J Am Acad Audiol 9: 134-140 (1998)
Effects of Repetition Rate, Phase, and
Frequency on the Auditory Brainstem
Response in Neonates and Adults
Teralandur K. Parthasarathy*
Paul Borgsmillert
Barbara Cohlan+
Abstract
This study evaluated the effects of stimulus repetition rate, phase, and frequency on the auditory brainstem response (ABR) in normal-hearing neonates and adults . In both neonates
and adults, the results clearly showed large ABR wave V latency differences between condensation and rarefaction for low-frequency stimuli . Phase dependent latency effects are
believed to be a result of the phase-sensitive low-frequency neurons. Increasing stimulus
repetition rate produced greater wave V latency shift in neonates than in adults . The consequences of rate changes were independent of stimulus phase and frequency.
Key Words: Auditory brainstem response (ABR), frequency, phase, repetition rate, singlecycle sinusoids, wave V latency
he auditory brainstem response (ABR) is
a transient response reflecting predomiTnantly neural activity synchronized to
the onset of the stimulus (Picton et al, 1974) .
Stimulus properties such as stimulus phase and
repetition rate exert profound effects on ABR
latencies and amplitudes . In addition, a subject-related variable such as age seems to influence the outcome of ABR recording (Stockard et
al, 1979).
Considerable debate has occurred regarding
the effects of stimulus phase/polarity on the
ABR. The phase of an acoustic stimulus refers
to the initial direction of the transducer
diaphragm and the resultant direction of the
sound wave produced in the outer ear canal .
The initial phase of the stimulus is referred to
as either condensation (C) or rarefaction (R),
depending on the movement of the transducer
*Departmer)t of Special Education and Communication Disorders, Southern Illinois University at Edwardsville,
Edwardsville, Illinois ; Central Institute for the Deaf, St . Louis,
Missouri ; tDepartment of Audiology, Cardinal Glennon Children's Hospital, St . Louis, Missouri ; tDepartment of Pediatrics, St . Mary's Health Center, St . Louis, Missouri
Reprint requests. 7eralandur K . Parthasarathy, Department of Special Education and Communication Disorders,
Southern Illinois University at Edwardsville, Edwardsville,
IL 62026-1776
134
diaphragm. Movement of the diaphragm toward
the tympanic membrane produces a positive
pressure wave, also known as "C" phase. A pressure wave in a negative direction, also known as
"R" phase, is produced by a movement of the
transducer diaphragm away from the tympanic
membrane (Cann and Knott, 1979).
Electrophysiologic studies exist that demonstrate the phase-locking ability of auditory neurons (Rose et al, 1967 ; Johnson, 1980) . This
phase-locking function seems to be predominantly low-frequency dependent and is reduced
or insignificant for frequencies above 2000 Hz .
Furthermore, at low frequencies, the R phase of
the stimulus is considered excitatory while the
C phase is inhibitory (Peake and Kiang, 1962) .
In normal-hearing subjects, there is a lack
of consensus on whether any phase effects exist
and, if they exist, on the degree and direction of
phase effects on ABR latencies. Some studies
report no effect of click polarity on ABR waveform latency peaks when averaged across sample subjects (Terkildsen et al, 1973 ; Rosenhamer
et al, 1978). Other studies report shorter latencies for all ABR waveform peaks with R clicks
(Ornitz and Walter, 1975). Still others report
shorter latencies for all ABR waveform peaks
with C clicks (Hughes et al, 1981 ; Pijl, 1987).
Most of the investigators, however, have
reported differential phase effects on the ABR
Rate, Phase, and Frequency Effects/Parthasarathy et al
waveform latency peaks (Coats and Martin,
1977 ; Stockard et al, 1978 ; Borg and Lofqvist,
1981 ; Emerson et al, 1982). Subject age and
stimulus repetition rate can influence the polarity-related effects . A greater wave I latency difference for C-R was reported (Stockard et al,
1979) for neonates (0 .13 msec) when compared
to adults (0 .07 msec) . With rapid click rates
(e .g ., 80/sec), an even longer latency for wave I
(0 .35 msec) is reported for C-R difference .
Gorga and Thornton (1989) relate the lack
of consensus among investigators regarding
phase effects on ABR to nonphysiologic factors
such as differences in sample selection, recording protocols, and/or the calibration of stimulus
phase. Furthermore, other nonphysiologic factors
such as intensity differences as a function of
stimulus polarity, significant after-ringing, and/or
relatively enhanced amplitude displacement of
the transducer diaphragm during the second
half-cycle of the oscillation (Stockard et al, 1979 ;
Arlinger, 1980 ; Hughes et al, 1981 ; Weber et al,
1981) also have been suggested as possible reasons for the reported ABR latency differences .
In addition, the effects of reversing the click
phase on ABR latencies are expected to be minimal due to the relative short time intervals
between the C and R phase clicks (Coats and
Martin, 1977 ; Gorga et al, 1991 ; Orlando and Folsom, 1995). Studies of such parametric effects
could be beneficial in suggesting procedural
strategies that may enhance ABR recording.
Sounds having greater duration than clicks have
been used in this study to ascertain the role
that frequency phase plays in the generation of
scalp recorded ABR and to ascertain also how
repetition rate interacts with stimulus phase, frequency, and age in evoking ABR waveforms.
The objective of the present research, therefore,
was to determine the effects of stimulus repetition rate, phase, and frequency on the ABR wave
V latency in neonates and adults .
METHOD
from obstruction based on an otoscopic examination by a licensed neonatologist ; (4) negative
family history of hearing loss and free from risk
ofhearing loss (Joint Committee on Infant Hearing, 1995); (5) informed signed consent from the
parent(s) for participation as a subject; and (6)
less than 72 hours postpartum age at the time
of ABR testing.
.
All 10 adult subjects were tested either in
natural sleep or in a relaxed awake state and met
the following criteria : (1) physically and neurologically normal based on subject interview; (2)
negative family history of hearing loss and neurologic problems ; (3) external auditory canals free
from obstruction based on an otoscopic examination ; and (4) normal hearing sensitivity
(-10-15 dB HL) at octave frequencies from 0.25
to 8.0 kHz and normal tympanometric findings
(re ANSI, 1969).
Stimuli
Acoustic stimuli consisted of single-cycle,
Blackman gated sinusoids at 0.25 and 2.0 kHz
at two repetition rates: 11 .1 and 55 .5/sec . C and
R signals of all two frequencies and repetition
rates were randomly presented at 75 dB nHL.
Acoustic polarity was initially determined by
coupling the earphone to the sound level meter
(SLM), routing the AC output from an SLM to
an oscilloscope . The initial portion of the sinusoid was characterized either by a positive or a
negative-going zero crossings on an oscilloscope
for C and R stimuli, respectively. After checking
for stimulus polarity, the stimulus repetition
rate and frequency were measured from the
oscillographic display. For two repetition rates
(11.1 and 55 .5/sec), the time interval between
identical points on successive stimuli was measured at 90 .09 and 18 .01 msec, respectively. The
frequency calibration for 0.25 and 2 .0 kHz stimuli was established by measuring one cycle duration on the oscillographic sweep at 4 and 0.5
msec, respectively. Stimuli were delivered via a
tube phone (Etymotic, ER-3A) .
Subjects
Procedures
Ten full-term neonates and 10 healthy,
young adults served as subjects . All neonates
were tested during natural sleep and met the following criteria : (1) normal, full-term gestational
age between 38 to 42 weeks; (2) APGAR scores
greater than or equal to 8 at 1 and 5 minutes
postparturition; (3) physically and neurologically normal with external auditory canals free
Two channel ABRs were measured between
gold-plated disc electrodes affixed to the vertex
and the ipsilateral and contralateral earlobes .
All three electrodes were referred to a ground
electrode placed at the high forehead . Impedance
among all four electrodes was always less than
3.0 kohms and differences among electrodes
were always less than 1.0 kohm . Baseline imped-
Journal of the American Academy of Audiology/Volume 9, Number 2, April 1998
ance values were monitored throughout testing
to ensure consistency of recording. The EEG
activity was amplified (100,000) and filtered
(0 .1 to 3 .0 kHz) using a Biologic Navigator
Evoked Potential System . The recording time
base was 15 msec . For each test condition,
responses to 2048 stimulus presentations were
included in each averaged response, which was
replicated once .
RESULTS
Figure 2 A, Representative ABR waveforms from an
adult subject in response to 75 dB nHL (2 .0-kHz tone
burst) at two repetition rates. Within each panel, the top
two superimposed traces represent responses to rarefaction (R) stimuli, the bottom two superimposed traces
represent responses to condensation (C stimuli. B, the
same except that stimulus is 0.25-kHz tone burst. ABR
Averaged Waveforms
Figure 1(A and B) illustrates the ABR waveforms from one neonate for 75 dB nHL at two
rates to 2.0 and 0.25-kHz tone bursts . In each
panel, the top two superimposed traces represent
the responses obtained for R stimuli and the
bottom two superimposed traces represent the
responses obtained for C stimuli . Clearly,
response latency depends on stimulus phase
and frequency. Well-formed ABR waveforms
were observed at both frequencies for C and R
stimuli. However, there were notable waveform
differences . Whereas the ABR morphology for the
C and R stimuli is essentially similar for the
high-frequency stimuli (see Fig. 1A), substantial
latency differences can be observed between C
and R responses for low-frequency stimuli (see
Fig. 1B). Furthermore, increasing the rate from
11 .1 to 55 .5/sec resulted in prolongation of the
ABR wave V latency (see Fig. 1, A and B) .
wave V peaks are labeled with triangles.
Figure 2 (A and B) illustrates the ABR waveform from one adult for 75 dB nHL at two rates
to 2.0- and 0.25-kHz tone bursts . In each panel,
the top two superimposed traces represent the
responses obtained for R stimuli and the bottom
two superimposed traces represent the responses
obtained for C stimuli. Again, clear ABR waveforms were observed for both frequencies for C
and R stimuli . Similar to those for neonates,
the morphology of the ABR waveform for the C
and R stimuli is essentially the same for the highfrequency stimuli (see Fig. 2A). However, substantial latency differences can be observed
between the C and R responses for low-frequency stimuli. Again, as seen in neonates,
increasing the rate from 11 .1 to 55.5/sec resulted
in prolongation of the ABR wave V latency (see
Fig. 2, A and B) .
Statistical Analysis
Figure 3 (A and B) illustrates average ABR
wave V latencies (-!-1 standard deviation) as a
function of repetition rate, phase, and frequency
in neonates and adults . Intersubject latency
variability, as indicated by the bars, is much
greater in neonates than in adults for lower
than for higher frequencies . A multivariate
analysis of variance (MANOVA) for repeated
measures was performed. A post hoc Tukey's
multiple comparison test on all of the interaction effects was calculated with the statistical significance level set at .05.
Figure 1 A, Representative ABR waveforms from a
neonate in response to 75 dB nHL (2 .0-kHz tone burst)
at two repetition rates. Within each panel, the top two
superimposed traces represent responses to rarefaction
(R) stimuli, the bottom two superimposed traces represent responses to condensation (C) stimuli . B, the same
except that stimulus is 0.25-kHz tone burst. ABR wave
V peaks are labeled with triangles.
136
Rate, Phase, and Frequency Effects/Parthasarathy et al
effect showed that the ABR wave V latency shift
with increases in repetition rates is significantly
greater (0 .75-0.9 msec) in newborn neonates
than in adults (0 .3-0 .5 msec) . The rate X frequency and rate X frequency X age interaction
effects on ABR wave V latency were insignificant .
Phase Effects
11 .1
65.5
Repetition Rob
(stlmulusec)
11 .1
55.5
Repeuuon Rate
(sumulusec)
Figure 3 A, The mean ABR wave V latencies in adult
subjects as a function of repetition rate for rarefaction
(open symbols), condensation (filled symbols) stimuli at
2.0 kHz (triangles), and 0 .25 kHz (circles). B, the same
except that the subjects are neonates . Error bars represent ±1 SD .
Rate Effects
The results of the MANOVA (Table 1)
revealed a significant interaction between rate
and age. A post hoc analysis on the interaction
Table 1
Results of MANOVA : ABR Wave V
Latency vs Rate, Phase, Frequency, and Age
Effect
Rate (R)
Phase (P)
Frequency (F)
Age (A)
RxP
RxF
RxA
PxF
PxA
FxA
RxPxF
PxFxA
FXAxR
RxPxFxA
Results
S
S
S
S
NS
NS
S
S
NS
S
NS
NS
NS
NS
S = significant (p < .05) ; NS = nonsignificant (p > .05) .
With few exceptions, in both neonates and
adults, the R stimuli at 0.25 kHz elicited shorter
absolute ABR wave V latencies. The MANOVA
results revealed a significant interaction effect
between phase and frequency (see Table 1) . A
post hoc analysis on the interaction effect showed
that the phase effect on ABR wave V latency produced significantly shorter latencies (0 .75-1
msec) to R stimuli at low frequency. However, the
phase effect on ABR wave V latency was not significant for the high-frequency stimuli. The
phase X rate, phase X age, phase X rate X frequency, phase X frequency X age, and phase X
rate X frequency X age interaction effects on
ABR wave V latency were insignificant .
Frequency and Age Effects
The results of the MANOVA (see Table 1)
uncovered a significant interaction between frequency and age . A post hoc analysis on the interaction effect showed significantly shorter ABR
wave V latencies (1 .25-1 .5 msec) in adults than
in neonates .
DISCUSSION
he results of this investigation clearly show
Tthat large ABR wave V latency differences
occur as a result of stimulus phase reversal for
low-frequency stimuli in both neonates and
adult subjects . For the high-frequency stimuli,
subjects were likely to demonstrate shorter
latencies with either R or C stimuli. Singlecycle sinusoids were used to produce placespecific excitation in the cochlear partition. The
frequency content of the signal produces, as
would be expected, a certain space-time pattern
of basilar membrane motion, which in turn activates specific sets of neural elements (Don and
Eggermont, 1978). Although few experiments
have shown place-specific excitation at low
levels of sound stimulation, basal spread of
excitation seems to occur for relatively moderate to high levels of sound stimulation (Klein
and Teas, 1978 ; Stapells and Picton, 1981 ; Gorga
et al, 1988).
Journal of the American Academy of Audiology/Volume 9, Number 2, April 1998
With few exceptions, in both neonates and
adults, the phase effects on ABR wave V waveforms produced shorter latencies to R stimuli for
low-frequency (0 .25 kHz) stimuli. Again, in the
majority of subjects, the phase effect was not
apparent for the high-frequency (2 .0 kHz) stimuli. Our findings in the present study are in
good agreement with the previous results (Ornitz
et al, 1980 ; Moller, 1986 ; Gorga et al, 1991 ;
Fowler, 1992 ; Orlando and Folsom, 1995), which
have shown larger latency differences as a function of phase reversal for low-frequency stimuli.
These phase-related latency changes that are
observed for low-frequency stimuli seem to be a
result of phase-locking neurons tuned to low-frequency stimuli (Rose et al, 1974 ; Gorga and
Thornton, 1989). It is presumed that the phasedependent neural responses may be delayed by
one-half period of the stimulus wavefo (Brama
and Sohmer, 1977).
In this study, for both neonates and adults,
the C-R latency difference (0 .75-1.0 msec) was
less than the predicted latency difference for
the C and R stimuli. A possible explanation for
the minimal C-R latency difference is the basal
spread of excitation at high-level stimuli (75 dB
nHL) being used in our study. Salt and Thornton (1984) and Beattie and Boyd (1984) reported
no systematic increase in C-R latency difference with an increase in stimulus rise time . In
their study, however, increasing the stimulus rise
time at a high-intensity level could not have
minimized either basalward spread of excitation
or increases in traveling wave velocity (Hecox
and Deegan, 1983 ; Neely, 1990). The lack of CR latency difference for the 2.0-kHz stimulus is
most likely caused by an inability to resolve the
relatively short temporal onset differences with
the volume-conducted far-field ABR recording
(Orlando and Folsom, 1995).
Although the majority of both neonates and
adults show shorter absolute ABR wave V latencies for the low-frequency R stimuli, a few
neonates and adult subjects show shorter latencies for the low-frequency C stimuli. Findings of
shorter latencies for C stimuli in our present
study are few: 20 percent in adults and 30 percent in neonates . These findings are consistent
with previous findings, which have reported
shorter latencies for C stimuli in 10 percent to
30 percent of the subjects (Coats and Martin,
1977 ; Stockard et al, 1979 ; Borg and Lofqvist,
1981 ; Orlando and Folsom, 1995). In addition
to nonphysiologic factors such as intensity,
frequency, sample selection, recording protocols, and calibration of stimulus phase (Gorga
138
and Thorton, 1989), the intersubject variability
might be a result of physiologic factors such as
variations in middle ear transfer function and
inner ear mechanics (Dallos, 1975 ; Borg et al,
1982 ; Gerull et al, 1985 ; Brenkman et al, 1987).
Furthermore, the analysis of data revealed
a significant interaction effect between repetition
rate and age. The rate-dependent change on
wave V latency was significantly greater in newborn neonates (0 .75-0.9 msec) than in adults
(0 .3-0 .5 msec) . The latency changes with repetition rate were independent of the stimulus
phase and frequency. These findings are in good
agreement with the previous results (Stockard et
al, 1979 ; Despland and Galambos, 1980 ; Lasky,
1984), which have shown that greater latency
shifts in newborn neonates occur as the repetition rate of the stimulus is increased. This agerelated difference in latency-rate functions has
obvious clinical implications for interpreting
developmental change in the ABR waveforms.
The younger the subject, the longer the expected
ABR latencies to the same auditory stimulus
(Schulman-Galambos and Galambos,1975; Starr
et al, 1977). Prolonged neural transmission time
in younger subjects, due to incomplete myelination and decreased synaptic efficiency, is considered to be the neurophysiologic basis for these
rate-age-latency interactions (Hecox, 1975 ; Pratt
and Sohmer, 1976 ; Lasky, 1984).
The frequency effects on ABR waveforms
in both the neonates and adults have shown
shorter wave V latencies to a 2.0-kHz tone burst
than to a 0.25-kHz tone burst. In addition, the
analysis of data showed a significant interaction
between frequency and age. As expected, independent of stimulus frequency, the ABR wave V
latencies were shorter (1 .25-1.5 msec) in adults
than in neonates . The frequency content of the
signal produces, as would be expected, a certain
space-time pattern of basilar membrane motion,
which in turn activates specific sets of neural elements (Don and Eggermont, 1978). The results
are also in consonance with previous results
(Stapells and Picton, 1981 ; Gorga et al, 1988,
1991 ; Parthasarathy and Moushegian, 1993).
CONCLUSIONS
irst, in both neonates and adults, large ABR
Fwave V latency differences occur as a result
of stimulus phase reversal for low-frequency
(0 .25 kHz) stimuli. With few exceptions, R stimuli elicited shorter ABR wave V latencies. However, minimal ABR wave V latency differences
occurred as a result of stimulus phase reversal
Rate, Phase, and Frequency Effects/Parthasarathy et al
for high-frequency (2 .0 kHz) stimuli. Findings
from our study are supported by data from subjects with high-frequency sensorineural hearing
loss who demonstrate significant C-R differences for clicks (Coats and Martin, 1977 ; Pijl,
1987). It is hypothesized that subjects with highfrequency sensorineural hearing loss receive
greater contribution to the ABR from the phasesensitive low-frequency neurons (Gorga et al,
1991). Considering the large C-R differences
expected for low-frequency stimuli in normalhearing subjects or in subjects with high-frequency sensorineural hearing loss (Borg and
Lofqvist, 1981 ; Borg et al, 1982 ; Pijl, 1987), summing or alternating the stimulus polarity in
clinical ABR application is not recommended.
Based on our results, the need for independent
norms for different stimulus polarity for neonates
and adults is strongly recommended. In both
neonates and adults, the use of single-polarity
stimuli or separate averaging for each polarity
is recommended.
Second, compared to adults, greater ABR
wave V latency shift occurs in neonates as a
result of increase in repetition rate . The latency
changes with repetition rate are both phase and
frequency independent. Finally, compared to
adults, neonatal ABR wave V latencies at 0.25
and 2.0 kHz are longer with greater variability
to a 0.25-kHz tone burst. The present research
study should be replicated in both normal and
sensorineural hearing loss subjects using different sound intensities, repetition rates, and age
groups . Aspects pertaining to ABR morphologic
differences as a function of changes in stimulus
repetition rate, phase, and frequency in different age groups warrant further investigation.
Acknowledgment . The authors wish to thank Dr. Fran
Tucker, Dr. Marlene Salas-Province, and three anonymous reviewers for their helpful suggestions regarding
an earlier version of this manuscript . Portions of this
paper were presented at the 1995 Acoustical Society of
America Convention, St . Louis, MO .
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