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E
stimating hearing thresh-
olds using electrophysio-
logic measures in infants,
children, and difficult-to-test
patients is an especially chal-
lenging task. The ABR has been a good friend
for 30 years, but there are some limitations
to its prediction precision and the range of
hearing losses that it can predict.
The auditory steady-state response:
Variations of the MLR have been studied
in an attempt to find a procedure that is effec- A primer
tive in gathering more frequency-specific infor-
mation. You might recall terms such as the By Brad A. Stach
SSR, SSEP, and the 40-Hz ERP. Over the
years, researchers have continued to refine
these procedures, and new research with
what we now call the ASSR (auditory steady-
state response) is very encouraging. The cur-
rent application of this evoked potential,
elicited with modulated tones (modulations
1 What is the auditory steady-state response?

around 90 Hz), shows promise as a reliable The auditory steady-state response (ASSR) is an auditory evoked
predictor of hearing sensitivity. potential, elicited with modulated tones, that can be used to pre-
Back in the 1980s at Baylor College of dict hearing sensitivity in patients of all ages. The response itself
Medicine, a young doctoral candidate com- is an evoked neural potential that follows the envelope of a com-
pleted a dissertation titled: “Optimum Stim-
plex stimulus. It is evoked by the periodic modulation, or turn-
ulus Rate for Measurement of the Auditory
Steady-State Evoked Potential.” In general, ing on and off, of a tone.
the research supported the use of the 40-Hz Stach The neural response is a brain potential that closely follows the
ERP. Now a seasoned audiologist, Brad time course of the modulation. The response can be detected objec-
Stach, PhD, has stopped by Page Ten to tran- tively at intensity levels close to behavioral threshold. Emerging data suggest that the
sition us from the 40-Hz ERP of the ‘80s to
ASSR will yield a clinically acceptable, frequency-specific prediction of behavioral thresh-
today’s ASSR. As Brad says, “It looks like I
only missed it by about 50 Hz.” olds in patients, regardless of age, subject state, or degree of hearing loss.
Dr. Stach is the director of audiology and
clinical services, Central Institute for the Deaf,
and professor and director of the Audiology 2 Sounds perfect, but do we really need another auditory
evoked potential?
Graduate Program, Washington University,
Well, yes, it would be nice, and here’s why. The earliest averaged evoked potentials,
St. Louis. He is the author of the Compre-
hensive Dictionary of Audiology, is complet- described over 4 decades ago, are what we now refer to as the auditory middle-latency
ing the Encyclopedia of Audiology, and has and late-latency responses. The late responses, as you know, can be elicited with tonal
a best-selling textbook, Clinical Audiology. stimuli, permitting the electrophysiologic prediction of an audiogram. However, these
Brad was a founder of the American Acad- potentials are fatally confounded by subject state of consciousness, rendering them unac-
emy of Audiology, and currently is its presi-
ceptable for routine clinical use in anyone but awake, cooperating adults.
dent-elect. You regular Journal readers

3
probably recall his previous visits to Page But what about the ABR?
Ten, and his annual contributions to our Jour-
nal Club Review of the Best of Audiology Lit-
erature. Be patient. I was getting to that. The auditory brainstem response (ABR), discovered
As Brad points out in this excellent review
about 3 decades ago, currently stands as the gold standard for threshold prediction. Its
of the ASSR, we still have much to learn, and
some of the techniques need further refine- immunity to subject state makes it an excellent choice for predicting hearing in sleeping
ment. But, research to date strongly suggests infants or sedated children.
that the ASSR has the potential to be a valu- However, there are two important limitations to the ABR. First, it is best elicited using
able clinical procedure for the assessment of a click stimulus, which is not frequency-specific and generally only allows an estimate
hearing loss, and may even have applica-
over a broad range of higher frequencies. Tone-burst-elicited ABRs, albeit more frequency-
tions in the diagnosis of neurologic pathol-
ogy. Stay tuned for further developments in specific, can be difficult to record and observe at near-threshold levels, especially at lower
this exciting area. frequencies. So, ABR provides a good prediction of high-frequency hearing in a broad
sense and, often, an idea of the shape of the audiogram. Unfortunately, the precision
Gus Mueller across frequencies remains less than optimal.
Page Ten Editor
The second limitation of ABR is the range of hearing loss that can be estimated. As
a rule of thumb, if the high-frequency pure-tone average exceeds 70 dB, the ABR may
well be absent. Said another way, an ear with a 70-dB hearing loss will have the same
absent ABR as an ear with a loss of 80 dB, 90 dB, 100 dB, and so on. That is a rather
broad range of loss predicted by an absent ABR, especially if you are the one fitting a
hearing aid on that ear.
10 The Hearing Journal Page Ten September 2002 • Vol. 55 • No. 9
4 Okay, that’s convincing.
So, why is the ASSR better?
A steady-state evoked potential is an
on-going response and is elicited in
Fortunately, around this same time,
Field Rickards and his colleagues at the
First, the ASSR is elicited by a tone. That response to an on-going, periodically vary- University of Melbourne noted the abil-
tone is modulated; you might think of ing stimulus. The response is phase-locked ity to record this modulation-following
amplitude modulation as turning the tone to the modulation envelope. That is, the response at higher rates.7 They found that
on and off periodically and frequency mod- neural response closely follows the time ASSRs could be readily recorded and were
ulation as warbling it. Although the mod- course of the modulation. The phase rela- particularly useful at modulation rates of
ulation expands the spectrum of the tone, tion of the response to the modulation is greater than 60 Hz. Later, in the early
the frequency spread is narrower than a reasonably fixed or locked in time. 1990s, they found that at modulation
tone-burst or, especially, a click. So, the Galambos et al. noted in measuring rates of around 90 Hz, robust ASSRs
portion of the basilar membrane being the transient MLR that, when the stim- could be recorded from sleeping adults
stimulated is more restricted, and a more ulation rate was increased to a rate fast and infants.8-10 Researchers in Terry
precise audiogram can be predicted. enough to occur within the recording Picton’s lab at the University of Toronto
Second, if the modulation rates are epoch, responses could be overlapped. If were in hot pursuit as well.11 By the late
high enough, the ASSR seems unaffected the rate corresponded to the period of ‘90s, clinical applications of the higher-
by subject state. When the modulation the major peaks of the waveform, the rate ASSRs were being developed and
rate is greater than 60 times per second response would appear as a rather robust implemented.
(60 Hz), the response can still be recorded sinusoid. In adults, that occurred at rates
reliably in sleeping babies. near 40/s.
The so-called 40-Hz response, or 40- 8 So, you losers back in the
‘80s were just looking at

5 Could you step back for a


minute? Is this the 40-Hz
response, or the SSEP, that they
Hz event-related potential, was studied
fairly exhaustively over the ensuing sev-
the wrong modulation rate.
Please, don’t sugarcoat it. Actually, steady-
eral years. David Stappells and his col- state responses can be recorded over a
talked about in the 1980s?
leagues from Terry Picton’s lab2 and some range of modulation rates. Different mod-
Well, yes and no. It is sort of a variation of us in Jim Jerger’s lab at the Baylor Col-
ulation rates result in stimulation of dif-
on the theme. But first, let me clarify ter- lege of Medicine3 began looking at it dif-
ferent portions of the auditory nervous
minology and acronyms. Several terms ferently. Instead of doing conventional
system. It now appears that lower rates
have been used synonymously to describe signal averaging, we measured how brain
(<20 Hz) reflect activity of the genera-
this modulation-following response. They activity at the frequency corresponding
tors responsible for late-latency response,
are the amplitude-modulation-following to the click rate followed the envelope of
moderate rates (20 Hz-60 Hz) reflect
response (AMFR), envelope-following the interrupted transient signal. That is,
those responsible for the middle-latency
response (EFR), steady-state evoked we turned a click or tone-burst signal on
response, and higher rates (>60 Hz) reflect
potential (SSEP), steady-state response and off at a rate of say, 40/s, and analyzed
activity from the brainstem.12 It is no
(SSR), and the auditory steady-state the 40-Hz component of the brain activ-
response (ASSR). Perhaps the most pop- ity to see if it increased in amplitude wonder, then, that the lower modulation
ular has been the SSEP, but since that and/or phase-locked to the periodic rates are more vulnerable to subject state
acronym is also used for somatosensory change in the stimulus. So, viewed in that than the higher rates,13 just as middle
evoked potentials, ASSR is becoming the way, the 40-Hz response could be con- and late responses are.

9
more commonly used term. sidered an ASSR. The procedure worked Okay, I think I understand
well, and we learned much about the it theoretically, but how do
6 Thanks, but would you
please answer my ques-
tion?
nature of the 40-Hz response and mea-
surement techniques.4,5
you actually record it?
The stimulus is a pure tone. In clinical
What a crab! The 40-Hz response was first
described by Galambos and his colleagues
7 If the 40-Hz response was
so great, what happened?
applications, the frequencies of 500 Hz,
1000 Hz, 2000 Hz, and 4000 Hz are
in 1981.1 At that time, and still today, the Two things. First, we learned that the 40- commonly used. The pure tone is either
most common approach to electrophys- Hz response was strongly influenced by modulated in the amplitude domain or
iologic assessment was to measure tran- subject state. Amplitudes varied tremen- modulated in both the amplitude and fre-
sient evoked potentials. Transient dously from waking to sleeping states. The quency domains. Optimum modulation
responses are those that are elicited by fact that there was a consistent phase rela- strategies continue to be evaluated.14-16
rapid change in the auditory stimulus at tionship between the response and the Electrodes are placed on the scalp at loca-
rates that allow the response to be finished modulation across subject state was tions typically used for the recording of
before the next stimulus presentation. For encouraging.3 other auditory evoked potentials. Brain
a middle-latency response (MLR), for Second, it became readily apparent electrical activity is pre-amplified, filtered,
example, a signal is presented, the response that the 40-Hz response was not record- sampled, and then subjected to spectral
is recorded for 100 milliseconds or so, able, at least not in any useful way, in analysis. The frequency of interest in the
another signal is presented, the response infants or babies.6 So, we stopped pursu- brainwaves is that corresponding to the
is recorded again, and so on. ing the 40-Hz measure. modulation rate.
14 The Hearing Journal Page Ten September 2002 • Vol. 55 • No. 9
10 Huh? 101 Hz. The four brainwave frequencies
are analyzed independently to determine
signal. Objective detection is made easier
by these factors.
Let me explain. When a tone of any fre- the presence of a response at each audio- The Toronto group derives a response
quency is modulated periodically at a rate metric frequency. Just to make it more amplitude from a fast Fourier transform
of 90/s, the 90-Hz component of the brain efficient, they use the same approach in of the brainwaves.17 The outcome is sub-
electrical activity is measured; when mod- the other ear, with each frequency assigned jected to a variance ratio test, or F test,
ulation rate is 96/s, the 96-Hz compo- a slightly different modulation rate. In comparing the amplitude of the response
nent is measured, and so on. Measurement that way, both ears can be tested at all fre- at the modulation frequency to the ampli-
is of some aspect of amplitude or phase. quencies simultaneously. Analysis of the tude at some distant frequency. When the
Amplitude of the response and its vari- waveforms is made with fast Fourier trans- difference reaches a pre-determined sta-
ability are ways of detecting a response. form, and detection is accomplished with tistical criterion, a response is deemed to
Various strategies for objective determi- statistical F ratios. have occurred.
nation of significant signal-to-noise ratios The Melbourne group analyzes the
(SNR) are proving successful.
Another way of detecting a response is
12 Whew! After all that,
please tell me there are
clinical advantages to using the
variance, or coherence, of the phase rela-
tionship of the response to the modula-
by analyzing phase and its variability. As tion envelope.10 If the phase coherence
ASSR. For starters, can it pre-
an example, the concept of phase coher- reaches a pre-determined criterion, it is
dict threshold?
ence has proven to be useful. Imagine that assumed that the brain is responding to
a sinusoid is modulated periodically and Yes. Various studies have shown that it the stimulus because the response is phase-
that the brain wave of the frequency cor- can provide a reasonably accurate predic- locked to it.
responding to that modulation rate is fol- tion of behavioral thresholds.8,10,11,18-20 Refinements in these techniques, as
lowing right along. The lag between the It appears to be comparable in accuracy well as new techniques, will likely emerge.
modulating signal and the response, if in to the ABR.12 Interestingly, some of the The point is that it is the periodic nature
fact the brain is following the signal, should earlier work showed it to be a strong pre- of the response that makes it so suscepti-
be fairly constant. This lag can be mea- dictor of thresholds in patients with hear- ble to objective detection.
sured as the phase angle. ing loss, but a less than adequate predictor
The variability of the lag over succes-
sive samples represents the coherence of
of normal hearing.20 That is probably an
SNR issue that will be solved with tech-
16 Does the test take a long
time?
the phase relationship. A robust following nologic advancements. Accurate threshold detection across audio-
response to the modulating tone will have metric frequencies in both ears can take
a fairly consistent or coherent phase rela-
tionship. If the brain is not responding to
13 Can the ASSR be recorded
in infants?
a while—probably somewhere between
30 and 60 minutes. The speed of this
the sound, then the phase relationship to Yes, it can. The response is present and approach seems acceptable and is likely
the modulation will be random. A crite- readily measurable in newborns,21 sleep- to improve as the technology advances.
rion level for significant phase coherence ing infants,20 and sedated babies. The Toronto approach provides a cre-
is then used to determine objectively ative example of the potential for this tech-
whether or not a response occurs.
14 Is it frequency-specific?
nology. If each of eight frequencies (four
per ear) is assigned a different modula-
11 Does everyone measure
it the same way?
As I stated before, the stimulus is a tone
that is only slightly distorted by modula-
tion rate, ASSRs can be measured simul-
taneously at all frequencies in both ears
That would be too simple. I’ll give you tion. It stimulates a portion of the basilar at a single intensity level.17,22 The devel-
two examples. The strategy derived from membrane that is restricted enough to opment of automated algorithms to
the Melbourne group uses a modulation provide very acceptable frequency reso- enhance the efficiency of the threshold
frequency of 90 Hz.10 Amplitude mod- lution. Not unexpectedly, I suppose, prediction process seems inevitable in the
ulation depth is 100%; frequency mod- threshold prediction appears to be more near future.
ulation depth is 10%. Automatic accurate for higher-frequency signals than
determination of a response is based on
phase coherence. One audiometric fre-
for lower-frequency signals.10,17 Never-
theless, the ASSR approach should enjoy
17 You said something ear-
lier about dynamic
range. Could you go over that
quency is tested at a time. an advantage over tone-burst ABR pre-
again?
The Toronto group takes a different diction of lower-frequency hearing. The
approach.17 They use a stimulus that is a outcome should be a more precise pre- Sure. Gary Rance and his colleagues from
combination of four carrier frequencies diction of the audiogram. Melbourne taught us this.23 Remember
of 500 Hz, 1000 Hz, 2000 Hz, and 4000 that modulated tones are being used to
Hz, each of which is modulated at a
slightly different frequency. For example,
15 And you say it can be
objectively detected?
elicit the ASSR. Maximum signal inten-
sity of modulated tones is comparable to
the 500-Hz tone is modulated at 77 Hz, Remember, the response itself is periodic equipment limits for pure tones on mod-
the 1000-Hz tone at 85 Hz, the 2000-Hz in nature and, when present, is at least ern clinical audiometers. This can be as
tone at 93 Hz, and the 4000-Hz tone at somewhat phase-locked to the eliciting high as 120 dB HL.
September 2002 • Vol. 55 • No. 9 Page Ten The Hearing Journal 17
REFERENCES
By comparison, air-conducted clicks dicting hearing loss, the emerging tech- 1. Galambos R, Makeig S, Talmachoff PJ: A 40-Hz audi-
used to elicit ABRs typically have a maxi- niques need refinement. Prediction of nor- tory potential recorded from the human scalp. Proc Nat
mum output of around 90 dB nHL. This mal hearing thresholds and of low- Acad Sci 1981;78:2643-2647.
2. Stapells DR, Linden D, Suffield JB, et al.: Human audi-
is adequate for predicting hearing thresh- frequency thresholds has room for tory steady state potentials. Ear Hear 1984;5:105-113.
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1986;7:240-244.
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frequency hearing loss greater than 70 dB. state response threshold prediction using phase coher-
In those patients, threshold simply cannot
be estimated with ABR. Thus, infants and
20 You’ve talked all about
threshold prediction.
Are there diagnostic applica-
5.
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Picton TW, Vajsra J, Rodriquez R, Campbell KB: Reli-
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extra 50 dB worth of information about thy).23 How sensitive they might be to 1984:163-168.
8. Cohen LT, Rickards FW, Clark GM: A comparison of
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determining early candidacy for amplifi- unknown. awake and sleeping humans. J Acoust Soc Am
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9. Rickards FW, Tan LE, Cohen LT, et al.: Auditory steady-
recently on the correlation of the ASSR
18 Does the ASSR have its state evoked potentials in newborns. Br J Audiol
to speech perception.14 Results suggest 1994;28:327-337.
own CPT code yet?
that steady-state response recordings to 10. Rance G, Rickards FW, Cohen LT, et al.: The auto-
mated prediction of hearing thresholds in sleeping sub-
Um, no, it’s a little early for that. multiple independent amplitude and fre- jects using auditory steady-state potentials. Ear Hear
quency modulations of a pure tone may 1995;16:499-507.

19 Why don’t more people


use the ASSR?
provide an objective assessment of
suprathreshold hearing. We obviously
11. Lins OG, Picton TW, Boucher BL, et al.: Frequency-
specific audiometry using steady-state responses. Ear
Hear 1996;17:81-96.
For all the potential of the ASSR in pre- have much more to learn. 12. Cone-Wesson B, Dowell RC, Tomlin D, et al.: The
auditory steady-state response: Comparisons with the
auditory brainstem response. JAAA 2002;13:173-187.
13. Pethe J, von Specht H, Muhler R, Hocke T: Amplitude
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humans—a comparison for 40 Hz and 80 Hz modu-
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14. Dimitrijevic A, John MS, van Roon P, Picton TW:
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Ear Hear 2001;22:100-111.
15. John MS, Dimitrijevic A, Picton TW: Auditory steady-
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16. John MS, Dimitrijevic A, van Roon P, Picton TW: Mul-
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17. Dimitrijevic A, John MS, Van Roon P, et al.: Estimat-
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18. Herdman AT, Stapells DR: Thresholds determined using
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response technique in normal hearing subjects. Scand
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19. Vander Werff KR, Brown CJ, Gienapp BA, Schmidt
Clay KM: Comparison of auditory steady-state response
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22. John MS, Purcell DW, Dimitrijevic A, Picton TW:
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23. Rance G, Dowell RC, Rickards FW, et al.: Steady-state
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18 The Hearing Journal Page Ten September 2002 • Vol. 55 • No. 9

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