Download Estimating the Audiogram Using Multiple Auditory Steady

J Am Acad Audiol 13 : 205-224 (2002)
Estimating the Audiogram Using
Multiple Auditory Steady-State Responses
Andrew Dimitrijevic*
M . Sasha John*
Patricia Van Roon*
David W Purcell*
Julija Adamonis`
Jodi Ostroff
Julian M. Nedzelski'
Terence W. Picton*
Abstract
Multiple auditory steady-state responses were evoked by eight tonal stimuli (four per ear), with
each stimulus simultaneously modulated in both amplitude and frequency. The modulation frequencies varied from 80 to 95 Hz and the carrier frequencies were 500, 1000, 2000, and 4000
Hz . For air conduction, the differences between physiologic thresholds for these mixed-modulation
(MM) stimuli and behavioral thresholds for pure tones in 31 adult subjects with a sensorineural
hearing impairment and 14 adult subjects with normal hearing were 14 ± 11, 5 ± 9, 5 -!- 9, and
9 ± 10 dB (correlation coefficients .85, .94, .95, and .95) for the 500-, 1000-, 2000-, and 4000-Hz
carrier frequencies, respectively . Similar results were obtained in subjects with simulated conductive
hearing losses . Responses to stimuli presented through a forehead bone conductor showed physiologic-behavioral threshold differences of 22 ± 8, 14 ± 5, 5 ± 8, and 5 ± 10 dB for the 500-,
1000-, 2000-, and 4000-Hz carrier frequencies, respectively. These responses were attenuated
by white noise presented concurrently through the bone conductor .
Key Words: Auditory steady-state responses, objective audiometry, thresholds
Abbreviations : AM = amplitude modulation ; FFT = fast Fourier transform ; FM = frequency modulation ; MASTER = multiple auditory steady-state response ; MM = mixed modulation ; OAE =
otoacoustic emission ; PTA = pure-tone average (of threshold hearing levels at 500, 1000, and
2000 Hz) ; SAL = sensorineural acuity level
Sumario
Se evocaron multiples respuestas auditivas de tipo estado estable (steady-state) por medio de ocho
estimulos tonales (cuatro en cada oido), con cada estimulo simultaneamente modulado tanto en amplitud como en frecuencia. Las frecuencias de modulaci6n variaron desde 80 a 95 Hz y las frecuencias
portadoras fueron de 500, 1000, 2000, y 4000 Hz . Para la via aerea, las diferencias entre los umbrales
fisiol6gicos para estos estimulos de modulacion mixta (mixed modulation : MM) y los umbrales conductuales para tonos puros, en 31 sujetos adultos con hipoacusias sensorineurales y 14 adultos con audici6n
normal, fueron 14 ± 11, 5 ± 9, 5 ± 9, y 9 ± 10 dB (coeficientes de correlaci6n de .85, .94, .95, y .95)
para las frecuencias portadoras de 500, 1000, 2000, y 4000 Hz, respectivamente . Se obtuvieron resultados similares en sujetos con hipoacusias conductivas simuladas . Las respuestas a estimulos presentados
a traves de un vibrador 6seo colocado en la frente mostraron diferencias entre los umbrales fisiol6gicos y conductuales de 22 ± 8, 14 ± 5, 5 ± 8, y 5 ± 10 para las frecuencias portadores de 500, 1000,
2000, y 4000 Hz, respectivamente . Estas respuestas fueron atenuadas por un ruido blanco presentado
a mismo tiempo a traves del vibrador 6seo .
Palabras Clave : Respuestas auditivas de estado estable, audiometria objetiva, umbrales
Abreviaturas : AM = modulacion de amplitud ; FFT = transformaci6n rapida de Fourier ; FM = modulacion
de frecuencia ; MASTER = respuesta auditiva multiple de estado estable ; MM = modulacion mixta ; OAE
= emisi6n otoacOstica ; PTA = promedio tonal puro (de los niveles de umbral en 500, 1000, y 2000 Hz) ;
SAL = nivel de agudeza sensorineural
*Rotman Research Institute, Baycrest Centre for Geriatric Care, University of Toronto; tDepartment of Otolaryngology,
Sunnybrook and Women's College Health Sciences Centre and University of Toronto, Toronto, Ontario
Reprint requests : Andrew Dimitrijevic, Rotman Research Institute, Baycrest Centre for Geriatric Care, 3560 Bathurst
Street, Toronto, ON M6A 2E1
205
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
major goal of objective audiometry is to
obtain a pure-tone audiogram without
A requiring any behavioral response on
the part of the subject. Objective methods to
evaluate hearing include the auditory brainstem response (ABR) (Galambos et al, 1994 ;
Sininger and Abdala, 1996 ; Sininger et al, 2000 ;
Stevens, 2001) and otoacoustic emissions (OAEs)
(White and Behrens, 1993 ; Norton et al, 2000).
Both methods have limitations . The ABR is commonly evoked by clicks that stimulate the cochlea
along the whole basilar membrane . The major
drawback of the click-evoked ABR is poor frequency specificity. More frequency-specific ABR
responses can be obtained using tone-pips (alone
or in notched noise) or clicks presented in masking noise at different high-pass cutoff frequencies so that "derived band responses" can be
recorded (Don et al, 1979 ; Picton et al, 1979 ;
Stapells et al, 1994 ; Oates and Stapells, 1997).
These techniques are slow since multiple recordings must be obtained to estimate thresholds at
the different audiometric frequencies . Transient
or distortion-product OAEs can identify hearing
losses when thresholds are above 40 dB HL and
can suggest the audiometric profile of residual
hearing at lower levels (Harrison and Norton,
1999 ; Norton et al, 2000). The major drawback
when using OAEs to evaluate hearing loss occurs
when the responses are absent since neither
the severity of the hearing loss nor the audiometric configuration can then be determined
(Wagner and Plinkert, 1999)
Owing to the limitations ofABRs and OAEs,
auditory steady-state evoked potentials have
emerged as an attractive means of objectively
estimating the audiogram. Auditory steadystate evoked potentials were first suggested as
an objective means to assess hearing by Galambos and colleagues (1981), who demonstrated
that the 40-Hz steady-state response was easy
to identify at intensity levels just above behavioral thresholds . However, some limitations of
using the 40-Hz evoked potential for objective
audiometry are as follows : (1) the response
diminishes with decreased levels of arousal
owing to sleep or anesthesia (Linden et al, 1985 ;
Jerger et al, 1986 ; Plourde and Picton, 1990 ;
Cohen et al, 1991 ; Dobie and Wilson, 1998),
(2) the response cannot be reliably recorded in
infants (Stapells et al, 1988 ; Maurizi et al, 1990 ;
Aoyagi et al, 1994a), and (3) response amplitude
diminishes when several stimuli are presented
simultaneously (John et al, 1998).
Recent work has therefore concentrated on
the steady-state responses at higher rates of
206
stimulus presentation . Cohen and colleagues
(1991) showed that in adults, responses could be
evoked at stimulus rates greater than 70 Hz
and that these responses were little affected by
sleep. Furthermore, these rapid responses can
be easily recorded in infants and young children (Rickards et al, 1994 ; Lins et al, 1996 ;
Savio et al, 2001 ; Cone-Wesson et al, 2002a,
2002b) . Lins and Picton (1995) demonstrated
that multiple responses can be recorded simultaneously without loss of amplitude at these
rapid stimulus rates, thereby allowing for rapid
assessment of thresholds at different audiometric frequencies. The 80-Hz auditory steadystate evoked response has been extensively
evaluated as an objective audiometric tool in
hearing-impaired patients (Aoyagi et al, 1994b;
Rance et al, 1995 ; Lins et al, 1996 ; Picton et al,
1998 ; Perez-Abalo et al, 2001 ; Cone-Wesson et
al, 2002a, 2002b, 2002c) .
Amplitude modulation (AM) has typically
been used to elicit the auditory steady-state
evoked response . Cohen and colleagues (1991),
using single stimuli, showed that mixedmodulation (MM) stimuli that consisted of 100
percent AM and 20 percent frequency modulation
(FM) evoked larger responses than 100 percent
AM alone . In that study, Cohen and colleagues
(1991) used a 0-degree phase difference between
the AM and FM (i .e ., the maximum amplitude
occurred at the same time as the maximum frequency) . John and colleagues (2001b), using multiple stimuli in each ear, showed that the response
enhancement with MM stimuli was present at
both threshold and suprathreshold intensities .
They further showed that the phase difference
between AM and FM that produced the maximum response varied with the carrier frequency.
Setting the relative phase to 0 degrees will usually be beneficial but may not always align the
AM and FM responses optimally. For most carrier frequencies, maximum responses could be
elicited if the maximum amplitude occurred
slightly earlier than the maximum frequency.
The current study used the multiple auditory
steady-state response (MASTER) technique (John
and Picton, 2000b) . This technique uses an automatic statistical evaluation of the responses to
multiple sinusoidally modulated stimuli. Since
each carrier has a unique modulation rate, separate responses to each carrier can be distinguished in the frequency transform of the
recorded activity by measuring the amplitude
spectra at the frequencies of modulation . The
major advantage of this technique is that by
simultaneously presenting multiple stimuli (e.g .,
Audiometry Using MASTER1Dimitrijevic et al
four stimuli in each ear for a total of eight), multiple responses can be recorded during the time
normally required to record one . This does not
necessarily mean that audiometry can be performed in one-eighth of the time . If the patient
has a sloping hearing loss and if the eight stimuli in MASTER are all presented at the same
sound pressure levels, recordings at several
intensity levels are required to bracket the thresholds at the different carrier frequencies . Nevertheless, audiometry should be able to be
performed in one-third to one half of the time .
The current study investigated the use of
MM stimuli in evaluating hearing thresholds in
2.
3.
hearing-impaired and normal-hearing subjects
using the MASTER technique . First, we wanted
to examine the accuracy of MASTER in predicting hearing thresholds . Second, we wanted
to see how well MASTER could estimate both
sensorineural and conductive hearing losses .
Third, we wanted to validate the MASTER technique for obtaining bone-conduction thresholds .
METHOD
Subjects
Four groups of subjects participated in the
experiments:
1.
Hearing-impaired adults (n = 31, 15 male
and 16 female) were volunteers from the
audiology clinic at Sunnybrook and Woman's
College Health Science Centre . These subjects varied in age from 32 to 86 (mean 69)
years . Three of the subjects had a profound
hearing loss in one ear and only the better
ear was tested, resulting in a total of 59
ears being examined . The mean three-tone
pure-tone average (PTA) threshold (500,
1000, and 2000 Hz) was 46 . 20 dB HL, with
a range of 15 to 87 dB HL . Mean PTAs indicated normal hearing in 7 ears (<-25 dB HL,
most of these subjects having a hearing loss
at 4000 Hz), mild hearing loss in 17 ears
(26-40 dB HL), moderate hearing loss in
19 ears (41-60 dB HL), and severe hearing
loss in 16 ears (61-90 dB HL) . Of the 59 ears
examined, 44 had sensorineural hearing
loss, 12 had mixed hearing loss (sensorineural predominant), and 3 had normal
hearing (subjects with a unilateral hearing
loss) . Only 1 subject had interaural threshold differences of 40 dB or greater at any frequency. This subject's ears were tested
separately, and the better ear was masked
4.
with white noise when the poorer ear was
evaluated . The audiometric configurations
for the ears were flat (n = 25), sloping to a
high-frequency loss (n = 31), and sloping
from a low-frequency loss (n = 3) .
Normal-hearing adults (n = 14 ; 4 male and
10 female) were volunteers obtained from a
departmental subject database . These subjects varied in age from 23 to 63 (mean 36)
years. All had pure-tone thresholds below
25 dB HL across frequencies 500 to 4000 Hz .
Normal-hearing adults (n = 10 ; 5 male and
5 female) participated in the experiment to
evaluate a simulated conductive hearing
loss . These subjects varied in age from 23 to
35 (mean 28) years . Three of these subjects
were also in group 2 . Simulated conductive
hearing loss was achieved by plugging the
insert earphones with plasticine . All subjects
had pure-tone thresholds below 25 dB HL
across all audiometric frequencies used
(500-4000 Hz) prior to the simulated hearing loss . After the insert earphones were
plugged, the audiograms showed a moderate flat hearing loss, with mean PTAs of
52 -} 4 dB HL ranging between 47 and
57 dB HL . In this group, behavioral and
MASTER thresholds were evaluated in the
plugged earphone condition only.
Normal-hearing adults (n = 16 ; 5 male and
11 female) were used to study bone conduction. These subjects varied in age from
23 to 49 (mean 28) years . Five of these subjects were also in group 2. All subjects had
air- and bone-conduction thresholds below
25 dB HL between 500 and 4000 Hz . All
subjects were evaluated to obtain behavioral thresholds for forehead placement of
the bone-conduction vibrator. Eleven of the
subjects were also evaluated using MASTER
to assess bone-conduction thresholds, and 10
of the subjects participated in a separate
bone-conduction masking study.
Auditory Stimuli
Each stimulus consisted of a sinusoidal tone,
with a carrier frequency of f.. MM stimuli have
both AM and FM components . Both AM and
FM occur at the same modulation rate (f,,) . The
depth ofAM (ma) was defined as the ratio of the
difference between the maximum and minimum
amplitudes of the signal to the sum of the maximum and minimum amplitudes. The FM component of the stimulus was formed by modulating
the phase of the carrier frequency (p). The depth
207
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
of FM (mf) was defined as the ratio of the difference between the maximum and minimum
frequencies to the carrier frequency. The formula used for generating the stimuli (s) was:
s(i) = a(l + m¢sin(2aTfnti))sin(2iTf ti + 0(i))/M
(formula 1)
where
cp(i) _ (mJ,l(2Q)sin(2arfmti + 8)
(formula 2)
and
M = (1 + mazl2)'12
(formula 3)
where a is the amplitude, i is the address in the
output buffer, t is the time per address at which
digital-to-analog occurs, 6 is the difference in
phase between AM and FM (expressed in radians), and fm is the modulation frequency. The
term mff 1(2ffm) represents the modulation index
for FM (usually denoted by (3). The final divisor
M is used to maintain a constant root-meansquare amplitude across the different amounts
of AM (Viemeister, 1979). In all of the experiments in this study, the auditory stimuli were
MM, with an AM depth of 100 percent (m ) and
an FM depth of 25 percent (mf) .
In the above formula, the phase of the modulations as determined by the formula is such
that when O is -90 degrees, the maximum frequency occurs at the same time as the maximum
amplitude. For simplicity's sake, and because the
relative phase is arbitrary, we shall henceforth
state that relative phase is 0 degrees when the
maximum amplitude coincides with the maximum frequency since this fits better with the previous literature . The sign of e is such that if this
term increases, the maximum FM moves ahead
relative to the maximum AM. Table 1 illustrates
Table 1
Relative Phase
between FM
and AM (degrees)
MASTER
Setting
(degrees)
0
-90
90
180
0
90
270
180
these effects. Figure 1 illustrates one of the
stimuli.
One of the properties of MM stimuli is that
varying the relative phases between the maximum AM and maximum FM will alter the frequency spectra . For example, when the
maximum amplitude of the AM and maximum
FM frequency occur at the same time (i .e ., 6 = 0
degrees), the peak of the spectra skews toward
higher frequencies . Conversely, when maximum
AM occurs at the minimum FM (i .e ., maximally
out of phase or 0 = 180 degrees), the peak of the
spectra skews toward lower frequencies.
For these experiments, the relative phases
between AM and FM were chosen to produce the
largest combined (AM and FM) response (John
et al, 2001b) . Relative phase values for the 500-,
915-, 1850-, and 3810-Hz carriers were 45, 315,
315, and 315 degrees, respectively. Because of
the asymmetry of the spectra, the carrier
frequencies were adjusted so that the maximum
energy of the spectra was at 500, 1000, 2000, and
4000 Hz for the left ear, and the same carrier frequencies were used in the right ear. Although the
spectra of the 500-Hz carrier were asymmetric,
the maximum energy still occurred at 500 Hz,
and the carrier frequency was thus not adjusted .
Each carrier was modulated by a unique modulation frequency. Table 2 provides the stimulus parameters . The highly specific modulation
frequencies were attributable to the requirement for an integer number of cycles of a stimulus within each recording epoch of 1.024 seconds
(John and Picton, 2000b) . In the remainder of
this article, the modulation frequencies will be
reported with only single-digit precision.
The digitally generated auditory stimuli
were converted to analog form at a rate of 32 kHz
using 12-bit precision. The analog waveforms
were routed to a Grason Stadler Model 16 audiometer for presentation at the desired root-mean-
Stimulus Characteristics
Time Waveforms
Maximum frequency occurs at the same time as maximum
amplitude
Maximum frequency occurs 1/4 cycle before maximum amplitude
Maximum frequency occurs at the same time as minimum
amplitude
Maximum frequency occurs 1/4 cycle after maximum amplitude
FM = frequency modulation ; AM = amplitude modulation ; MASTER = multiple auditory steady-state response .
208
Spectra
Skewed toward
high frequencies
Symmetric
Skewed toward
low frequencies
Symmetric
Audiometry Using MASTER/Dimitrijevic et al
+1 .0
100% AM and
25% FM
f , = 84 .96 Hz
Instantaneous
Frequency (Hz)
1 .0
ak
Amplitude
Spectrum
X 0.0
1000
2000 Hz
Figure 1 Mixed-modulation stimuli. The upper part of
the figure shows the time waveforms for a stimulus with
a carrier frequency of 915 Hz that is 100 percent amplitude modulation (AM) and 25 percent frequency modulation (FM) . Both the AM and FM occur at 84 .96 Hz . The
middle plot shows the instantaneous frequency of the
sound. The phase difference (O) between the AM and FM
components is +45 degrees in this case . The maximum
FM occurs a little later than the maximum AM . The bottom plot shows the amplitude spectrum of the stimulus .
A 915-Hz carrier was chosen to estimate 1000-Hz puretone thresholds since the spectrum is skewed toward a
higher frequency and the maximum energy in the stimulus occurs at 1000 Hz (the carrier frequency of 915 Hz
plus the modulation frequency of 85 Hz).
square sound pressure level intensity levels
through Eartone 3A insert earphones calibrated
with a DB 0138 coupler. Stimuli were calibrated
in hearing level in the MASTER setup using the
reference values of Wilber and colleagues (1988) .
According to Wilber and colleagues (1988), using
Eartone 3A inserts with a DBO138 (HA-2) 2-cc
coupler, the reference equivalent thresholds for
500, 1000, 2000, and 4000 Hz are 8 .0, 3 .5, 6 .5,
and 7 .0 dB SPL . The amplitude of the 1000-Hz
stimulus relative to loudest stimulus (500 Hz)
should be -4 .5 dB (3 .5-8 dB) . The amplitude
(a in formula 1) of the 500-Hz stimulus was
arbitrarily set at 20 (a number based on the
range of the digital-analog converter, which has
a maximum of 100), and amplitudes of the other
stimuli were adjusted according to the formula :
Table 2
ax = a500 *10d500-/20
(formula 4)
where ax is the amplitude at x Hz and d500 -x is
the decibel difference between the threshold at
x and the threshold at 500 Hz . In the 1000-Hz
case, this difference in decibel sound pressure
level is -4 .5 and the amplitude is 11 .91 . The
more recent standard reference equivalent
thresholds for insert earphones (ANSI, 1996)
are lower than those of Wilber and colleagues
(1988) :5.5,0 .0,3 .0, and 5 .5 dB SPL for 500, 1000,
2000, and 4000 Hz . However, since both the
pure tones and the MASTER stimuli were
similarly calibrated, this does not affect our
comparisons .
For the bone-conduction studies, a Radioear
model B-71 oscillator was placed on the middle of the forehead and held in place with an
adjustable elastic strap exerting an average
force of 7 .5 (range 5-9) Newtons or 765 g. Four
stimuli were simultaneously presented using
the parameters listed for the left ear in Table
2. Both ear canals were occluded with inserts
throughout both the behavioral threshold estimations and the MASTER recordings . Normal
hearing levels for both pure tones and the four
individual MASTER stimuli were determined
in 16 normal-hearing subjects (Table 3) . The
pure-tone stimuli were calibrated in hearing
level. For the masking studies, the boneconducted tones were presented in white noise
with an effective masking level (as determined
by the audiometer for speech) of 50 dB HL
(root-mean-square dynamic force measured
using an artificial mastoid as 0.27 Newtons, or
109 dB relative to 1 p,N) . This was significantly
higher than the average level needed to mask
the perception of the tones (see Results) since
we wished to ensure that there was no undermasking (see Discussion).
The air-conducted stimuli were calibrated
using a Briiel & Kjaer model 2230 sound level
meter with a DBO138 2-cc coupler. On repeated
testing, the accuracy of calibration for airconducted tones was ± 2 .5 dB . The bone-
Stimulus Parameters
Right Ear
Left Ear
f (Hz)
fn (Hz)
Phase (degrees)
Amplitude
f (Hz)
f (Hz)
Phase (degrees)
Amplitude
500
915
1850
80 .08
84 .96
89 .84
45
315
315
20 .00
11 .91
15 .00
500
915
1850
78 .12
83 .01
86 .91
45
315
315
20 .00
11 .91
15 .00
3810
94 .73
315
15 .89
3810
91 .80
315
15 .89
209
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
conducted stimuli were calibrated using a Bruel
& Kjaer Artificial Mastoid Type 4930 (ANSI
1992, 1997) with a static application force equivalent to that used on subjects during the experiment. The levels were calibrated in decibel
hearing level for bone-conduction stimuli presented to the mastoid with unoccluded ears .
The accuracy of calibration for the bone-conducted stimuli was ± 5 dB . At the levels used
for our recordings (20 and 30 dB HL), there was
no measurable mechanical distortion artifact
above the noise floor (about -10 dB HL) at the
MASTER modulation frequencies.
Recordings
Each of the four experiments was carried out
in one session that lasted about 2 hours. Electrophysiologic responses were collected from a
gold-plated Grass electrode located at Cz and referenced to the midline posterior neck (7-8 cm
below the inion) . All electrode impedances were
under 5 kOhm at 10 Hz . Recordings occurred in
a sound-attenuated testing booth with the subjects sleeping in a reclining chair. The subjects
slept through most of the experiments . The
responses were amplified using a Grass P50
battery-powered amplifier with a filter handpass of 3 to 300 Hz . The MASTER data acquisition system (John and Picton, 2000b; see also
<w.hearing.cjb .net>) collected the data using
an analog-digital conversion rate of 1 kHz with
12-bit precision. Consecutive data epochs of
1 .024 seconds were linked together to form
sweeps of 16 .384 seconds, which were averaged
and then submitted to a fast Fourier transform
(FFT) to produce an amplitude spectrum with
a resolution of 0.061 Hz . When an epoch contained electrophysiologic activity exceeding
±90 nV it was rejected, and the next acceptable
epoch was used to build the sweep .
Table 3
Subjects
Sensorineural
hearing impaired
Normal hearing
Combined
Simulated conductive
hearing loss
Normal-hearing bone
conduction
Weighted averaging (John et al, 2001a) was
used to combine sweeps . Briefly, weighted averaging involves multiplying the data in each
recorded epoch (1 .024 sec of data) by a factor that
is inversely scaled by the amount of variance in
that particular epoch. The more noise in a recording, the less it contributes to the overall average.
To determine if the FFT components at the
stimulus modulation frequencies were different than background electroencephalographic
activity, the value at each of these frequencies
was compared, using an F ratio, to the 120 adjacent frequencies (60 bins above and 60 below the
stimulus frequency, or -3 .7 Hz), excluding those
frequencies at which other stimuli were modulated. Comparing this ratio against the critical
values for F at 2 and 240 degrees of freedom gives
the probability of a response being within the distribution of the background noise (John and
Picton, 2000b) . Responses were considered significantly different from background noise when
p < .05 .
Threshold Estimations
Behavioral thresholds were established for
the pure tones using a standard 10-dB down
5-dB up searching protocol (Carhart and Jerger,
1959).
For the physiologic thresholds, stimuli were
initially presented at 20 dB above the behavioral
PTA. If the initial stimulus level did not yield
eight significant responses (four if hearing was
unilateral), the intensity was increased by 10 dB
until all responses reached significance . Stimulus presentation level never exceeded 90 dB HL
and was never set at levels that caused discomfort to the subject. The recording was stopped
if any of three criteria were met . First, the
recording was stopped when the responses to all
stimuli presented at an intensity above behav-
Difference between Physiologic and Behavioral Thresholds
Carrier Frequency (Hz)
Number
of Subjects
500
1000
2000
31
13 - 11 (-10-+40)
5 ± 8 (-15-+30)
5 ± 9 (-15-+25)
14
45
10
17 ± 10(-10-+35)
14 ± 11 (-1-+40)
20 - 10(0-+35)
4 - 11 (-15-+25)
5 - 9 (-15-+30)
15 ± 8 (0-+30)
4 - 8 (-5-+25)
11
22 - 8(10-+40)
14 - 5 (5-+20)
Differences are in decibels . Results are given as mean - SD, with range in brackets .
210
4000
8 ± 11 (-20-+40)
11 - 7 (-5-+25)
5 ± 9 (-15-+25)
11 ± 7 (-5-+25)
9 - 10 (-20-+40)
13 ± 9 (-5-+30)
5 ± 8 (-5-+20)
5 ± 10 (-10-+20)
Audiometry Using MASTER/Dimitrijevic et al
ioral threshold reached significance . In cases
in which there was a sloping hearing loss, stimuli were below behavioral thresholds for some
carriers and suprathreshold for other carriers .
Second, the recording was stopped when the
mean noise level was below 10 nV Third, the
recording was stopped after reaching a maximum
allotted recording time of 17 minutes (equivalent
to 64 sweeps, each lasting 16 .384 sec) . Typically, a noise level of 10 nV was reached after
about 15 minutes of recording .
In some cases (n = 26 ears), less than four
stimuli per ear were used to estimate hearing
thresholds . In many of these ears, this occurred
when there was a steeply sloping high-frequency
hearing loss . Even when some stimuli were still
below threshold, the other suprathreshold stimuli could be uncomfortably loud for a subject, and
we continued with single stimuli. In these subjects, a comparison could not be made between
the thresholds estimated with four stimuli and
with one stimulus . In 17 ears, a formal comparison could be made between threshold estimation using multiple stimuli and using one or
two stimuli. In 11 ears, this was done because
the physiologic thresholds were more than 20 dB
greater than the behavioral thresholds . In the
other ears, the extra testing was performed
since the subject was willing to donate some
extra time .
Physiologic thresholds were primarily
defined as the lowest intensity level at which
there was a significant response . In 13 cases (of
a total of 348 threshold estimations), nonsignificant values were recorded for highintensity stimuli even though significant
responses were recorded at lower intensities .
In these cases, the absent response at high
intensity might have been a "miss" or the present response at lower intensity might have
been a "false alarm ." We therefore used a secondary rule that if the difference between the
louder (nonsignificant) and softer (significant)
stimulus was 20 dB or greater, the threshold was
taken to be the intensity of the louder stimulus .
If the difference was 10 dB, then the threshold
was taken to be the intensity of the less intense
stimulus . In some cases (five at 500 Hz, two at
1000 Hz, five at 2000 Hz, and eight at 4000 Hz),
no significant responses were recorded, regardless of intensity. In these cases, the threshold was
arbitrarily set to 10 dB above the highest intensity presented.
Physiologic thresholds for bone-conducted
stimuli were determined in 11 normal subjects
using the four stimuli . Additional recordings
were performed with white noise added to the
bone-conducted stimuli in 10 subjects . In four
separate recordings, MASTER stimuli were presented at two intensity levels, 20 and 30 dB HL,
both with and without white noise, at an effective masking level (on the audiometer) of 50 dB
HL . The actual behavioral masking level was
checked by presenting the MASTER stimuli at
30 dB HL and increasing the noise intensity
until the MASTER stimulus could not be recognized . The mean level was 37 dB (range 35-40) .
The white noise was therefore approximately
13 dB higher than the intensity needed for perceptual masking.
Statistical Analyses
The main variable for analysis was the difference between the threshold estimated using
MASTER (the physiologic threshold) and the
threshold estimated using pure-tone audiometry (the behavioral threshold) . Changes in this
variable between different subject groups were
evaluated using a two-way group by carrier frequency analysis of variance (ANOVA) with
repeated measures across carrier frequency.
Relations between variables were evaluated
using linear regression, and the significance of
these relations was assessed using Pearson
product-moment correlation coefficients . Incidence data were assessed using the cumulative
binomial distribution function .
The amplitudes and phases of the responses
were quite variable . Recordings were stopped
when responses were recognized rather than
when a good signal-to-noise ratio was obtained .
Many of the measurements were therefore contaminated with more residual noise than usual .
Furthermore, comparing measurements across
groups at equivalent sensation levels led to
unequal numbers at different intensities . Rather
than dispensing with these data entirely, we
decided to present grand mean data and to evaluate these in terms of general trends .
RESULTS
Subjects with Sensorineural Hearing
Impairment or Normal Hearing
The amplitude of the responses increased
with increasing intensity above threshold in
both the subjects with hearing impairment and
the normal subjects . Figure 2 shows the amplitudes of the responses plotted relative to behavioral threshold in the two groups of subjects
211
Journal of the American Academy of Audiology/ Volume 13, Number 4, April 2002
80
60
40
20
0
80
60
40
20
0
9 Hearing impaired
o Normal hearing
0
10
20
30
40
0
10
20
30
40
Intensity (dB SL)
Figure 2 Amplitudes of steady-state responses. Amplitudes for the responses to air-conducted MASTER stimuli are
plotted for normal-hearing and hearing-impaired subjects . The intensity is given in decibel sensaton level, or decibel
across all subjects for whom
above each subject's behavioral threshold for pure tones. Data have been collapsed
intensity increases for all
amplitude
increases
as
the
stimulus
each
intensity.
Response
responses were available at
circarrier frequencies: 500 Hz (top left), 1000 Hz (top right), 2000 Hz (bottom left), and 4000 Hz (bottom right) . Filled
subjects
.
represent
the
normal-hearing
subjects
and
open
circles
cles represent hearing-impaired
using only those responses that were considered significantly different from noise. Average
amplitudes across the carrier frequencies are
shown in the left graph of Figure 3 (together with
other results) . Since behavioral thresholds were
accurate to within 5 dB and the physiologic
measurements were obtained only in 10-dB
steps and only for certain intensities, the data
are based on different groups of subjects at the
different intensities and could not be analyzed
using an ANOVA. Nevertheless, the amplitudes
are clearly larger for the patients with sensorineural hearing loss compared to normal subjects. Only 2 amplitudes of 28 failed to show a
higher amplitude for the normal subjects
(p < .001 using the binomial distribution to
assess the probability that this number or lower
212
occurs in a sample of this size at a probability
of .5).
The onset phase was more variable across
subjects than the amplitude. To evaluate phase,
we therefore collapsed data across frequencies.
Phases were averaged geometrically because of
their circularity. In normal subjects, the onset
phase of the responses increased significantly
with increasing intensity (slope of 2.6 degrees/dB),
but this did not occur in the patients with sensorineural hearing loss (slope of 0.2 degrees/dB).
The right graph of Figure 3 plots these effects of
intensity on onset phase.
Figure 4 shows the steady-state responses
and plots the behavioral and physiologic thresholds in an 80-year-old patient with a moderate
bilateral hearing loss caused by Meniere's
Audiometry Using MASTER1Dimitrijevic et al
80
Z
60
b
40
o.
C
O
20
-135
0
0
10
20
30
-180
40
0
dB SL
10
20
30
40
dB SL
" Bone conduction (normal hearing)
V Air conduction (normal hearing)
A Air conduction (hearing impaired)
E Air conduction (simulated conductive hearing loss)
Figure 3 Amplitudes and phases . Average response amplitudes (left graph) and onset phases (right graph) for airand bone-conducted MASTER stimuli. Data have been collapsed across carrier frequency. Measurements for responses
to air-conducted stimuli (normal hearing, hearing impaired, and simulated conductive hearing loss) are averages of the
left and right ears . For both graphs, circles represent bone-conducted stimuli, triangles represent air-conduction stimuli in hearing-impaired subjects, in uerted triangles represent normal-hearing subjects, and squares represent air-conducted
stimuli in subjects with simulated conductive hearing loss .
disease. The amplitude spectra of the electroencephalographic recordings at various presentation levels are shown on the left . Stimuli
presented at 80 dB HL resulted in eight significant responses (four per ear) . The number of sig-
nificant responses decreased with decreasing
intensity. The figure demonstrates how physiologic thresholds were determined . For example,
when evaluating the physiologic threshold at
500 Hz in the right ear, significant responses
MASTER Recordings
Thresholds
0.5
40
v
Right 0
v
v
30
50
v
60
60
v
vV
1
4
tH
H
VV
Left
70
70
80
90
100
Modulation Frequency (Hz)
110
Hz portion of the response spectra is
plotted. The triangles indicate when the
responses were significantly different
from the background noise (right ear,
open triangles; left ear, closed triangles) .
For each carrier frequency, threshold is
80
dB HL
2
Figure 4 Threshold estimation using
MASTER. This figure demonstrates how
kHz physiologic thresholds are determined .
The subject is a patient with a sensorinerual hearing loss due to Meniere's
disease. The left side of the figure shows
the auditory steady-state responses and
the right side shows the behavioral and
MASTER audiograms . Steady-state
stimuli were presented at 40, 50, 60,
70, and 80 dB HL . Only the 70- to 110-
120
dB HL
tt
0
O Behavioral
MASTER
defined as the lowest intensity that produced a significant response. For example, the 500-Hz left ear response was
significant at 80, 70, 60, and 50 dB HL
but not significant at 40 dB HL . Therefore, the threshold is 50 dB HL . MASTER thresholds are shown by the black
diamond in the audiograms .
213
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
(open triangles) were recorded at 80, 70, 60,
and 50 dB HL and no response was found at
40 dB HL. The physiologic threshold was therefore determined as 50 dB HL, as is shown on the
audiogram on the right .
Of the 348 physiologic thresholds obtained
(59 ears with sensorineural hearing loss and 28
normal ears, each at four frequencies), the
physiologic-behavioral threshold difference was
less than or equal to 15 dB in 83 percent of the
responses. The mean results are presented in Figure 5 and compared between groups in the upper
part of Table 3. The data plotted in Figure 5 also
show the range of values since the upper and
lower T bars show the 10th and 90th percentiles
of the distribution . Combining the threshold estimations across the carrier frequencies showed a
median value (50th percentile) of 5 dB with the
10th and 90th percentiles at -5 and 25 dB . The
p < .5 confidence limits (2 .5th to 97 .5th percentile) for the threshold estimations were -10
and 30 dB .
The normal and hearing-impaired groups
were compared using a two-way (group by carrier frequency) ANOVA. The mean differences
between behavioral and physiologic thresholds
were not significantly different in hearingimpaired subjects compared to those with normal hearing (main effect of group: F = 0.7, df = 1,
85, p > .05) . In both normal-hearing and hearingimpaired subjects, the greatest difference
between the physiologic and behavioral thresholds was seen for the 500-Hz carrier frequency
T
T
500
1000
'J'
2000
i
4000
Carrier Frequency (Hz)
Figure 5 Physiologic-behavioral differences . This figure shows the differences in physiologic and behavioral
differences for each carrier. The box boundaries represent
the 25th and 75th percentile limits, and the T bars show
the 10th and 90th percentile limits . The median (50th percentile) is represented by the horizontal line in the box,
and the asterisks show the mean . The number of ears for
which data were obtained (same for each frequency) was
87 .
214
(main effect of carrier frequency: F = 23 .0, df = 3,
285, p < .001). There were no significant interaction effects .
The physiologic thresholds were significantly correlated with behavioral thresholds .
The results of the regression analyses are plotted in Figure 6 and the regression parameters
are given in Table 4. The probabilities of the correlation coefficients were all less than .001 .
We compared the level of noise in the recordings to the magnitude of the physiologic-behavioral
threshold differences to determine whether noisier recordings produced higher threshold differences. Because of the different stopping conditions,
it was not simple to measure a comparable level
of the residual background noise across the recordings . To estimate the amount of noise that was present in the recordings, we used the recording
obtained at the lowest sound level since this went
for the full 17 minutes, or 64 sweeps (since no
responses were significant). We used simple rather
than weighted averaging. The correlation coefficients with the thresholds at 500, 1000, 2000,
and 4000 Hz were 0.06, 0.17, 0.07, and 0.01, none
of which were significant .
In the 17 ears for which the thresholds could
be compared between single and multiple stimuli, 12 ears were presented with only a 500-Hz
stimulus, 1 ear was presented with a 2000-Hz
stimulus, and 4 ears were presented with a
4000-Hz stimulus . In the 500-Hz alone stimulus condition, the mean difference between MASTER and behavioral thresholds was 17 - 8
compared to 19 ± 10 dB in the four stimulus conditions (not significant) . For the 2000- and
4000-Hz stimuli combined, the mean differences
were 9 ± 7 and 21 - 11 dB for the singlestimulus and four-stimulus conditions, respectively (t = 6.0, df = 4, p < .01) .
Simulated Conductive Hearing Loss
The simulated conductive hearing loss
resulted in flat audiograms for all subjects . The
physiologic-behavioral differences are presented
in Table 3 . An ANOVA comparing these differences with those of the patients with sensorineural hearing loss showed a main effect of
carrier frequency (F = 9.4, df = 3, 228, p < .01),
with the difference being larger at 500 Hz than
at other carrier frequencies . There was also a significant main effect of group (F = 21 .8, df = 1, 76,
p < .001), with the differences being larger in the
subjects with a simulated conductive hearing
loss . There was no significant interaction
between group and frequency. The average
Audiometry Using MASTER/Dimitrijevic et al
Figure 6 Regression analyses .
This figure shows the regression
lines between behavioral and physiologic thresholds for 500 Hz (top
left), 1000 Hz (top right), 2000 Hz
(bottom left), and 4000 Hz (bottom
right) and all of the carriers combined (middle plot) . The data used
for these regressions come from the
Thresholds
Behavioral
(dB HL)
31 hearing-impaired subjects and
the 14 normal-hearing adults (subject groups 1 and 2) . The size of the
points varies with the number of
overlapping points .
Physiologic
(dB HL)
amplitudes and phases are plotted in Figure 3
(together with those for the normal subjects and
those with sensorineural hearing loss).
Bone-Conduction Responses
The behavioral thresholds for the various
bone-conduction stimuli are given in Table 5. The
mean amplitudes and phases are shown in Figure 3, and sample bone-conduction results are
shown in Figure 7 . Figure 7 uses polar plots to
show both the amplitudes and the phases of the
responses. Using the amplitude spectrum to
show the responses, as was done in Figure 4, does
Regression Analyses
Table 4
Carrier
Frequency
500
1000
2000
4000
All carriers
Number
of Points
Slope
(m)
Intercept
(b)
r
87
0.88
-8 .87
85
87
348
0.99
0.92
-8 .32
-4 .47
95
92
87
87
0 .92
0 .89
-1 .46
-0 .21
94
95
The regression equation is of the form y = mx + b, where y
is the behavioral threshold for pure tones, x is the physiologic
threshold for the MASTER responses . m is the slope, and b is the
y intercept .
not provide any information about the phase of
the responses. A polar plot is constructed such
that the amplitude of the response (at only one
bin in the spectrum where the frequency equals
the modulation frequency) is represented by the
length of the line (or vector) departing from the
origin (the cross) and the phase is represented
by the angle between the response line and the
horizontal axis . The onset phase normally
decreases (the vector moves clockwise) with
decreasing intensity (discussed more fully in
John and Picton, 2000a) . Responses are recognized in the spectrum by comparing the amplitude at the modulation frequency to the
amplitudes in the adjacent bins . In the polar plot,
the confidence limits of the amplitudes in these
adjacent bins can be plotted as a circle, and this
circle can be positioned over the furthest extent
of the amplitude vector . If the circle does not
include the origin (the shaded circles in the
figure), then the response is significantly different from the noise levels recorded in adjacent
frequencies.
The amplitudes of the responses were larger
than those found in normal subjects for air conduction . Although in some subjects, the phases
changed quite regularly (see Fig . 7), the mean
onset phases were quite variable . Although overall they tended to be a little larger than those for
215
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
Table 5
Behavioral Bone-Conduction Thresholds
Frequency (Hz)
Threshold
500
1000
2000
4000
5 .0 ± 3 .6
3 .8--2 .9
2 .7±6 .3
0 .9±6 .9
3 .6±8 .2
0 .9±8 .0
-2 .7±4 .6
-4 .1 +4 .6
7 .2 ± 5 .4
5 .9--4 .6
4.8±7 .0
2 .8±6 .8
5 .0-8 .0
2 .8!-8 .4
2 .7±5 .2
0 .3±4 .3
-5 .6--5,4
0 .3--6 .2
-5 .0-8 .4
1 .3±9 .2
5 .0±7 .7
6 .3±7 .4
5 .9-!-5 .5
5 .0-!-6 .8
Air conduction
Pure tone
Mean
Best of ears
Modulated
Mean
Best of ears
Bone conduction
Pure tone
Modulated tone
Mean = SD in dB HL (for mastoid placement and for unoccluded ears) . As discussed in the text,
the forehead placement and the
occlusion of the ears will change these thresholds . Data from 16 subjects .
air conduction (on average 40 degrees between
5 and 30 dB SL), the mean bone-conduction
phases did not show any clear relationship with
dB HL
500
1 kHz
2 kHz
4 kHz
20
10
50 nV
-10
0
Nonsignificant
0
Significant
Figure 7 Response to bone-conducted stimuli. The
bone vibrator was located on the forehead. This figure presents the data from a single subject, whose behavioral
bone-conducted pure-tone thresholds were -10, -10, 0, and
10 dB HL at 500, 1000, 2000, and 4000 Hz, respectively.
The data are presented in polar plots such that the onset
phase of the response is represented as the angle from
the x-axis measured counterclockwise . As intensity
decreases, the onset phase decreases (the vectors move
clockwise) . Since phase delay is equal to 360 minus the
onset phase, this means that the phase delay increases
with decreasing intensity. The p < .05 confidence limits
of the residual noise in the recording are plotted as a circle centered at the point of the amplitude vector. If the
circle does not include the origin (shaded circles), the
response is significantly different from zero at p < .05.
Since the recording at 20 dB HL was based on averaging 15 sweeps, the noise level is higher in this recording
than in those at the lower intensities, where the recordings were based on 64 sweeps . Physiologic thresholds were
determined as 20, 0, 10, and 10 dB HL .
216
sensation level. These data were more variable
than those for the air-conduction studies since we
were not able to combine data across right and
left ears. The mean differences between MASTER
and behavioral thresholds for the bone-conduction stimuli are presented in Table 3. An ANOVA
comparing the physiologic-behavioral threshold
differences with bone conduction to air conduction showed no main effect of air versus bone but
a significant effect of carrier (F = 18 .8, df = 3, 37,
p < .001), with the 500-Hz measurement being
higher than the others, and a significant interaction (F = 5.5, df = 3, 37, p < .01), with the
500-Hz threshold difference being higher for
bone conduction than for air conduction .
The masking effects were examined using
a three-way (masking, intensity, carrier frequency) ANOVA. As shown in Figure 8, white
noise masking significantly decreased the amplitude of the MASTER responses (F = 36 .3, df = 1,
9, p < .001). There were also significant effects
of intensity (F = 12 .5, df = 1, 9, p < .01) and a
significant interaction between intensity and
masking (F = 13 .4, df = 1, 9, p < .01) caused by
the noise floor limiting the masking change so
that it was less for the less intense sound. The
other tests were not significant. Usually, the
masked responses were no longer recognizable
in the background noise. However, the incidence
of significant responses in the masked conditions
was higher than the 5 percent false alarm rate
predicted from the F statistic used to determine
whether a response was significant (Table 6) . At
the 30-dB intensity, the incidence of seven false
positives of a total of 40 evaluations (17.5%)
was significantly different from the expected
5 percent at p < .001 using the binomial distribution to check the probability of obtaining this
Audiometry Using MASTER/Dimitrijevic et al
80
60
Stimuli
40
30 dB
30 dB
20 dB
20 dB
Masking
Noise levels
Noise levels
20
0
500
1000 2000 4000
Carrier Frequency (Hz)
Figure 8 Masking of bone-conduction responses . The
figure plots the amplitudes of the responses to multiple
stimuli presented through bone conduction with the
vibrator on the forehead and both ears occluded . The
MASTER stimuli were presented at 20 and 30 dB HL with
and without masking. In the masking condition, the
stimuli were presented mixed with white noise at 50 dB
HL equivalent masking. The squares show the mean
level of electrical noise in the recorded data with and without masking .
number of false alarms or more from a sample
of this size . There were no differences in the background noise levels between the unmasked and
the masked conditions .
DISCUSSION
T
he results of this study are similar to others reported in the literature . In normal-
hearing subjects, we found mean differences
between MASTER and behavioral thresholds
of 17, 4, 4, and 11 dB for the 500-, 1000-, 2000-,
and 4000-Hz carriers, respectively. These differences are similar to other comparable studies (tins et al, 1996 ; Picton et al, 1998 ; Herdman
and Stapells, 2001 ; Perez-Abalo et al, 2001).
For example, using AM tonal stimuli in naturally
sleeping adults, Herdman and Stapells (2001)
found differences between MASTER and behavioral thresholds of 14, 8, 8, and 9 dB . In hearingimpaired subjects, using MM stimuli, we found
that the difference between physiologic and
Table 6 Steady-State Responses
to Bone-Conducted Stimuli
Stimulus
Intensity
(dB HL)
30
30
20
20
Effective
Masking
Level (dB)
Number of
Significant
Responses (of 40)
Percentage
Significant
50
-10
50
7
36
2
17 .5
90 .0
5 .0
-10
30
75 .0
behavioral thresholds was 13, 5, 5, and 8 dB for
the 500-, 1000-, 2000-, and 4000-Hz carriers,
respectively. Previous studies (Rance et al, 1995 ;
Lins et al, 1996 ; Picton et al, 1998 ; Perez-Abalo
et al, 2001) have reported similar results . For
example, Perez-Abalo and colleagues (2001)
found differences of 13, 7, 5, and 5 dB . Our
results with bone conduction (22, 14, 5, and 5 dB)
are similar to those (11, 14, 9, and 10 dB)
reported by Lins and colleagues (1996), except
at 500 Hz . We shall discuss this difference later.
Factors Affecting Threshold Estimation
Several points must be considered when
comparing studies using auditory steady-state
responses to estimate thresholds . First, the
method of determining threshold can vary. In this
study (and in the majority of other studies),
physiologic thresholds were determined using a
bracketing technique. This technique involves
initially presenting a stimulus at sufficient
intensity to record a response significantly different from the background noise and then
reducing the stimulus intensity until no response
is recognizable . The threshold is defined as the
lowest stimulus intensity at which a response can
be distinguished from background noise.
The physiologic threshold is usually higher
than the behavioral threshold, and this difference may vary with the frequency and with the
degree of hearing loss . Rance and colleagues
(1995) used regression analyses to estimate
behavioral thresholds from physiologic thresholds . If the slope of the regression differs from
1.0, this is more accurate than simply subtracting the mean difference between the two
techniques from the physiologic threshold . For
our particular data set, the slopes of the regressions were close to 1.0 (see Table 4) .
Another method for determining threshold
takes advantage of regular relationships between
stimulus intensity and the response amplitude
and/or phase. Generally, as the stimulus level
decreases, the response amplitude decreases
and the onset phase of the response decreases
(changes in a clockwise direction when plotted
on polar plots) . Based on either amplitude or
phase, or both, one could extrapolate from two
or more high-intensity responses to obtain an
intensity at which the responses should have
gone away. A major problem with this approach
is that the functions used for extrapolation may
not be valid in patients with hearing loss .
Another difference among studies is the size
of the intensity steps at which the responses are
217
Journal of the American Academy of Audiology/Volume
13, Number 4, April 2002
recorded . In this study, 10-dB steps were used .
Although using 5-dB increments will yield more
accurate thresholds, significantly more time is
then needed to determine the threshold.
Also, the state of the subjects must be considered . Recordings can be made while the subjects are awake, in natural sleep or sedated.
Many auditory steady-state threshold studies
have used sedated children . This will decrease
levels of physiologic noise and therefore make the
responses easier to detect at near-threshold values. This will, in turn, cause smaller differences
in physiologic and behavioral thresholds .
A final factor is the noise level at which a
response is judged to be absent . This will depend
on both the state of the subject (which determines
the amount of noise to be reduced) and also on
the extent of noise reduction by the analysis
procedure . Noise reduction by averaging varies
with the time over which the recording is continued . Ifthe threshold estimation procedure considers that a response is absent (and therefore
that the stimulus intensity is below threshold)
at a noise level of 20 nV then the physiologic
thresholds will be higher than if one uses a criterion level of 10 nV Since we averaged until the
noise level was below 10 nV or for 17 minutes
(in which case, the noise level was close to 10 nV),
the noise level of the recording did not explain
the variance in our threshold estimations. This
variance was then likely attributable to the
variance in the amplitude of the response among
the different subjects .
Several conditions must be met if one wishes
to compare how well two techniques (e .g., tonepip ABR versus steady-state responses or multiple
versus single steady-state responses) estimate
audiometric thresholds . First, one must set up
the optimal recording parameters for each technique . Second, one must evaluate each over the
same period of time . Third, the evaluations must
be done in the same subjects or types of subjects .
Unfortunately, such comparisons are not presently available .
Types of Hearing Impairment
In this study, the subjects with sensorineural
hearing impairment showed slightly smaller
differences between physiologic and behavioral
thresholds than subjects with normal hearing.
This difference (between rows 1 and 2 of Table
3) was not significant . Nevertheless, similar
results were found in other studies (Rance et al,
1995 ; Lins et al, 1996 ; Picton et al, 1998 ; PerezAbalo et al, 2001). Furthermore, we did find
218
that the physiologic-behavioral differences in
the subjects with simulated conductive hearing
impairment (row 4 of Table 3) were significantly
larger than the differences in patients with sensorineural hearing loss . This phenomenon has
been related to recruitment (Lins et al, 1996).
The basic idea is that the response increases in
amplitude more quickly with increasing intensity in subjects with sensorineural hearing loss .
This would make it easier to recognize the
response at intensities close to behavioral thresholds . Other reasons related to the absolute intensity of the stimuli may also play a role since we
did not find any threshold difference between the
subjects with sensorineural hearing loss and
those with normal hearing.
Response amplitudes in the subjects with
sensorineural hearing loss were significantly
higher than in the subjects with normal hearing
(see Fig. 2) . This result is compatible with the idea
that recruitment occurs in the subjects with sensorineural hearing loss . Once the stimulus was
above threshold, the response amplitude was
more determined by the absolute intensity of
the stimulus than by the sensation level. This
relationship may actually depend on the slope of
intensity change rather than the intensity.
The phase measurements were quite variable . This is likely attributable to the fact that
we stopped recording once responses were recognized, and this would occur at low signal-tonoise levels for some of the responses. The
measurement of phase provided by the MASTER
system is the phase of the signal at the onset of
the recording sweep . Onset phase can be converted to phase delay by subtracting it from 360
degrees . Phase delay can be related to latency,
although there are ambiguities in this relation
related to the circularity of phase measurements
(discussed more fully in John and Picton, 2000a) .
Phase measurements vary with both the carrier
frequency and the modulation frequency. However, it is justifiable to collapse across carrier frequency to view overall trends in the data (see Fig.
4) . The main findings were that the onset phases
in the subjects with sensorineural hearing loss
were larger (or the phase delays were shorter)
than in subjects with normal hearing, and these
did not appear to change with intensity. These
trends might be related to recruitment (the
sounds at equivalent sensation level being
processed as louder), to absolute stimulus intensity (sounds at equivalent sensation level being
more intense), or to a broadening of the tuning
curve (the less effective filter being associated
with a shorter filter build-up time). Resolving
Audiometry Using MASTER/Dimitrijevic et al
these possibilities would need more data collected with higher signal-to-noise ratios .
Efficiency of Testing
The efficiency of objective audiometry varies
with the rate at which threshold information is
collected . This rate can be altered by making the
noise level in the recording lower, making the
amplitude of the responses bigger, and testing
at multiple frequencies simultaneously. Several
techniques can decrease the noise level of the
recording. Since the main noise source is the
scalp and neck muscles and since sleep relaxes
these muscles, testing the subject when asleep
is important. Another approach of reducing noise
is to use weighted averaging (Ldtkenhoner et al,
1985 ; John et al, 2001a). Finally, the likely phase
of the response is known; the statistical testing
can be biased by projecting both noise and signal onto this expected phase (Dobie and Wilson,
1994 ; Picton et al, 2001). Response amplitudes
can be increased by using MM stimuli (Cohen
et al, 1991), exponential envelopes (John et al,
in press), or multiple carrier frequencies at the
same modulation rate (Sturzebecher et al, 2001).
MM stimuli have been used before in estimating behavioral thresholds (Rance et al, 1995,
1998) . In these studies, the maximum AM and
maximum FM occurred at the same time (H = 0
degrees) . We have previously shown that the
MM response amplitude varied with different
phases of AM and FM and that these differences varied with different carrier frequencies
(John et al, 2001) . In the current study, we used
MM stimuli with phases that gave maximum
response amplitudes in normal-hearing subjects . These "ideal" phases may not have been
optimal for the hearing-impaired population .
However, since the physiologic-behavioral differences for hearing-impaired individuals were
the same or slightly smaller than that obtained
for subjects with normal hearing, the phase values seemed to have worked successfully.
Recording responses to multiple simultaneous stimuli can increase the speed of testing
over recording response to individual stimuli. If
the responses do not interact when the stimuli
are presented together, if the response amplitudes are equal across the carrier frequencies,
and if the thresholds are equal at the different
audiometric frequencies, then recording
responses to four stimuli instead of one stimulus would speed the time of testing by a factor
of 4. However, as discussed more fully by John
and colleagues (2002), these conditions are not
always fulfilled. Nevertheless, testing with multiple stimuli should be faster (by perhaps a factor of 2 or 3) than testing each audiometric
frequency and each ear separately.
Multiple responses can be recorded in both
the frequency and time domains . In the frequency domain, multiple steady-state responses
are disentangled by selecting different modulation frequencies for each carrier frequency. Time
domain analyses can also be designed to disentangle multiple responses to concomitantly presented stimuli, for example, using maximum
length sequences (e .g., Hall and Rupp, 1997) . The
frequency domain analyses have an added
advantage in that the statistical tests for
response recognition are simple and reliable .
Effects of Carrier Frequency
The biggest discrepancy between physiologic
and behavioral thresholds was for the 500-Hz
stimulus . Other studies have found similar elevated thresholds for this frequency (Aoyagi et
al, 1994a ; Rance et al, 1995 ; Lins et al, 1996;
Herdman and Stapells, 2001 ; Perez-Abalo et al,
2001) . This 500-Hz discrepancy may be related
to issues of neural synchrony. There is likely
more latency jitter in the neurons responding to
the low-frequency sounds caused by both the
slowly changing stimulus and the broader region
of activation on the basilar membrane . The jitter
would decrease the time-locked summation of
responses . Interestingly, 500-Hz thresholds are
quite accurate when modulation rates in the
40-Hz range are used to evoke steady-state
responses (e .g., Dauman et al, 1984 ; Aoyagi et al,
1993) . The lower modulation rate may allow the
neurons to be more precisely time-locked to the
stimulus . Alternatively, the 40-Hz response is
mainly generated in the cortex, and it is also possible that the cortex has compensatory mechanisms that rely on other information in the
auditory code to make up for the decreased
synchrony.
Using stimulus envelopes different from a
simple sinusoid might evoke larger responses
and thereby compensate for the smaller response
at 500 Hz . John and colleagues (2001, in press ;
see Fig. 4) showed that changing the shape of the
stimulus envelope to an exponential sinusoid
with an exponent of 2 (as opposed to the firstorder sinusoidal envelopes typically used) can
increase response amplitudes by 20 to 25 percent
for the 500- and 4000-Hz carriers .
In some subjects, the physiologic thresholds at higher carrier frequencies (2000 and
219
Journal of the American Academy of Audiology/Volume 13, Number 4, April 2002
4000 Hz) showed significant elevations (around
20 dB) compared to the behavioral thresholds,
and these differences were significantly reduced
by presenting the stimuli singly rather than
together with multiple stimuli. Similar findings
were noted in a study of aided thresholds
(Picton et al, 1998). These effects may have been
caused by masking of high-frequency responses
by the concomitant low-frequency sounds . However, the high-frequency region of the basilar
membrane may have been unresponsive - a
"dead region," as described by Moore and colleagues (2000) . In this case, the response to the
single tone may have been mediated by spread
of activation to adjacent low-frequency regions
of the basilar membrane . This could have been
prevented by the masking effect of the lowfrequency stimuli in the multiple-stimulus condition . These different possibilities can be disentangled only by more sophisticated masking
experiments. The elevated thresholds in selected
patients at 500 Hz were not affected by changing between the single- and multiple-stimulus
protocol . These threshold elevations were likely
attributable to the relatively small size of the
response rather than to any unresponsiveness
of the cochlea.
Bone-Conduction Thresholds
Determining bone-conduction thresholds is
not an easy task even when thresholds are determined behaviorally. Thresholds vary with where
the vibrator is located on the scalp, how much
tension is used to hold it in place, and whether
the external ear canals are occluded (Dirks,
1994). Even when all of these variables are held
constant, bone-conduction thresholds are more
variable from one subject to the next than airconduction thresholds .
Two main factors affected our behavioral
thresholds for the bone-conducted stimuli : the
occluded ears and location of the vibrator on
the forehead . The main explanation for the occlusion effect is that the unoccluded ear allows
passage of bone-conducted sound in the cochlea
through the middle ear and out of the external
ear canal. The normal middle ear is exquisitely
designed to convey sound from the external ear
canal to the cochlea and works just as well in the
reverse direction. The energy activating the
cochlea is thus decreased by this loss of sound.
Occluding the canals attenuates this loss. Other
factors contributing to the occlusion effect are the
decrease in the background noise from air220
conducted sound, the relative phases of the boneconducted energy in the middle and inner ears,
and the acoustic filtering effects of the occluded
canal (which will vary with the depth of the
occlusion) (Tonndorf, 1972 ; Khanna et al, 1976).
Occluding the ear canals changes the thresholds
by -16, -8, 0, and 2 dB at frequencies of 500,
1000, 2000, and 4000 Hz (average of values from
Goldstein and Hayes, 1965, and Dirks and
Swindeman, 1967). When the vibrator is located
on the forehead, the thresholds are higher than
when it is located on the mastoid by 14, 9, 12,
and 8 dB at frequencies of 500, 1000, 2000, and
4000 Hz (Frank, 1982 ; ANSI, 1992). Summing
the effects of occlusion and forehead placement
together gives an expected difference between our
behavioral thresholds and the normal mastoid
thresholds with unoccluded ears (i .e ., hearing
level for bone conduction, to which our audiometer was calibrated) of -2, 1, 12, and 10 dB . This
pattern (low frequency less than high frequency)
fits with the behavioral thresholds in the bottom
two lines of Table 5.
The MASTER bone-conduction threshold
was higher at 500 Hz than we expected based
on the data obtained before by Lins et al (1996).
The resonance characteristics of the individual
human skull are unique, and there may be
changes of 20 dB or more across different skulls
(Khalil et al, 1979 ; Hakansson et al, 1994). The
changes in the bone-conduction thresholds at
500 Hz between the two studies could have been
owing to such effects. However, this is unlikely
since there were no specific changes in the behavioral thresholds at 500 Hz (see Table 5) . We are
left with some variability of the physiologic
thresholds at 500 Hz . The Lins and colleagues'
(1996) study used simple AM stimuli, whereas
the present study used MM stimuli. One possibility is that the AM and FM do not combine in
the same way with bone-conducted stimuli.
However, we feel that this is unlikely. The various frequency components of a modulated stimulus will experience magnitude scaling and
phase shifts during bone transmission that are
different than they would receive during transmission through the ear canal and middle ear
(Hakansson et al, 1996). However, given the
relatively narrow band of the MM stimuli, one
would not expect the signals to be significantly
altered at the cochlea relative to the mechanical output of the bone conductor. The possible role
of MM stimuli needs to be ruled out, but our present results may just be attributable to the
intrinsic variability of the MASTER thresholds
for 500-Hz carrier frequencies.
Audiometry Using MASTER/Dimitrijevic et al
Stimuli presented via bone conduction are
transmitted to both ears . When the vibrator is
placed on the mastoid, there is a slightly greater
activation of the ipsilateral cochlea for higher frequencies (Dunlap et al, 1988 ; Vanniasegaram et
al, 1994), although this difference is very small,
and protocols for clinical masking consider the
cochleae to be equally activated (Goldstein and
Newman, 1994) . When the vibrator is placed
on the forehead, the activation of the two ears
should be more exactly equal . If there is an
asymmetry in the thresholds of the cochleae or
asymmetry in the transmission of sound from the
forehead to the cochleae (Khalil et al, 1979), the
bone-conducted sound will cause greater activation of the cochlea with the lower threshold,
and the sound will be localized to that ear. Many
of our subjects reported such perceptual asymmetries . Nevertheless, since the steady-state
responses were effectively evoked by binaural
stimuli, their amplitudes should have been
larger than the responses evoked by monaural
air-conducted stimuli . Lins et al (1995) showed
that the responses to binaural air-conducted
stimuli were equal to the sum of the responses
to monaural stimuli . Lins et al (1996) found
that the binaural bone-conduction response was
actually larger than the sum of the monaural
responses (obtained by masking one ear via air
conduction) . This difference may have been
caused by the masking used to isolate the monaural bone-conduction response . The data in Figure 3 show that the binaural bone-conduction
responses were approximately twice the size of
the monaural air-conduction responses in subjects with normal hearing for higher-intensity
sounds, although these differences were not
clear for sounds of lower intensity.
The phases of the responses to boneconduction stimuli were highly variable . This
was in part owing to the noise levels in the
recording, since we stopped averaging as soon as
responses were detected, and in part owing to the
variability of skull transmission characteristics .
The responses were earlier (had a larger onset
phase) than the air-conduction responses . Part
of this difference was caused by the air-conduction responses being evoked by stimuli delayed
by the time taken to pass through the tube from
earphone to ear canal -0 .9 msec or approximately one-twelfth of a cycle (30 degrees) at the
modulation frequencies being used . Some subjects showed clear decreases in onset phase
with decreasing intensity (see Fig. 7), although
this was not apparent in the collapsed data
(see Fig. 3) .
There are two ways to determine boneconduction thresholds . One can simply present
the stimuli directly through a bone-conduction
vibrator and evaluate the thresholds . Air-conducted masking is usually necessary to isolate
the responses of one ear from the other. In bilateral conductive hearing loss, this is not always
possible . The sensorineural acuity level (SAL)
test (Jerger and Jerger, 1965) measures the
amount that air-conduction thresholds are
increased by noise presented through bone
conduction . Cone-Wesson and colleagues (2002c)
have used the SAL technique to estimate boneconduction thresholds with steady-state
responses and found the results promising.
We have used the direct approach to estimating bone-conduction thresholds with the
steady-state responses . In the acoustic spectra
of air-conducted stimuli, energy exists only at the
carrier frequency and at its sidebands, not at the
modulation frequency. Accordingly, there is no
acoustic energy at the rate of modulation in the
stimulus itself. Any electrical artifact from the
air-conduction transducer would have no energy
at the modulation frequency. The boneconduction transducer may not reproduce the
stimuli with the same fidelity and may generate electrical activity at the frequency of modulation . If this electrical activity is picked up as
an artifact in the scalp recording, one may not
be sure whether the recorded responses are
coming from the brain or from the bone vibrator . We believe that our responses were not artifactual because the amplitude changed less with
intensity than a stimulus artifact (which would
generally triple with a 10-dB increase), because
in some subjects the onset phase of our recorded
responses decreased regularly with decreasing
intensity (see Fig. 7), and because the thresholds
were related to behavioral thresholds in a similar manner to air-conduction thresholds . However, artifacts are clearly possible since the
bone-conduction vibrator and its interface with
the skin may be nonlinear and thus generate
activity at the modulation frequencies .
White noise masking might be a helpful
tool in determining whether the recorded
responses are contaminated by artifact . In our
experiment, white noise masking at levels sufficient to eliminate the hearing of the sounds significantly attenuated the response (see Fig. 8) .
The premise of the masking experiment was
that an electrical artifact would not have been
affected by the masking noise, other than that
the background electrical noise level of the
recording might have been increased by the
221
Journal of the American Academy of Audiology/Volume 13,
Number 4, April 2002
artifact from the random noise stimulus . The fact
that the noise levels in our recording were not
significantly affected by the presence of masking noise itself suggests that the bone-conduction
vibrator caused very little artifact .
Choosing the level of white noise to mask the
response was not simple . We chose levels that
were about 15 or 25 dB above the levels necessary to mask perception . The problem is that perceptual masking may occur at levels of the
nervous system higher than the levels generating the steady-state responses . In this situation, a physiologic response might be recognized
even when there is no perception . When deciding on masking levels for the derived response
technique, one can ensure that the physiologic
response is masked, but this approach is not
helpful if one is worried that the physiologic
response may be contaminated by artifact . It is
possible that the higher number of false alarms
for the 30 dB HL stimuli was caused by undermasking. However, we feel that it was more
likely that small electrical artifacts from the
bone conductor were recorded . In clinical situations, if a bone-conduction MASTER response
is detected, one can then rule out an artifact by
presenting the stimuli in masking noise and
seeing whether this significantly attenuates the
response .
Another approach to estimating the incidence and size of bone-conductor artifacts would
be to record the steady-state responses to subthreshold bone-conducted stimuli in patients
with bilateral sensorineural hearing loss .
CONCLUSIONS
T
his study showed that the thresholds for
MASTER can predict behavioral thresholds . On average, across all carrier frequencies,
physiologic thresholds were 8 dB higher than
behavioral thresholds for air-conducted stimuli. The overall confidence limit (p < .05) for
these differences is -10 to 30 dB . One in 20 estimations will equal or exceed these limits. Both
air- and bone-conduction thresholds can be estimated. When using bone conduction, one must
be careful to rule out electrical artifacts. White
noise masking might be helpful in this regard .
Acknowledgment . This research was supported by the
Canadian Institutes of Health Research . The authors
also thank James Knowles and the Baycrest Foundation
for addititional support. Some of these results were presented at the International Evoked Response Audiometry
Study Group meeting in Vancouver, British Columbia,
222
Canada, July 2001 . Preliminary data were also presented
in a talk at the 8th Symposium on Cochlear Implants in
Children, March 2000, which will be published in Annals
of Otology, Rhinology and Laryngology (in press) .
REFERENCES
American National Standards Institute. (1992). Reference
Zero for the Calibration of Pure-Tone Bone-Conduction
Audiometers. (ANSI 53 .43-1992). New York : ANSI.
American National Standards Institute . (1996). American
National Standard Specification for Audiometers. (ANSI
S3 .6-1996) . New York : ANSI .
American National Standards Institute. (1997) . American
National Standard Mechanical Coupler for Measurement
ofBoneVibrators. (ANSI S3 .13-1987 [R1997]) . NewYork :
ANSI .
Aoyagi M, Kiren T, Furuse H, et al . (1994a) . Pure-tone
threshold prediction by 80-Hz amplitude-modulation
following response . Acta Otolaryngol (Stockh) 511:7-14.
Aoyagi M, Kiren T, Furuse H, et al . (1994b) . Effects of
aging on amplitude-modulation following response. Acta
Otolaryngol (Stockh) 511 :15-22 .
Aoyagi M, Kiren T, KimY, et al. (1993). Frequency specificity of amplitude-modulation-following response detected
by phase spectral analysis. Audiology 32 :293-301 .
Carhart R, Jerger JJ . (1959) . Preferred method for clinical determination of pure-tone thresholds . J Speech Hear
Res 24 :330-345 .
Cohen LT, Rickards FW Clark GM . (1991) . A comparison of steady-state evoked potentials to modulated tones
in awake and sleeping humans . J Acoust Soc Am
90 :2467-2479 .
Cone-Wesson B, Dowell RC, Tomlin D, et al . (2002a) . The
auditory steady-state response . Part I: comparisons with
the auditory brainstem response . J Am Acad Audiol
13 :173-187 .
Cone-Wesson B, Parker J, Swiderski N, Rickards F.
(2002b). The auditory steady-state response. Part II : fullterm and premature neonates . J Am Acad Audiol (in
press) .
Cone-Wesson B, Rickards F, Poulis C, et al . (2002c). The
auditory steady-state response. Part III : clinical applications in infants and children . J Am Acad Audiol (in
press) .
Dauman R, Szyfter W Charlet de Sauvage R, Cazals Y
(1984) . Low frequency thresholds assessed with 40 Hz
MLR in adults with impaired hearing. Arch
Otorhinolaryngol 240 :85-89 .
Dirks DD . (1994) . Bone-conduction threshold testing. In :
Katz J, ed . Handbook of Clinical Audiology. Baltimore:
Williams and Wilkins, 132-146.
Dirks D, Swindeman JG . (1967) . The variability of
occluded and unoccluded bone-conduction thresholds . J
Speech Hear Res 10 :232-249 .
Dobie RA, Wilson MJ . (1994) . Phase weighting: a method
to improve objective detection of steady-state evoked
potentials . Hear Res 79 :94-98 .
Audiometry Using MASTER/Dimitrijevic et al
Dobie RA, Wilson MJ . (1998) . Low-level steady-state auditory evoked potentials : effects of rate and sedation on
detectability. J Acoust Soc Am 104:3482-3488 .
Don M, Eggermont JJ, Brackmann DE . (1979) .
Reconstruction of the audiogram using brain stem
responses and high-pass noise masking. Ann Otol Rhinol
Laryngol Suppl 57 :1-20.
Dunlap SA, Lenhardt ML, Clarke AM . (1988) . Human
skull vibratory patterns in audiometric and supersonic
ranges . Otolaryngol Head Neck Surg 99 :389-391 .
John MS, Dimitrijevic A, Picton TW. (2002) . Auditory
steady-state responses to exponential modulation
envelopes . Ear Hear (in press) .
John MS, Picton TW. (2000a). Human auditory steadystate responses to amplitude-modulated tones: phase and
latency measurements . Hear Res 141 :57-79 .
John MS, Picton TW. (2000b). MASTER: a Windows program for recording multiple auditory steady-state
responses . Comput Methods Programs Biomed
61 :125-150 .
Frank T. (1982) . Forehead versus mastoid threshold differences with a circular tipped vibrator. Ear Hear 3:91-92 .
Khalil TB, Viano DC, Smith DL . (1979) . Experimental
analysis of the vibrational characteristics of the human
skull. J Sound Vibration 63: 351-376.
Galambos R, Makeig S, Talmachoff PJ . (1981). A 40-Hz
auditory potential recorded from the human scalp . Proc
Natl Acad Sci U S A 78 :2643-2647 .
Khanna SM, Tonndorf J, Queller JE . (1976) . Mechanical
parameters of hearing by bone conduction . JAcoust Soc
Am 60 :139-154 .
Galambos R, Wilson MJ, Silva PD . (1994) . Identifying
hearing loss in the intensive care nursery: a 20-year summary. J Am Acad Audiol 5 :151-162 .
Linden RD, Campbell KB, Hamel G, Picton TW. (1985) .
Human auditory steady state evoked potentials during
sleep. Ear Hear 6:167-174 .
Goldstein BA, Newman CW. (1994) . Clinical masking: a
decision-making process. In : Katz J, ed . Handbook of
Clinical Audiology. Baltimore: Williams and Wilkins,
109-131.
Lins OG, Picton TW. (1995) . Auditory steady-state
responses to multiple simultaneous stimuli .
Electroencephalogr Clin Neurophysiol 96 :420-432 .
Goldstein R, Hayes C . (1965) . The occlusion effect in bone
conduction hearing . J Speech Hear Res 8 :137-148 .
HAkansson B, Brandt A, Carlsson P. (1994) . Resonance
frequencies of the human skull in vivo. JAcoust Soc Am
95 :1474-1481 .
HAkansson B, Carlsson P, Brandt A, Stenfelt S. (1996) .
Linearity of sound transmission through the human skull
in vivo . J Acoust Soc Am 99 :2239-2243 .
Hall JW Rupp KA. (1997) . Auditory brainstem response :
recent developments in recording and analysis . Adv
Otorhinolaryngol53 :21-45 .
Harrison WA, Norton SJ . (1999) . Characteristics of transient evoked otoacoustic emissions in normal-hearing
and hearing-impaired children. Ear Hear 20 :75-86 .
HerdmanAT, Stapells DR . (2001) . Thresholds determined
using the monotic and dichotic multiple auditory steadystate response technique in normal-hearing subjects .
Scand Audiol 30 :41-49 .
Jerger J, Chmiel R, Frost JD, Coker N. (1986) . Effect of
sleep on the auditory steady state evoked potential . Ear
Hear 7:240-245 .
Jerger J, Jerger S. (1965) . Critical evaluation of SAL
audiometry. J Speech Hear Res 8 :103-127 .
John MS, Lins OG, Boucher BL, Picton TW. (1998) .
Multiple auditory steady state responses (MASTER) :
stimulus and recording parameters . Audiology 37 :59-82 .
John MS, Dimitrijevic A, Picton TW. (2001a). Weighted
averaging of steady-state responses. Clin Neurophysiol
112:555-562 .
John MS, Dimitrijevic A, van Roon P, Picton TW (2001b).
Multiple auditory steady-state responses to AM and FM
stimuli. Audiol Neurootol 6:12-27 .
Lins OG, Picton PE, Picton TW, et al . (1995) . Auditory
steady-state responses to tones amplitude-modulated at
80-110 Hz . J Acoust Soc Ana 97 :3051-3063 .
Lins OG, Picton TW Boucher B, et al . (1996) . Frequencyspecific audiometry using steady-state responses. Ear
Hear 17 :81-96 .
Liitkenhoner B, Hoke M, Pantev C. (1985) . Possibilities
and limitations of weighted averaging. Biol Cybern
52 :409-416 .
Maurizi M, Almadori G, Paludetti G, et al . (1990) . 40-Hz
steady-state responses in newborns and in children .
Audiology 29 :322-328 .
Moore BCJ, Huss M, Vickers DA, et al. (2000) . Atest for
the diagnosis of dead regions in the cochlea. Br JAudiol
34 :205-224 .
Norton SJ, Gorga MP, Widen JE, et al . (2000) .
Identification of neonatal hearing impairment : evaluation of transient evoked otoacoustic emission, distortion
product otoacoustic emission, and auditory brain stem
response test performance. Ear Hear 21 :508-528 .
Oates P, Stapells DR . (1997) . Frequency specificity of the
human auditory brainstem and middle latency responses
to brief tones. 11 . Derived response analyses . J Acoust
Soc Am 102:3609-3619 .
Perez-Abalo MC, Savio G, Torres A, et al . (2001) . Steady
state responses to multiple amplitude-modulated tones :
an optimized method to test frequency-specific thresholds in hearing-impaired children and normal-hearing
subjects . Ear Hear 22 :200-211 .
Picton TW, Ouellette J, Hamel G, Smith AD . (1979) .
Brainstem evoked potentials to tonepips in notched noise.
J Otolaryngol 8:289-314 .
Picton TW, Durieux-Smith A, Champagne SC, et al .
(1998) . Objective evaluation of aided thresholds using
auditory steady-state responses. J Am Acad Audiol
9:315-331 .
223
Journal of the American Academy of Audiology/ Volume 13, Number 4, April 2002
Picton TW Dimitrijevic A, John MS, van Roon P. (2001) .
The use of phase in the detection of auditory steady-state
responses . Clin Neurophysiol 112:1692-1711 .
Plourde G, Picton TW (1990) . Human auditory steadystate response during general anesthesia . Anesth Analg
71 :460-468 .
Rance G, Rickards FW, Cohen LT, et al . (1995) . The automated prediction of hearing thresholds in sleeping subjects
using auditory steady-state evoked potentials . Ear Hear
16:499-507 .
Rance G, Dowell RC, Rickards FW et al . (1998) . Steadystate evoked potential and behavioral hearing thresholds
in a group of children with absent click-evoked auditory
brain stem response . Ear Hear 19 :48-61 .
Rickards FW Tan LE, Cohen LT, et al . (1994) . Auditory
steady-state evoked potential in newborns . Br JAudiol
28 :327-337 .
Savio G, Cardenas J, Perez-Abalo M, et al . (2001) . The
low and high frequency auditory steady state responses
mature at different rates. Audiol Neurootol 6:279-287 .
Sininger YS, Abdala C. (1996) . Hearing threshold as measured by auditory brain stem response in human neonates.
Ear Hear 17 :395-401 .
Sininger YS, Cone-Wesson B, Folsom RC, et al . (2000) .
Identification of neonatal hearing impairment : auditory
brain stem responses in the perinatal period . Ear Hear
21 :383-399.
Stapells DR, Galambos R, Costello JA, Makeig S . (1988) .
Inconsistency of auditory middle latency and steady-state
responses in infants . Electroencephalogr Clin
Neurophysiol 71 :289-295 .
Stapells DR, Picton TW, Durieux-Smith A. (1994) .
Electrophysiological measures of frequency-specific auditory function . In : Jacobson JT, ed . Principles and
Applications in Auditory Evoked Potentials . Boston: Allyn
and Bacon, 251-282.
Stevens J . (2001) . State of the art neonatal hearing screening with auditory brainstem response . Scand Audiol
Suppl 52:10-12 .
Sturzebecher E, Cebulla M, Pschirrer U. (2001) . Efficient
stimuli for recording of the amplitude modulation following response . Audiology 40 :63-68 .
Tonndorf J. (1972) . Bone conduction . In : Tobias J, ed.
Foundations of Modern Auditory Theory. Vol. II . New
York : Academic Press, 197-237 .
Vanniasegaram I, Bradley J, Bellman S. (1994) . Clinical
applications of transcranial bone conduction attenuation
in children . JLaryngol Otol 108:834-836 .
Viemeister NF. (1979) . Temporal modulation transfer
functions based upon modulation thresholds . J Acoust
Soc Am 66 :1364-1380 .
Wagner W Plinkert PK. (1999) . The relationship between
auditory threshold and evoked otoacoustic emissions.
Eur Arch Otorhinolaryngol 256:177-188 .
White KR, Behrens TR . (1993) . The Rhode Island Hearing
Assessment Project . Implications for universal newborn
hearing screening . Semin Hear 14 :1-119 .
Wilber LA, Kruger B, Killion MC . (1988) . Reference
thresholds for the ER-3A insert earphone . J Acoust Soc
Am 83 :669-676 .