Objective Evaluation of Aided Thresholds Using Auditory Steady

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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
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
C
*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
ofABR 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
316
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
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.
METHOD
Subjects
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
500
80 .9
1000
88 .9
2000
96 .9
aooo
loan
Time
Frequency
~_ ., ~ .,go,-~
L
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.
318
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 1000and 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
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
500 w
0
754 msec
Frequency
] 50 nV
340 Hz
Polar Plots
] 50 nv
80.9
88 .9
96 .9
104 .8 Hz
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 .
320
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 10dB 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
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.
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.
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
RESULTS
Nofmal Subjects
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
Behavioral Threshold =
Intercept + Slope (Physiologic Threshold) .
Correlations and regressions were performed
separately for each of the four carrier-frequenTable 1
Results in Normal Subjects
Carrier Frequency (Hz)
500
Threshold
Earphone multiple stimuli
Earphone single stimulus
Soundfield speaker multiple stimuli
P
B
1000
D
37
(10)
31
(8)
10
(6)
21
(9)
P
32
(15)
34
(10)
36
(15)
B
2000
D
P
B
4000
D
30
(7)
10
(4)
26
28
(13) (15)
10
(8)
18
(13)
P
30
(7)
33
(12)
26
(11)
B
6
(8)
D
20
(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
500
1 kHz
Stimulus
Frequencies
(kHz)
2 kHz 4 kHz
y
Intensity
(dB SPL)
Spectrum
(60-120 Hz)
" y
500
1 kHz
2 kHz 4 kHz
yy
0.5, 1, 2, 4
40
0.5, 1,2,4
50
0.5, 1,2,4
30
0.5, 1, 2, 4
40
0.5, 1, 2, 4
20
0.5, 1, 2, 4
30
y
so nv ]
0.5, 1,2,4
Subject N3
Left Ear
10
0.5, 1, 2, 4
Physiologic
Behavioral
30
10
30
5
10
5
30
5
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 reli322
Subject A23
Right Ear
20
.~
Physiologic
Behavioral
~ ~ .f- +,
(~_
40
30
0
(440
30
00 ~v]
0 +
30
30
40
30
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
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
Difference (SD)
17(8)
13(8)
14(8)
17(13)
After correction
Difference (SD)
Regression SE
Slope
Intercept
Correlation
17(8)
8
0 .68
-1
0 .69
13(7)
5
0 .54
9
0 .75
13(7)
5
0 .63
4
0 .81
16(9)
7
0 .60
4
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.
Stimulus
Intensity
Frequencies (dB SPL)
(kHz)
Stimulus
Intensity
Frequencies (dB SPL)
(kHz)
Spectrum
(60-120 Hz)
500
1 kHz
2 kHz 4 kHz
Subjects in Whom Behavioral
Responses Were Not Available
The recordings obtained in the two aided
infants showed recognizable responses. Subject
0.5,1,2,4
50
0.5, 1,2,4
60
0.5, 1,2,4
40
0.5, 1, 2, 4
50
0.5, 1, 2, 4
30
2, 4
70
0.5, 1, 2, 4
40
4
80
Spectrum
(60-120 Hz)
y
500
1 kHz
2 kHz 4 kHz
~ 4~- i~ -,;~
y
+
+
-I
+
y
Subject A25
Left Ear
Physiologic
Behavioral
20
25
30
25
20
15
40'
25
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 .
Subject A3
Right Ear
+
+
b
I
Physiologic
Behavioral
50
35
50
30
70`
60
80`
65
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
500 Hz
Stimulus
Intensity
Frequencies (dB SPL)
(kHz)
1000 Hz
90
0.5, 1, 2, 4
70
(unaided)
0.5, 1, 2, 4
70
4000 Hz
2000 Hz
ro
a" .
O
.;
Co
0 .5, 1, 2, 4
60
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
Intensity
Stimulus
Frequencies (dB SPL)
(kHz)
60
(unaided)
Spectrum
(60-120 Hz)
"4.* .
yy
0.5 , 1 , 2,4
60
0.5, 1, 2, 4
50
0 .5, 1, 2, 4
50
MMW
1 kHz
500
U
0
Subject X1
Right Ear
Y
O
40
Physiologic
Behavioral
+0+ (1) +
?
?
50
?
50
?
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.
324
2 kHz 4 kHz
't'
+
I
I
+
+
+
+
~
+
+
60
?
50
?
?
?
70
?
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
Intensity
Frequencies (dB SPL)
(kHz)
2 kHz 4 kHz
'Y
Physiologic
Behavioral
0.5, 1, 2, 4
70
0.5 , 1, 2 , 4
60
0.5, 1, 2, 4
50
Spectrum
(60-120 Hz)
1 kHz
++
0. 5 , 1 , 2, 4
Subject A29
Left Ear
500
+
50 w]
0 .5 , 1 , 2 , 4
1 kHz
++
zoo w]
Subject X3
Right Ear
O
Ga
0.5, 1,2,4
500
y
0
0
Spectrum
(60-120 Hz)
Physiologic
Behavioral
2 kHz 4 kHz
+
+
+
6-
++++
?
40
?
25
30
5u nv ]
20
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.
Objective Evaluation of Aided Thresholds/Picton et al
Behavioral Audiometry
Left
Right
250
0
20
1000
4000
250
0 L-a--i
20
M
40
C
40
1000
l
O
4000
l
Figure 11
C
60
60
80
O
100
80
U
3
100
120
W
120
SRT
WRS
45 dB
56% at 80 dB
SRT
WRS
7l
35 dB
72% at 80 dB
Auditory Brainstem Responses
Right
Left
90 dB nHL
Clicks
Rarefaction
Condensation
r
0
.
.
.
.
.
.
.
.
a
10
Combined
O .S [IV
f
0
.
.
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-
Possible auditory neu-
ropathy? This figure represents the
audiogram and auditory brainstem
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
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 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.
~
rr ~ 3 0 msec
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 signif326
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
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 ofthe 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 .
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
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
100
Normal
a
m
L
0
100
Pathological
a
m
b
0
100
T,
000
r,V
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
328
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
Objective Evaluation of Aided Thresholds/Picton et al
behavioral thresholds at low intensity and come
closer to the behavioral thresholds at high intensity, perhaps on the basis of recruitment . Our
findings show an opposite effect . The discrepancy
is not related to the problems estimating highfrequency thresholds with multiple stimuli,
since the single-stimulus thresholds were used
in the final regressions. One possible explanation is that when the behavioral thresholds are
still significantly elevated, despite amplification, the sounds at these frequencies may be
processed through areas of the cochlea that are
not place specific for those frequencies. This
mechanism might not lead to well-synchronized
steady-state responses and the physiologic
thresholds may then be significantly elevated relative to the behavioral thresholds .
Subjects without Responses
We were unable to record steady-state
responses in one of our hearing-impaired subjects despite presenting sounds at intensities
significantly above the behavioral thresholds
(see Fig. 10) . Further investigations of this subject (see Fig. 11) suggested that she might have
a disorder akin to what has been termed "auditory neuropathy" (Berlin et al, 1998 ; Starr et al,
1996). This disorder is characterized by absent
or severely abnormal ABRs in the presence of
preserved function in the external hair cells as
demonstrated by normal OAEs or cochlear microphonics . Clinically, the patients have worse
speech discrimination than their audiometric
thresholds for pure tones would predict, show little benefit from hearing aids, and may have evidence for a more generalized neuropathy. Stein
et al (1996) have found this disorder in neonates
with hyperbilirubinemia . Deltenre et al (1998)
have shown that the OAEs in these patients
may decrease over time . Our patient may therefore have such a disorder even though the OAEs
were not clearly recognizable . The early waves
in the response almost certainly represent
cochlear microphonics (Berlin et al, 1998). Rance
et al (1998) studied three children with no ABRs
but present cochlear microphonics (in a series of
108 hearing-impaired children with absent
ABRs). The thresholds for the auditory steadystate responses in these children were between
50 and 80 dB higher than behavioral thresholds .
We are not sure what the residual wave at about
4 msec in the combined response represents . It
might be caused by some nonlinearity in the
cochlear microphonic, some residual, poorly synchronized auditory nerve response (cf Berlin et
al, 1998, Fig. 13) or some response of the vestibular system to the loud click (Mason et al, 1996).
This patient illustrates the general principle
that one may not be able to use the evoked
potentials to assess hearing when the neurophysiologic mechanisms for generating the
evoked potentials are compromised.
Subjects Requiring Objective'
Assessment of Aided Thresholds
The experiments reported iri this paper
address the possibility of using evoked potentials
to assess aided hearing thresholds in subjects
who cannot provide reliable behavioral thresholds . The steady-state responses are clearly not
needed in the group of 35 hearing-impaired children that we studied since behavioral testing is
faster and more accurate . However, many subjects with hearing impairment cannot provide
reliable results on behavioral testing. Fitting
hearing aids in these patients is a matter of
luck and intuition. An objective assessment of
aided thresholds would allow us to determine
how well the patient responds to sounds using
hearing aids and to adjust the hearing aid to optimize the response . The Joint Committee on
Infant Hearing (1994) recommended that all
hearing-impaired infants be identified and treatment initiated by the age of 6 months . Meeting
this goal requires methods to evaluate aided
performance in the treated infants. In order to
determine whether the auditory steady-state
responses can be used in this context, we evaluated the technique in two infants being fitted
with hearing aids . Our initial results show that
steady-state responses can be clearly recorded
in these patients when hearing aids are used .
Much still needs to be done . We will have to
develop ways of testing these children that will
reduce the electrical noise levels in the recording. Although patients do not have to provide
behavioral responses to the stimuli in an objective test (Dobie, 1993), they do have to remain
sufficiently quiet to allow a reasonable recording. We also evaluated the technique in one
child with severe developmental delay. The aided
responses recorded in this child were the first
clear responses to sound ever seen in the patient.
Follow-up studies will be needed to see how
accurately we assessed the aided thresholds in
all three of these children . We admit to cautious optimism .
Acknowledgments. This research was funded by the
Research Institute of the Children's Hospital of Eastern
329
Journal of the American Academy of Audiology/Volume 9, Number 5, October 1998
Ontario, the Medical Research Council of Canada, and
the Faculty of Health Sciences at the University of
Ottawa . The authors would also like to thank James
Knowles, Paul Madsen, and the Baycrest Foundation
for additional support . Patricia Van Roon helped with the
manuscript.
Some of the data included in this paper were presented
at the XV meeting of the International Evoked Response
Audiometry Study Group in Memphis, TN, June 8-12,
1997 .
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