domain results can be expressed in two ways : an amplitude spectrum showing the response amplitude at different frequencies and polar plots showing the amplitude and phase of the response at the different modulation frequencies. The presence or absence of a response was assessed using the F-technique (Zurek, 1992 ; Dobie and Wilson, 1996 ; Lins et al, 1996). This method compared the response at the frequency of stimulation (the modulation frequency) to the noise in the recording as assessed at adjacent frequencies. The program computed the ratio between the power at the signal frequency and the average power in 120 neighbouring frequency bins - 60 above and 60 below the signal frequency (extending about 5 Hz on each side of the signal). When using this technique, those frequencies at which another signal was present were excluded from the calculation. The significance of the F ratio was calculated against critical values for F at 2 and 240 degrees of freedom. As well, an FFT analysis was performed on each of the 16 sections of the averaged sweep. This provided 16 separate measurements of the amplitude and phase of the responses at the frequencies of stimulation. We could then calculate the confidence limit of this response using the circular T2 test (Picton et al, 1988 ; Victor and Mast, 1991 ; Dobie and Wilson, 1993). This test provided almost identical results to the F-test. Threshold estimations were based only on the F-tests. However, the T2 confidence limits are presented in the figures since they are easier to visualize. Threshold Estimation Behavioral thresholds were assessed using conventional audiometric techniques (Carhart and Jerger, 1959) with 5-dB steps in the ascending mode of presentation. The thresholds were measured for each of the stimuli presented singly rather than in combination. All subjects were tested with imfnittance audiometry to ensure that they had normal middle ear functions. For subjects wearing hearing aids, the voltage of the hearing aid battery was measured and a listening check of the aid was carried out prior to testing. The hearing aid settings were adjusted to those recommended by the Audiology clinic. Low voltage batteries were replaced. The physiologic thresholds were determined by the presence or absence of recognizable steady-state responses recorded at different intensities using the multiple stimulus technique. These intensities were varied using 10- db steps. We attempted to bracket threshold by recording responses above and below the threshold at which a response became recognizable (using the F-test). However, because of time limitations, this was occasionally not possible : in the hearing-impaired children, this occurred in 4 of 140 estimates. When considering the differences between the physiologic and behavioral thresholds, we therefore arbitrarily made the physiologic thresholds in these cases 10 db higher than the maximum intensity evaluated when no response was present. Because the protocols recognized a response using probability estimates, it is possible that a response may be "present" by statistical chance rather than reality. We therefore required that a response must also have been recognized at an intensity 10 db higher than the threshold. The threshold was the lowest intensity at which a response was recognized as different from noise (p <.05), provided that a response occurred at an intensity 10 db higher or that this intensity was the highest tested. Experimental Design The first question was whether there was any difference in the thresholds obtained when multiple stimuli were presented separately compared to when each stimulus was presented singly. Previous findings had indicated that there was no difference in the amplitudes of the responses between multiple and single presentation (Lins and Picton, 1995) provided that the intensity is not too high (John et al, 1998), but had not assessed interactions near threshold. The first group of subjects had physiologic thresholds estimated under three conditions : four simultaneous stimuli (500-, 1000-, 2000-, and 4000-Hz carriers), 1000-Hz carrier alone, and 4000-Hz carrier alone. The main hypothesis was that there were no significant differences between the 1000- and 4000-Hz thresholds obtained in the simultaneous and single conditions. This experiment was performed using earphones rather than the soundfield speaker. The second question concerned whether we could obtain similar thresholds to those obtained with earphones when presenting the multiple stimuli through the soundfield speaker. We 320

Objective Evaluation of Aided Thresholds/Picton et al wished to rule out problems with electrical artifact or acoustic interactions between the soundfield stimuli. Behavioral and physiologic thresholds were therefore evaluated in a second group of normal subjects when stimuli were presented using the soundfield speaker. The third (and main) question for investigation was whether the physiologic thresholds obtained using the multiple steady-state response technique in hearing-impaired children wearing their hearing aids accurately reflected their behavioral thresholds. Both physiologic and behavioral thresholds were therefore assessed in 35 children using hearing aids. Finally, pilot data were recorded from two infants and one older child with severe developmental delay to investigate the possibility of using this technique as an objective assessment of aided thresholds in patients who cannot be tested behaviorally. Statistical Analyses Statistical evaluations were carried out using SPSS. The initial calculations assessed the mean and standard deviations of the physiologic and behavioral thresholds and the differences between them. Comparisons among different conditions were assessed using analyses of variance with repeated measures where appropriate. The relations between the physiologic and behavioral thresholds in the 35 hearing-impaired children were also evaluated using Pearson product-moment correlations and a regression analysis that fit the data with a line having the formula Behavioral Threshold = Intercept + Slope (Physiologic Threshold). Correlations and regressions were performed separately for each of the four carrier-frequen- ties. In order not to distort the regressions, data where no physiologic thresholds could be estimated at a particular carrier frequency were omitted from these analyses. The regressions were therefore based on 31 or 32 data points. In addition, the elevated physiologic thresholds at high frequencies found in six subjects with the multiple-stimulus technique were replaced with those obtained using single-stimulus presentation. The rationale for this will become clear when the results are presented. There were clear interindividual differences in our data. In order to determine whether the difference between physiologic and behavioral thresholds differed across subjects independently of the carrier frequency, we calculated correlations between the physiologic-behavioral differences among the different frequencies. Significant positive correlations would indicate that subjects with a large difference at one frequency would have a large difference at another frequency. Nofmal Subjects RESULTS The average physiologic thresholds in the first group of normal subjects for the stimuli presented (through earphones) either alone or as part of the multiple-stimulus technique are shown in Table l. There was no significant difference between the single- and multiple-stimulus conditions (F = 1.6, df = 1, 9 ; p >.1). The average behavioral and physiologic thresholds for the second group of 10 normal subjects tested with soundfield stimuli can also be seen in Table 1. In general, the thresholds for the steady-state responses were between 10 and 30 db above the behavioral thresholds. There were no significant differences between the SPL Table 1 Results in Normal Subjects Carrier Fre quency (Hz) Threshold P 500 B D P 1000 B D P 2000 B D P 4000 B D Earphone multiple stimuli 37 32 30 30 Earphone single stimulus (10) (15) (7) (7) 34 33 Soundfield speaker multiple stimuli (10) (12) 31 10 21 36 10 26 28 10 18 26 6 20 (8) (6) (9) (15) (4) (13) (15) (8) (13) (11) (8) (10) Thresholds are measured in db SPL. The P columns contain the physiologic thresholds, the B columns the behavioral thresholds, and the D columns the differences between these measurements. Numbers in brackets represent standard deviations.

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 Stimulus Intensity Frequencies (db SPL) (khz) Spectrum (60-120 Hz) 4 y 500 1 khz 2 khz 4 khz Stimulus Frequencies (khz) Intensity (db SPL) Spectrum (60-120 Hz) " y yy 500 1 khz 2 khz 4 khz 0.5, 1, 2, 4 40 0.5, 1,2,4 50 y 0.5, 1,2,4 30 0.5, 1, 2, 4 40 0.5, 1, 2, 4 20 0.5, 1, 2, 4 30 ~ ~.f- + so nv ], 00 ~v] 0.5, 1,2,4 10 0.5, 1, 2, 4 20.~ 0 (~_ (4-0 + Subject N3 Physiologic 30 30 10 30 Subject A23 Physiologic 40 40 30 40 Left Ear Behavioral 10 5 5 5 Right Ear Behavioral 30 30 30 30 Figure 3 Response of a normal subject to soundfield stimulation. The data presented in the first line of the figure are the same as in Figure 2. For this figure and all succeeding figures, the presentation of the amplitude spectrum is limited to the range 60-120 Hz. In the spectrum, responses recognized as significantly different from zero are indicated by arrows. There is a small and variable pick-up of line noise at 60 Hz seen at the left edge of the plotted spectrum. In the polar plots provided on the left of the figure, a response judged as significantly different from zero is indicated by shading in the confidence limit circle. With this particular subject, clear responses at all carrier frequencies are seen at 30 and 40 db SPL. The response at 2000 Hz continues to be recognizable down to 10 db. The thresholds for the physiologic responses and for behavioral responses are provided at the bottom of the figure. In this particular subject, the physiologic thresholds were between 5 and 25 db above the behavioral thresholds. This and succeeding figures are limited to only four intensities. Some of the threshold estimations were occasionally based on recordings not displayed in the figure. thresholds obtained with the earphones or the soundfield speaker (F = 0.47, df = 1,72 ; p >.1 ; this test could not use repeated measures since the subjects were different for the two measurements). The responses for one subject (N3) in sound field are illustrated in Figure 3. Hearing-Impaired Children As for the normal-hearing subjects, most hearing-impaired children showed recognizable responses within 10 and 30 db above their behavioral thresholds with their hearing aids. An example (A23) is illustrated in Figure 4. This subject's recordings showed a "spurious" response (one that was probably significant by chance rather than in reality) at 20 db at 1 khz after showing no response at 30 db SPL. One subject (A29) showed no recognizable responses at any intensity, despite having reli- Figure 4 Evaluation of aided thresholds. This figure represents the steady-state responses recorded in a hearing-impaired subject (A23) using hearing aids. The setup of the figure is the same as that described for Figure 3. Physiologic responses are recognized down to within 0-10 db of the aided behavioral thresholds. The steadystate response at 20 db SPL for the 1000-Hz carrier probably represents a spurious response since no response is recognized at 30 db. able behavioral thresholds. The results of this subject were not included in the analyses of the thresholds and will be considered at the end of this section. The results of the analyses (for the 34 remaining subjects) are shown in the upper section of Table 2. The physiologic thresholds are quite closely related to the behavioral thresholds except at 4000 Hz where there was a significantly greater variability in the relation between the behavioral and physiologic thresholds (shown in the standard deviation). In several of the aided subjects, we found that the response at 4000 Hz was not recognized even when the stimuli were significantly above behavioral thresholds. In these subjects, if we presented the 4000-Hz stimulus by itself, we were often able to record a clear response. An example (A25) is shown in Figure 5. In one subject (A5) where the aided thresholds at 2000 and 4000 Hz were much higher than those for the lower frequencies, it was uncomfortable to present the four stimuli simultaneously at intensities above 60 db. In this particular subject, thresholds were also assessed using either the 2000- and 4000-Hz stimuli presented simultaneously or the 4000-Hz stimulus presented alone. The results are illustrated in Figure 6. If we replaced the thresholds in the few cases like A5 and A25 with the better thresholds obtained using the same stimuli presented singly, the relations between the physiologic 322

Objective Evaluation of Aided Thresholds/Picton et al Table 2 Results in Children Using Hearing Aids Carrier Frequency (Hz) 500 1000 2000 4000 Before correction After correction Difference (SD) 17(8) 13(8) 14(8) 17(13) Difference (SD) 17(8) 13(7) 13(7) 16(9) Regression SE 8 5 5 7 Slope 0.68 0.54 0.63 0.60 Intercept -1 9 4 4 Correlation 0.69 0.75 0.81 0.71 Relations between physiologic and behavioral thresholds in db were initially assessed by calculating the mean and standard deviation of the difference between the two measurements. The initial data were "corrected" by using the thresholds obtained with single stimuli rather than those obtained with the multiple stimuli for high-frequency carriers, and by omitting those measurements in which physiologic thresholds were only estimated. The regression analysis led to a line with the formula Behavioral Threshold = Intercept + Slope (Physiologic Threshold). and behavioral thresholds became closer. This is shown in the lower section of Table 2. There were no significant differences in the physiologic-behavioral differences among the different audiometric frequencies (F = 1.95 ; df = 3, 87 ; p >.1). The physiologic-behavioral differences were significantly smaller for the patients than for the normal subjects (F = 11.3 ; df = 3, 114 ; p <.01). Figure 7 shows the regression analyses. The intercepts are close to zero and the slopes are less than unity. This means that higher physiologic thresholds are associated with greater difference between the physiologic and behavioral thresholds. For example, a physiologic threshold of 70 db SPL is associated with a behavioral threshold of 40 db, whereas a physiologic threshold of 30 db is associated with a behavioral threshold of 20 db. Correlation coefficients among the physiologic-behavioral differences for the different carrier frequencies varied between -0.12 and 0.33. None of these was significantly different from zero (p >.05). The threshold difference at one frequency does not predict the threshold difference at another. Subjects in Whom Behavioral Responses Were Not Available The recordings obtained in the two aided infants showed recognizable responses. Subject Stimulus Intensity Spectrum Frequencies (db SPL) (60-120 Hz) 500 1 khz 2 khz 4 khz (khz) 0.5,1,2,4 50 Stimulus Intensity Spectrum Frequencies (db SPL) (60-120 Hz) 500 1 khz 2 khz 4 khz (khz) y 0.5, 1,2,4 60 ~ 4~- i~ -,;~ 0.5, 1,2,4 40 0.5, 1, 2, 4 50 y + + y 0.5, 1, 2, 4 30 2, 4 70 + + -I + 0.5, 1, 2, 4 40 4 80 b I Subject A25 Physiologic 20 30 20 40' Left Ear Behavioral 25 25 15 25 Subject A3 Physiologic 50 50 70` 80` Right Ear Behavioral 35 30 60 65 Figure 5 Problems estimating high-frequency thresholds. In this subject (A25), the responses at 4000 Hz were not recognizable when using multiple stimuli. However, the responses were recognized at 40 db SPL when the 4000-Hz stimulus was presented alone. The asterisked threshold noted at the bottom of the figure is that obtained using the single stimulus. Figure 6 High-frequency hearing losses. In this particular subject (A3) with very high aided thresholds for the high-frequency stimuli, multiple-stimulus presentation was uncomfortable at intensities of 60 db SPL. We therefore elected to assess the high-frequency thresholds using only the 2000- and 4000-Hz stimuli (third line) or only the 4000-Hz stimulus (bottom line). 323

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 90 500 Hz 1000 Hz Stimulus Intensity Frequencies (db SPL) (khz) Spectrum (60-120 Hz) 500 1 khz 2 khz 4 khz 0.5, 1, 2, 4 70 't' + + + (unaided) 0.5, 1, 2, 4 70 I I + 0 0 y 2000 Hz 4000 Hz 0.5, 1, 2, 4 60 ++ zoo w] ro a"..; O Co O Ga 0.5, 1, 2, 4 50 + ~ + + Subject X3 Physiologic 60 50? 70 Right Ear Behavioral???? Physiologic Thresholds (db SPL) Figure 7 Regressions between physiologic and behavioral thresholds. The regressions were calculated according to the formula Behavioral Threshold = Intercept + Slope (Physiologic Threshold). These are plotted separately for each of the carrier frequencies. The number of subjects (N), correlation coefficient (r), and slope of the line (m) are given with each graph. Xl showed no response to amplitude-modulated tones presented in sound field at 60 db SPL. In the aided condition, responses at 1000- and 2000-Hz tones were seen down to 50 db SPL. These findings are shown in Figure 8. Subject X2 showed no response at 50 db SPL in the unaided condition but responses at 2000 Hz down to 30 db SPL in the aided condition. The results in the older developmentally delayed Figure 9 Aided responses in a developmentally delayed child. This subject (X3) was 9 years old. The responses shown at the top of the figure were obtained without aids. Recordings with the hearing aid show significant responses at 500, 1000, and 4000 Hz. These are the first reliable responses to sound obtained in this patient. child (X3) were quite striking (Fig. 9). With the steady-state evoked potentials, responses were absent at all frequencies at 70 db SPL in sound field but were identified with the hearing aid at 1000 Hz down to 50 db SPL. Unusual Subject with Hearing Impairment One subject (A29) in the group of children with hearing impairment showed no recognizable steady-state responses at intensities up to 80 db SPL with her aids, despite having reliable Stimulus Frequencies (khz) Intensity Spectrum (db SPL) (60-120 Hz) 500 1 khz 2 khz 4 khz Stimulus Frequencies (khz) Intensity (db SPL) Spectrum (60-120 Hz) 500 1 khz 2 khz 4 khz 0.5, 1,2,4 60 (unaided) 0.5, 1, 2,4 60 O "4.*. U 0 'Y Y yy MMW 1, 0.5, 1, 2, 4 70 + + + 0.5, 2, 4 60 ++ + 6-0.5, 1, 2, 4 50 0.5, 1, 2, 4 50 0. 5, 1, 2, 4 40 +0+ (1) 50 w], 4 + 0. 5, 1, 2 ++++ Subject X1 Physiologic? 50 50 Subject A29 Physiologic?? Right Ear Behavioral??? Left Ear Behavioral 40 25 30 20 5u nv ] Figure 8 Aided responses in an infant. This infant (Xl) was 51/2 months old. The responses shown at the top of the figure were obtained without aids. Recordings with the hearing aid show significant responses at 1000 and 2000 Hz down to 50 db SPL. Figure 10 Absent steady-state responses. In this subject (A29), who showed reliable behavioral responses to aided stimuli, no recognizable steady-state responses were obtained, even at intensities 50 db above the behavioral thresholds. 324

~ Objective Evaluation of Aided Thresholds/Picton et al Behavioral Audiometry 0 20 40 60 80 100 120 Right 250 1000 4000 250 0 L-a--i M O U SRT 45 db SRT WRS 56% at 80 db WRS r 0 Auditory Brainstem Responses Right........ 90 db nhl Clicks Rarefaction Condensation Combined a f 10 0 20 40 60 80 100 120.. C O 3 Left 1000 4000 Figure 11 Possible auditory neuropathy? This figure represents the audiogram and auditory brainstem l l C responses (ABRs) in the subject with the absent steady-state responses (preceding figure). The audiogram shows a mild hearing loss at the low frequencies with a severe hearing loss in W 7l the high frequencies in both ears and in the mid frequencies in the right ear. Stapedius reflexes (S) were absent except at 500 Hz in the left ear. The word recognition score (WRS) was the percentage of phonetically balanced words correctly identified at the intensity at which maximum discrimination occurred. The ABRs show no clear wave V but reliable waveforms out to about 4 msec when using high-intensity Left clicks. These reverse in polarity when the stimulus is changed from a condensation to a rarefaction click (two-headed arrows). This suggests that the findings largely represent a prolonged cochlear microphonic. The remaining waves when the condensation and rarefaction responses are combined for the left ear (asterisk) may represent some distorted neural response or some nonlinearity in the cochlear microphonic. 35 db 72% at 80 db O.S [IV ~ rr - 3 0 msec behavioral thresholds near 30 db SPL (Fig. 10). This subject was a 17-year-old girl with a history of jaundice at birth, although the original records were not available since the child had immigrated to Canada. The mother felt that the child did not respond normally to sounds in the first few years of life. However, development was within normal limits except for some slurring of speech articulation. The speech had some characteristics of the speech of a hearingimpaired child but this was unusual in view of the mild hearing loss found on audiometry. A hearing loss was diagnosed when the child was 7 years old, and low-gain hearing aids have been used since age 8 years. The child derives little benefit from the aids and wears them only in class. At the time of our testing, the audiometric evaluation of the unaided left ear showed a mild hearing loss in the low- and mid-fre- quencies and a severe hearing loss at 8000 Hz ; the unaided right ear showed a similar pattern with an additional severe loss near 2000 Hz. Speech discrimination at comfort level was 72 percent in the left ear and 56 percent in the right, respectively. Stapedius reflexes were absent except in response to 500-Hz tones at 95 db HL in the left ear. These results are shown in the top half of Figure 11. ABRs recorded using a Nicolet Spirit System are shown in the bottom half of the figure. There was no recognizable wave V Replicable earlier waves in the recording largely inverted when the click polarity was reversed and most likely represented cochlear microphonic, although there were still small residual waves, particularly a negative peak at about 4 msec after combining the responses to condensation and rarefaction clicks. Recording click-evoked and distortion-product OAEs with

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 an Otodynamics IL092 System showed no recognizable responses. DISCUSSION Thresholds in Normal Subjects The thresholds for recognizing the auditory steady-state responses in normal subjects (see Table 1) are similar to those reported in the literature. The average SPL thresholds for the steady-state responses vary between 26 and 36 db SPL. Lins et al (1996) reported thresholds for normal adults between 29 and 39 db SPL and Aoyagi et al (1994) reported thresholds approximately equivalent to 36 and 40 db SPL for 1000- and 4000-Hz stimuli (numbers converted from HL). These thresholds in normal subjects are significantly higher than normal HL thresholds or from the actual behavioral thresholds obtained in the subjects tested. We found the difference between the physiologic thresholds and behavioral thresholds in normal subjects to be between 18 and 26 db (see Table 1). This is a greater difference than we measured in previous papers (e.g., Lins et al, 1996). The most likely cause for this discrepancy rests in the acoustic environment in which the subjects were tested. In the present study, the subjects were evaluated in a properly sound-attenuated chamber, whereas in our previous studies, many of the subjects were studied without significant sound attenuation (other than that provided by the earphones). In the previous studies, the presence of low-level background masking could have elevated the behavioral thresholds without affecting the thresholds for the auditory steady-state responses. The background noise could have imitated a mild sensorineural hearing loss with recruitment. We did not find any differences between the thresholds obtained when four stimuli were presented simultaneously and the threshold obtained with single stimuli. We had previously shown that multiple stimuli had no significant effect on the amplitude of the responses (Lins and Picton, 1995), provided that the stimuli had carrier frequencies separated by at least a halfoctave and the intensity was 60 db SPL or less (John et al, 1998). This experiment demonstrated that the multiple-stimulus technique provides similar thresholds to those obtained using single stimuli. Within an acoustic environment suited for audiometric testing, we did not find any signif- icant differences between the thresholds obtained for earphones and in sound field (see Table 1). Our comparison used the SPL measurements and did not correct for the small differences in HL thresholds between earphones and soundfield conditions that would have made the earphone thresholds a little lower since, for example, 0 db HL corresponds to 7 db SPL for the earphone and 4 db SPL for sound field at 0 azimuth (ANSI, 1996). These differences would not have affected the results. We had been concerned that in the sound field the depth of modulation might have decreased from 100 percent because of room reflections arriving at the head position with different delays. This certainly occurred but probably had little effect since the response is stable at modulation depths greater than 50 percent (Lins et al, 1995). The steady-state response is evoked by the modulation of the carrier rather than the simple occurrence of the carrier. Since one can only obtain a response to an amplitude-modulated tone if the amplitude modulation is actually audible, we considered the possibility that the modulation might not become audible until the sound intensity is significantly elevated above threshold. The frequency spectrum of an amplitude-modulated tone contains two side bands that are below the intensity of the carrier frequency. If the side bands are not audible, there will be no detection of the modulation. The side bands are one half the amplitude of the carrier frequency when the modulation is 100 percent. This suggests that the responses should not be recordable until 6 db above the SPL intensity where the stimulus becomes audible. However, this effect is countered by the fact that modulation decreases the intensity of the sound (which therefore has to be increased to provide the same audibility). We have found that a 100 percent modulated tone is clearly discriminable from an unmodulated tone at 5 db above the hearing threshold for the tone, with attention paid to the appropriate balancing of intensity (Viemeister, 1979). Bacon and Viemeister (1985) have found that modulations of -6 db (equivalent to 50%) can be detected at 5 db above hearing threshold at modulation frequencies between 64 and 128 Hz. The 20-dB difference between physiologic and behavioral thresholds in normal subjects might be due to an inadequate reduction of noise by the recording techniques used by us and other investigators. Further averaging might have shown responses at intensities closer to threshold. Prolonged averaging of the ABR shows 326

Objective Evaluation of Aided Thresholds/Picton et al recognizable responses at intensities much closer to threshold than conventional averaging (Elberling and Don, 1987). Although we have not formally assessed this question, our experience so far suggests that there would not be recognizable responses below 10 db HL regardless of the amount of averaging. At near-threshold intensities, there is probably too much latency jitter in the modulation response to allow averaging to detect a response. The phase of the response might be used to facilitate the recognition of low-amplitude responses (Dobie and Wilson, 1994). As intensity decreased, the cosine-onset phase of the response generally became smaller. In the figures, the responses tend to rotate clockwise as the intensity decreases. The phase delay of the response compared to the stimulus is calculated by subtracting the onset phase from 360 (Rodriguez et al, 1986). Thus, as intensity decreased, the phase delay became longer. Since we are using a statistical test to determine whether a response is present or not, we should detect spurious responses (i.e., consider noise as signal) at a probability equal to the criterion level of the test (1/20). A spuriously significant response often had an onset phase that was greater than that recorded above threshold. (This is, however, not true of the example given in Figure 3.) Phase information could therefore be used in the rejection of responses recognized by chance as well as in the detection of low-amplitude responses. Aided Thresholds The aided thresholds for the steady-state responses were on average between 13 and 17 db higher than the behavioral thresholds (see Table 2). This physiologic-behavioral difference is less than that found in normal subjects (see Table 1). This probably does not relate to different signalto-noise levels in the recordings, since these were better in the normal subjects. The difference was probably not related to the age differences between the groups since the younger subjects in the normal group did not show lower physiologic thresholds. A similar finding was obtained in assessing unaided thresholds in hearing-impaired subjects (Lins et al, 1996). The effect is probably related to recruitment. In the hearing impaired, the response reaches a level where it is recognizable at an intensity closer to threshold than in normal subjects. The differences between physiologic and behavioral thresholds varied between 10 and 40 db. We considered the possibility that this variance might be explainable by intersubject differences. If some subjects had high threshold differences for all frequencies and others had low threshold differences, then the frequency pattern of the thresholds would be preserved. However, we found no support for this possibility, and we are left with physiologic thresholds that are usually (94% of assessments) between 5 and 25 db above behavioral thresholds. This 20-dB range is far from optimal. However, in patients where there is no other information about aided thresholds, this degree of accuracy is still acceptable. As can be seen in Table 1, there were no differences between the steady-state thresholds in normal subjects between multiple- and single-stimulus presentation. However, this is not the case in some hearing-impaired subjects using hearing aids. In some of these subjects (e.g., Fig. 7), the threshold for recording steady-state responses is much lower when the stimulus is presented alone compared to when it is part of a combined stimulus. This problem at the high frequencies might be ekplained on the basis of the abnormal tuning curves for the auditory nerve fibres in cochlea-damaged ears (Kiang et al, 1976 ; Dallos and Harris, 1978). As illustrated in Figure 12, these tuning curves lack the normal high-sensitivity "tip" at the characteristic frequency and have a shape similar to the Bekesy traveling Normal Pathological a m a m b 100 0 100 0 L T r,v 100, 000 Frequency (Hz) 10000 Figure 12 Hypothetical explanation for some of the difficulties in recording high-frequency responses using the multiple-stimulus technique. The figure combines the amplitude spectrum of the responses (see Fig. 1) with normal and pathological tuning curves for neurons that respond best to 4000 Hz. In the pathological ear, it is possible that the high-frequency responsiveness may be masked by concomitant activation of the cells by the lower frequency stimuli.

Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998 wave with a relatively greater sensitivity to low frequencies than to high. The distorted tuning curves usually maintain their high-frequency cut-off slopes. When multiple stimuli are presented simultaneously, the low-frequency stimuli might interfere with the response to the high-frequency stimulus because of these distorted tuning curves. Although this might occur at high intensities in normal subjects, it occurs close to threshold in subjects with sensorineural hearing loss. Although the response is abnormally elevated for the high-frequency stimuli in the multiple-stimulus conditions, this finding may actually represent the effective hearing of the individual. Although a pure tone might be audible in the absence of any other competing stimuli, frequency information might not be available in the usual stimuli one hears in the real world since these contain multiple frequencies. At our present level of understanding, however, it is necessary to check abnormally elevated thresholds at higher frequencies using single-frequency stimulation. In cases where the thresholds vary substantially across the audiometric frequencies, the multiple-stimulus technique runs into problems when all stimuli are presented at the same intensity. Thresholds at one frequency might not be measurable because the intensity of the sounds at other frequencies is too high (see Fig. 8). It should be possible to use an algorithm that adjusts the intensity of each carrier frequency automatically once a response is recognized as present. For example, once a response to the 1000-Hz stimulus is recognized (say in the first three or four sweeps), its intensity would be decreased. If no response were recognized for the 4000-Hz carrier, its intensity would remain at that level until a set number of sweeps had been analyzed (or a set noise level obtained), at which time its intensity would be elevated. The intensities of the different carrier frequencies in the combined stimulus would thus be continually adjusted until the audiogram was approximated. The present study was designed to assess thresholds and did not consider the responses in relation to the optimal setting of the hearing aid. It is possible that the amplitude of the steady-state response might correlate in some way with the loudness of the sounds. This might only be true over the low range of intensities since there are interactions between the stimuli at high intensity (John et al, 1998). We might therefore be able to use the amplitude of the response to construct an input-output function for the hearing aids. This could provide an objective assessment of such hearing aid measurements as comfort levels, and might be a more efficient approach to fitting the hearing aid than determining aided thresholds. For example, one could present a series of amplitude- or frequency-modulated stimuli at intensities near those of normal speech and adjust the hearing aid to give optimal responses (i.e., of good amplitude and without significant harmonics indicating distortion). The amplitude-modulated stimuli that we used are much more frequency specific than the brief tones or clicks that are used to record the ABRs. This would suggest that the steady-state thresholds are also frequency specific and that the masking protocols needed for recording frequency-specific thresholds using the ABR (Don et al, 1979 ; Ponton et al, 1992 ; Stapells et al, 1994) are not necessary for the steady-state responses. However, without masking, the thresholds will be frequency specific but not place specific (Starr and Don, 1988). Responses to low-frequency stimuli may be mediated through places on the basilar membrane place specific for high frequencies. As well as assessing the effect of the hearing aid, aided thresholds might also be helpful in demonstrating hearing that cannot be recognized using other objective techniques. Rance et al (1998) studied 108 children with hearing losses that were sufficiently severe that no click ABRs were recordable. They found that steadystate responses, which can be presented at higher levels and at specific frequencies, could provide precise estimates of hearing threshold in children with little or no residual hearing. Studying the steady-state responses when these children used their hearing aids should provide further information. The regression equations that we obtained when relating the physiologic to the behavioral thresholds showed slopes (calculated as behavioral/physiologic) that were consistently less than one (see Fig. 9). This was unexpected since it is customary when relating physiologic to behavioral thresholds in unaided hearingimpaired subjects to obtain slopes greater than one (e.g., Stapells et al, 1994 ; Lins et al, 1996). (When comparing slopes in the literature, it is important to ensure that the axes of the regression are not rotated, that is, that the slope is behavioral/physiologic rather than physiologic/behavioral.) What normally happens is that the physiologic thresholds are higher than 328