Development of Low-Frequency Tone Burst versus the Click

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J Am Acad Audiol 16:114–121 (2005)
Development of Low-Frequency Tone Burst
versus the Click Auditory Brainstem
Response
Raymond M. Hurley*
Annette Hurley†
Charles I. Berlin‡
Abstract
Often ABR threshold testing employs clicks to assess high-frequency hearing,
and low-frequency tone bursts to assess low-frequency sensitivity. While a
maturation effect has been shown for click stimuli, similar data are lacking for
low-frequency toneburst stimuli. Thus, 305 infants ranging in conceptional age
(CA) from 33 weeks to 74 weeks were tested. Absolute latencies were
measured for wave V at 55, 35, and 25 dB nHL in response to a click and for
wave V500 in response to a 500 Hz tone burst. Major wave latency in response
to 500 Hz tone bursts decreases with age and do not stabilize by 70 weeks
CA. Likewise, waves III and V latencies in response to clicks decrease with
age, as has been reported by others, and do not stabilize by 70 weeks CA.
Wave I latency produced by clicks did not decrease with age, being mature
by 33 weeks CA.
Key Words: Auditory brainstem response, auditory development, click, tone
bursts
Abbreviations: ABR = Auditory brainstem response; CA = conceptional age
Sumario
A menudo, la evaluación de umbrales de ABR emplea clicks para estimar la
audición en altas frecuencias y bursts tonales de baja frecuencia para la
sensibilidad en las bajas frecuencias. En tanto que se ha mostrado un efecto
de maduración para los estímulos de tipo click, se carece de datos similares
para los estímulos de tipo burst tonal de baja frecuencia. Así, se evaluó a 305
infantes con edad de concepción (CA) de 33 a 74 semanas. Se midieron las
latencias absolutas para la onda V a 55, 35 y 25 dB nHL en respuesta a un
click, y para la onda V500 en respuesta a un burst tonal de 500 Hz. La latencia
de las ondas principales en respuesta a los bursts tonales de 500 Hz disminuyó
con la edad y no se estabiliza antes de la semana 70 de CA. Asimismo, las
latencias de las ondas III y V en respuesta a clicks disminuyen con la edad,
como ha sido reportado por otros, y no se estabiliza antes de la semana 70.
La latencia de la onda I producida por clicks no disminuye con la edad,
alcanzando la madurez a la semana 33 de CA.
Palabras Clave: Respuesta auditiva del tallo cerebral, desarrollo auditivo, click,
bursts tonales
Abreviaturas: ABR = respuesta auditiva de tallo cerebral, CA = edad de
concepción
*Department of Communication Sciences and Disorders, University of South Florida; †Department of Communication
Disorders, Louisiana State University Health Sciences Center; ‡Kresge Hearing Research Laboratory, Department of
Otorhinolaryngology and Biocommunication, Louisiana State University Health Sciences Center
Raymond M. Hurley, Ph.D., Department of Communication Sciences and Disorders, University of South Florida,
4202 East Fowler Avenue—PCD 1017, Tampa, FL 33620-8150; Phone: 813-974-9784; Fax: 813-974-0822;
E-mail: rhurley@chuma1.cas.usf.edu
114
Development of ABR/Hurley et al
A
uditory brainstem response (ABR)
testing has been widely used to assess
peripheral auditory sensitivity and
synchrony in neonates and infants. Often
ABR testing employs clicks to assess highfrequency hearing (2000–4000 Hz), and lowfrequency tone bursts (500 Hz) to assess lowfrequency hearing (Hood, 1998; Goldstein
and Aldrich, 1999; Sininger and Cone-Wesson,
2002). A click-produced ABR does not just
represent hearing in the 2000–4000 Hz zone
of the cochlea but is an excellent (r = .98)
predictor of average hearing loss (Sininger
and Abdala, 1996). Further, a click ABR
corresponds best to the zone of hearing above
500 Hz (Sininger and Cone-Wesson, 2002);
however, the contour of a hearing loss cannot
be ascertained by a click-produced ABR alone.
To estimate low-frequency sensitivity and
hearing loss contour, a low-frequency test
paradigm must be utilized. Common
paradigms to access more frequency-specific
hearing include the derived band procedure
(Ponton et al, 1992), tone bursts with a
Blackman windowing function (Gorga et al,
1987; Gorga et al, 1988; Gorga et al, 1989),
and tone burst in notched noise (Stapells et
al, 1995; Sininger et al, 1997). The derived
band procedure provides excellent frequency
specificity but is time-consuming and can
lack response clarity; thus, it has fallen out
of favor, being replaced by the use of tone
bursts. While some investigators recommend
the use of tone bursts tapered by a Blackman
gating function (Gorga et al, 1988; Gorga
and Thornton, 1989; Hurley et al, 1996),
others favor tone bursts in notched noise for
improved frequency specificity (Picton et al,
1979; Purdy et al, 1989; Stapells et al, 1990;
Stapells et al, 1995). Like a click-produced
ABR, a toneburst ABR is an excellent (r =
.94–.97) predictor of hearing at the nominal
toneburst frequencies in neonates and infants
(Stapells et al, 1995; Sininger et al, 1997).
Numerous reports have shown a
maturation effect of the ABR from birth to
approximately two years of age when using
click stimuli (Hecox and Galambos, 1974;
Mokotoff et al, 1977; Cox et al, 1981; Salamy,
1984; Rotteveel et al, 1986; Gorga et al, 1987;
Gorga et al, 1989; Ponton et al, 1992).
However, similar data are lacking for lowfrequency stimuli, that is, 500 Hz. Further,
there are conflicting data concerning
frequency specific development with one data
set (Ponton et al, 1992; Sininger et al, 1997),
suggesting that low-frequency sensitivity
development occurs more slowly than
midfrequency sensitivity development, while
other data sets (Teas et al, 1982; Folsom and
Wynne, 1986) suggest that frequency
development occurs more rapidly for lower
than for higher frequency stimulation.
Age-equivalent ABR norms are important
when predicting hearing levels in neonates
and infants. Moreover, because the ABR is a
test of neurosynchrony, delayed absolute
latencies can often indicate other pathologies
or unique conditions (Murray, 1988; Sininger
et al, 1995; Starr et al, 1996; Berlin et al,
1998). Therefore, it is useful to have ageequivalent norms for low-frequency toneburst
stimuli. In the present paper, we provide
age-equivalent norms for a 500 Hz toneburst
evoked ABR obtained from a large group of
children ranging in conceptional age from
33 weeks to 74 weeks and compare these
toneburst norms to age-equivalent norms for
click-evoked ABR. In addition, we investigate
further the issue of low-frequency sensitivity
development.
METHODS
Subjects
Three hundred five infants ranging in
conceptional age (CA) from 33 weeks to 74
weeks were referred for ABR testing as they
had met with one or more high risk factors
for hearing loss. CA was determined by
adding the gestational age (GA) and the
elapsed time from birth to ABR testing. GA
was based on neuromuscular and physical
maturity (Dubowitz et al, 1970; Ballard et al,
1977). Because of the previously reported
lack of independent latency values between
ears (Gorga et al, 1987), correlation analyses
were carried on four ABR parameters and are
displayed in Table 1. While these correlation
values are not as high and consistent as
previously reported (Gorga et al, 1987), they
do demonstrate the lack of ear independence
and support using the latency value obtained
from only one ear. Thus, only the latency
data from the right ear were used for
analyses. All infants had ABR responses at
25 dB nHL to clicks. The infants were divided
into 11 CA groups as outlined in Table 2. For
comparison purposes, ABR data were
obtained from 20 subjects, 22–30 years of
115
Journal of the American Academy of Audiology/Volume 16, Number 2, 2005
Table 1. Latency Correlation Values between the Right and Left Ears at 55 dB nHL
ABR Parameter
Correlation
Wave I Latency
0.65
Wave III Latency
0.76
Wave V Latency
0.86
Wave V500
0.76
age, with HTLs ≤10 dB for the octave
frequencies of 250–8000 Hz.
Procedures
The infants were tested in a sedated
stable physiological state just prior to hospital
discharge and were medically cleared of
middle ear disease. Testing was performed in
a quiet test room using Nicolet Pathfinder II
and Spirit evoked potential systems. The
stimuli were 75, 55, 35, and 25 dB nHL (re:
30 dB peak equivalent SPL) condensation
100 µsec clicks at a rate of 27.7/sec with the
filter band pass at 100–3000 Hz and the time
base at 12–15 msec. For the 500 Hz toneburst
testing, the band pass was 30–1500 Hz with
a 15 msec time base. The stimuli were 75, 55,
45, and 35 dB nHL alternating 500 Hz bursts
having a "2-0-2" cycle envelope using a
Blackman gating function at a rate of 27.7/sec.
All ABRs were two-channel recordings from
Cz-A2 and Cz-A1. Each ABR was replicated
and the result of 1500 stimulus presentation.
Testing 20 young adults with normal
hearing (thresholds for 500–8000 Hz were ≤10
dB HL) indicated that the average and modal
psychophysical threshold for the 500 Hz ABR
stimuli was 25 dB HL, which is consistent
with other reported psychophysical thresholds
at 500 Hz for similar toneburst durations
(Beattie and Boyd, 1985; Purdy et al, 1989).
The reason that toneburst ABR threshold
estimates do not often match psychophysical
thresholds as depicted on the audiogram,
particularly at 500 Hz, is related to stimulus
duration. Data collected with standard
audiometric procedures use relatively long
duration stimuli compared to the short
duration stimuli used to obtain ABRs. Signal
duration needs to be approximately 200 msec
for the lowest hearing thresholds as stimulus
duration interacts with threshold because of
temporal integration. The default dB nHL
reference values provided by the
manufacturer were obtained using a stimulus
envelope different than the optimal one for
toneburst ABR testing. For example, Nicolet’s
dB nHL values were obtained using stimuli
with a 5-10-5 cycle envelope, which for 500
Hz means a stimulus duration of 40 msec. In
contrast, our 500 Hz toneburst stimuli had
a 4 msec rise/fall and a zero plateau for a total
duration of 8 msec. Thus, temporal
integration factors account for the elevation
in tone psychophysical threshold; however,
stimulus presentation rate does not appear
to significantly alter psychophysical threshold
Table 2. Breakdown of Infant Groups by Conceptional Age and
Number of Infants in Each Group
116
Conceptional Age
Number in Group
33–36 wks
27
37–38 wks
27
39–40 wks
27
41–42 wks
44
43–44 wks
32
45–47 wks
26
48–50 wks
25
51–55 wks
24
56–60 wks
25
61–65 wks
24
66–74 wks
24
Development of ABR/Hurley et al
a
b
Figure 1. (a) Comparison of our present click stimulus wave V latency data to previously published data for
33–40 weeks conceptional age (Gorga et al, 1987, 1989). (b) Comparison of present click stimulus wave V latency
data to previously published data for 41–65 weeks conceptional age (Gorga et al, 1987, 1989).
if the rate is kept between 10/sec and 40/sec
(Stapells et al, 1985; Purdy et al, 1989). If the
default dB nHL values were adjusted to the
psychophysical threshold for our shorter
duration tone burst, 75, 55, and 45 dB nHL
would be 55, 35, and 25 dB nHL, respectively.
In order to remain consistent with the click
reference values, we will use the adjusted
dB HL values throughout this paper.
RESULTS
I
n order to insure that our data were
consistent with previously published data,
we compared our click stimulus wave V
latency data to previously published data
(Gorga et al, 1987, 1989). These graphic
comparisons are displayed in Figure 1. In
reviewing this figure, note that for all age
groups our wave V latency data falls well
within the mean (±2 SDs) of the previous
data (Gorga et al, 1987, 1989). Thus, we feel
confident that our data were obtained from
a representative sample of neonates.
Absolute latencies were measured for
waves I, III, and V at 75 and 55 dB nHL and
for wave V at 35 and 25 dB nHL in response
to a click, and for wave V at 55, 35, and 25
dB nHL in response to a 500 Hz tone burst.
The mean latency data were analyzed by CA
group for significant changes using an
analysis of variance (ANOVA) with the post
117
Journal of the American Academy of Audiology/Volume 16, Number 2, 2005
Table 3. Mean (SD) Latency Values by Conceptional Age (CA)
for Click and 500 Hz Toneburst Stimuli
CA
Click 75 dB
Click 55 dB
Click 35 dB
Click 25 dB
.5k 55 dB
.5k 35 dB
.5k 25 dB
35
7.33 (0.41)
7.96 (0.47)
8.78 (0.15)
9.50 (0.70)
9.35 (0.73)
10.91 (0.82)
14.42 (0.48)
37
7.29 (0.46)
7.81 (0.46)
8.62 (0.47)
9.35 (0.60)
9.60 (0.53)
11.47 (0.84)
13.83 (0.70)
39
7.05 (0.40)
7.56 (0.38)
8.43 (0.64)
9.08 (0.61)
9.37 (0.75)
11.26 (0.61)
13.03 (0.47)
41
6.94 (0.35)
7.56 (0.39)
8.29 (0.40)
8.98 (0.54)
9.27 (0.61)
10.85 (0.92)
13.11 (1.33)
43
6.90 (0.38)
7.41 (0.40)
8.22 (0.46)
8.84 (0.58)
9.21 (0.71)
10.90 (0.84)
12.85 (0.96)
45
6.90 (0.38)
7.48 (0.38)
8.32 (0.42)
9.02 (0.52)
9.35 (0.52)
11.28 (0.86)
14.11 (0.74)
48
6.70 (0.31)
7.16 (0.41)
8.03 (0.57)
8.58 (0.65)
8.95 (0.71)
10.82 (1.06)
14.03 (1.19)
51
6.64 (0.46)
7.20 (0.48)
7.87 (0.64)
8.47 (0.76)
8.82 (0.70)
10.42 (0.99)
13.14 (0.57)
56
6.40 (0.36)
7.00 (0.31)
7.71 (0.44)
8.36 (0.50)
8.64 (0.45)
10.33 (0.74)
13.83 (1.09)
61
6.44 (0.41)
7.00 (0.42)
7.77 (0.50)
8.41 (0.72)
8.70 (0.52)
10.60 (0.98)
13.04 (1.42)
70
6.23 (0.33)
6.97 (0.38)
7.89 (0.40)
8.60 (0.48)
8.61 (0.50)
10.55 (0.73)
13.00 (0.98)
hoc analyses utilizing the Scheffé procedure
and the alpha level set at <0.01. Table 3 lists
the means (±1 SDs) of wave V data by
conceptional age for the click and 500 Hz
toneburst stimuli. To determine if the latency
values were normally distributed for each
CA group at 55 dB nHL, the data were
analyzed using the Kolmogorov-Smirnov
Figure 2. Mean (±1 SD) latency of waves I, III, and
V for a click, and wave V500 for a 500 Hz tone burst
at 55 dB nHL.
118
statistic. The results of these analyses were
not significant (p = > 0.50), indicating that the
distributions for each CA were not different
from normal.
The latency values of waves I, III, and V
at 55 dB nHL are displayed in Figure 2. Note
the significant (F = 18.86, p < 0.0001) decrease
in wave V latency until after 70 weeks CA.
Further note the significant (F = 3.98, p <
0.01) decrease in wave III latency until 70
weeks CA. Wave I latency did not significantly
(F = 0.98, p > 0.05) change across all the age
groups. Thus, waves III and V do not reach
maturity until after 70 weeks CA while wave
I is mature by 36 weeks CA. Additionally,
Figure 2 displays the latency values for the
500 Hz toneburst stimuli at 55 dB nHL. Wave
V latency for the 500 Hz tone burst
significantly (F = 6.83, p < 0.0001) decreases
until 61 weeks CA.
Figure 3 shows the individual latency
values for waves I, III, and V, and 500 Hz for
wave V plotted as a function of CA. Linear
regression analyses indicated the r2 values to
be 0.06, 0.22, and 0.38, respectively, for waves
I, III, and V, produced by a click, and 0.28 for
wave V produced by the 500 Hz tone burst.
Since wave I latency did not significantly
change across the CA groups, the low r2 value
is not unexpected. However, the remaining r2
values indicate that CA is not heavily
accountable for the recorded variance in
latency values across CAs for waves III and
V and the 500 Hz tone burst. Figure 4
Development of ABR/Hurley et al
Figure 3. Scattergrams of the latency values for
waves I, III, and V at 55 dB nHL and the latency values for wave V500 at 55 dB nHL.
Figure 4. The best-fit functions from Figure 3 replotted on log-linear coordinates.
displays the best-fit functions from Figure 3
replotted on log-linear coordinates. The slopes
of these lines indicate that the rate of
maturation of wave V for both click and 500
Hz tone burst is the same while wave III
maturation proceeds at a different rate.
Again, the flatness of the wave I log-linear
best-fit line is consistent with a
nonmaturation cochlear development.
In order to determine whether intensity
affects the developmental sequence, the wave
V latency/intensity functions produced by
click stimuli for the CA groups were analyzed
at lower intensity levels. These data are
displayed in Figure 5. While the
characteristics of these latency/intensity
functions follow the predicted developmental
sequence at all intensity levels, at higher
intensity levels, the decrease in wave V
latency becomes significant at an earlier CA
Figure 5. Mean wave V latency/intensity functions
by conceptional age group for click stimuli.
Figure 6. Mean wave V500 latency/intensity functions
by conceptional age group.
119
Journal of the American Academy of Audiology/Volume 16, Number 2, 2005
than at lower intensity levels. Similarly, in
order to determine whether intensity affects
the developmental sequence for the 500 Hz
tone burst, the wave V500 latency/intensity
functions by CA groups were analyzed at
lower intensity levels. These data are
displayed in Figure 6. There is a significant
(F = 3.45, p < 0.01) decrease in latency at 55
and 35 dB nHL until after 70 weeks CA.
Thus, the latency/intensity functions for the
500 Hz tone burst follow a predicted
developmental sequence at 55 and 35 dB
nHL but not at 25 dB nHL. In fact, groups of
older infants had longer latencies than their
younger counterparts at 25 dB nHL. Again,
these data suggest the need for a large
normative latency range at or near threshold.
DISCUSSION
with previously reported data (Gorga et al,
1987). The finding that wave III latency does
decrease with age, being mature by 70 weeks
CA, may be a new finding as we are not
aware of any previously reported data on
wave III development. Lastly, our data appear
to be consistent with the model that the
auditory development of the brain stem
proceeds from peripheral to central, and
proceeds from inferior to superior.
Acknowledgment. Thank you to Tracey W. Smith
for her help in obtaining these data and Richard A.
Roberts for his comments on a previous version of this
paper. Annette Hurley and Charles I. Berlin were
supported by NIH-NIDCD P01-DC00379, and
Raymond M. Hurley was supported by TC2 DC 00007
during the data collection phase of this investigation.
Further, this investigation was supported by the
Kam's Fund for Hearing Research.
T
his investigation had three purposes: (1)
to provide age-equivalent norms for a
500 Hz toneburst evoked ABR obtained from
a large group of infants; (2) to compare these
toneburst norms to age-equivalent norms for
click evoked ABR; and (3) to investigate the
issue of low-frequency sensitivity
development. Wave V500 latency in response
to 500 Hz tone bursts decreased with age
and did not stabilize by 70 weeks CA. Wave
V latency in response to clicks decreased
with age, as has been reported by others
(Gorga et al, 1987; Gorga et al, 1989; Ponton
et al, 1992), and did not stabilize by 70 weeks
CA. These results are consistent with other
investigations, which suggest a progressive
decrease in wave V latency until 18–24
months of age postdelivery (Hecox and
Galambos, 1974; Gorga et al, 1987, 1989;
Ponton et al, 1992). Specifically, the data of
Gorga et al (1987, 1989) and Ponton et al
(1992) show that wave V latency stabilizes by
23–24 months postbirth, while the data of
Hecox and Galambos (1974) show that wave
V stabilizes by 18 months postbirth. The
finding that wave V latency for clicks and lowfrequency tone bursts develop at the same
rate is in keeping with other reports (Ponton
et al, 1992; Sininger et al, 1997). While the
Sininger et al (1997) paper does not directly
address the development issue, Ponton and
colleagues (1992) show that low-frequency
toneburst development is complete by 23
months postbirth. Wave I latency produced
by clicks did not decrease with age; it was
mature by 33 weeks CA, which is consistent
120
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