Sleep. 14(3):241-248
© 1991 Association of Professional Sleep Societies
Modification of Sleep Respiratory Patterns
by Auditory Stimulation: Indications of
a Technique for Preventing
Sudden Infant Death Syndrome?
Malcolm W. Stewart and Lara A. Stewart
Department of Psychology, University of Otago, Dunedin, New Zealand
Summary: Sudden infant death syndrome (SIDS) has been associated with premorbid respiratory irregularities
that may contribute to the subsequent occurrence of SIDS (e.g. by chronic hypoxia). Conventional apnea alarms
will detect periods of extended apnea but not other chronic respiratory irregularities that could contribute to SIDS.
The effect of a brief, quiet, repetitive auditory stimulus on the sleep respiratory behavior of infant dogs and pigs
was assessed. Stimulus presentation was associated with an increase in the sleep respiration rate irrespective of the
stimulus presentation rate being faster or slower than the baseline respiratory rate, and irrespective of the pattern
of presentation being regular or random. These results suggest that apnea monitoring systems may be improved by
an additional function in which less extreme respiratory irregularities initiate the time-limited presentation of a
quiet, repetitive, auditory stimulus, aimed at normalizing the respiratory pattern. This function could enhance the
preventative role of the alarm systems by reducing the development of pathology that may promote some instances
of SIDS. Key Words: SIDS, Infant respiration, Sleep respiration, Sleep apnea.
Sudden infant death syndrome (SIDS or cot death)
is defined as sudden death of any infant or young child
which is unexpected by history and unexplained by
postmortem (1). The highest prevalence of SIDS is in
the second to fourth month postpartum. The etiology
of SIDS is not well understood and is generally considered to be multifactorial (1).
An extensive literature has related SIDS to irregularities in the respiratory patterns of infants (2). Nearmiss SIDS infants (those resuscitated following an almost-fatal incident), siblings ofSIDS infants and groups
considered at risk for SIDS have all shown irregularities of sleep breathing patterns when compared with
controls (3). Although prospective studies have shown
few differences in the overall respiratory patterns of
infants who were subsequently SIDS victims and
matched controls (4), subtle differences, indicative of
delayed cardiorespiratory development in SIDS victims, have been shown to be present as early as within
the first two postnatal weeks (5). Among the primary
Accepted for publication February 1991.
Address correspondence and reprint requests to Malcolm Stewart,
Department of Psychology, University of Otago, P.O. Box 56, Dunedin, New Zealand.
respiratory irregularities are prolonged periods of apnea and a highly variable respiratory rate. The respiratory irregularities are widely believed to be due to
an abnormality in the brainstem neuroregulation of
cardiorespiratory control (2). Some postmortem studies have shown anatomical changes in SIDS victims
that are consistent with chronic hypoxia (6,7), possibly
due to prolonged apnea during sleep. Chronic hypoxia
may in tum exacerbate the neurological deficit and lead
to increased apnea (1).
Despite a huge research effort related to SIDS in
recent years, few preventative measures are available
to minimize the risk of SIDS occurring in at-risk infants. A common intervention for infants considered
to be at risk is the use of an apnea alarm, in which a
loud alarm sounds if the child does not breathe for a
set period of time: e.g. 20 sec. Although these alarms
may prevent some incidents of SIDS and often give
considerable comfort to the parents, their efficacy has
not been clearly demonstrated and remains contentious (2). One limitation on the efficacy of apnea alarms
may be the lack of response to sustained respiratory
patterns that are slow or irregular, but which do not
show apneas of sufficient duration to trigger the alarm.
These respiratory patterns, if unchecked, may lead to
241
242
M. W. STEWART AND L. A. STEWART
inefficient ventilation and chronic hypoxia. Thus, although the alarm may prevent a SIDS death from occurring when the infant is properly monitored, the alarm
may not prevent the development of a pathological
state increasing the risk offuture mortality due to SIDS.
Modification of such pathological respiratory patterns
may be required.
Environmental stimuli can modify sleep respiratory
patterns (8,9). Humans are certainly capable of perceiving and responding to auditory stimuli during sleep.
Studies have shown differential electroencephalograph
(EEG) and galvanic skin response to personally relevant and irrelevant auditory stimuli (names) in sleeping adult humans (10). Badria et al. (8) trained normal
adults to terminate an auditory signal by taking a deep
breath. EEG recordings showed that the behavioral
response was frequently achieved with no evidence of
change in sleep state.
Human infants are also able to process environmental information and respond to environmental
stimuli during sleep (11,12). These findings are consistent with the increasing recognition by developmental psychologists that infants are more competent
processors of environmental information than was previously thought (13). McKenna (12) presented evidence that appropriate stimuli, including auditory
stimuli such as parental breathing sounds, typically
made the infant respiration pattern more regular and
increased the respiratory rate. In contrast, Busby and
Pivik (14), using a loud, pure-tone auditory stimulus
(1,500 Hz, up to 123 dB sound pressure level, alternating 3 sec on, 3 sec off), found no modification in
the childrens' (mean age = 10.3) sleep respiration rate.
The differing results may reflect variations in the auditory stimuli used and in the age of the subjects studied. The respiratory patterns of very young infants appear to be particularly responsive to external stimuli
(12).
Kahn and his colleagues (11) showed similar auditory arousal thresholds for infants who were at risk fix
SIDS and normal infants. This indicates that at-risk
infants are able to process environmental stimuli during sleep in the same way as normal infants. McKenna
(12) presented evidence that such stimuli may be a
protective factor against the occurrence of SIDS in
infants with respiratory problems.
Appropriate environmental stimuli could cause
modification of the respiratory responses through a
number of processes. First, the infants may entrain
(synchronize) their breathing with the environmental
stimulus. Unpublished anecdotal reports suggest that
this may sometimes occur. Second, a kind of partial
entrainment or pacing effect may occur in which a
stimulus at one time (for example, during an apneic
period) may promote a respiratory response, whereas
Sleep, Vol. 14. No.3, 1991
a stimulus at another time (for example, during regular
breathing) would not. Third, the environmental stimuli could cause arousal leading to a change in the depth
of sleep, with a consequent change in the respiration
rate. Increased auditory stimulation leads to an increase in respiration rate in awake adults (15). However, arousal is not always necessary for modification
of sleep respiration (8).
The present studies were aimed at testing the hypothesis that the sleep respiratory patterns of infant
animals could be influenced by the presentation of a
repetitive artificial auditory stimulus and to explore
the effect of modification of some parameters of the
pattern of stimulus presentation.
STUDY 1: INFANT DOGS
The first study was a pilot study to test the effectiveness of an auditory stimulus at modifying respiration rates. The first hypothesis was that presentation
of a stimulus at a rate faster than the mean respiration
rate during the baseline period would lead to an increased respiration rate. The second hypothesis was
that provision of a signal slower than the intrinsic respiration rate would lead to a reduction in the respiration rate, consistent with a full entrainment mechanism.
Method
Subjects. Three 6-wk-old German shepherd cross
puppies (two males, one female) were randomly chosen
for testing from six litter-mates. The puppies were separated from their litter-mates and mother and were
tested individually. Separation did not appear to cause
the puppies undue distress.
Apparatus. The auditory stimulus was generated by
a white noise generator that delivered a 1.2-sec burst
of white noise at a regular rate that could be varied
from 5 to 60 sounds/min. The amplitude envelope was
shaped so as to give a O.4-sec attack and a O.6-sec
decay. The signal was broadcast to the animal, from a
speaker adjacent to the enclosure, at approximately 60
dB sound pressure level, which could be described as
the sound intensity of normal conversational speech.
Procedure. All testing was carried out in a partially
darkened, temperature-controlled, sound-attenuated
room, during the hours of daylight. After a short settling period the puppy was placed in a basket lined
with a blanket. The experimenters sat quietly in the
room near the basket. The animals tended to settle and
sleep within 15 min of being placed in the basket.
Criteria for sleep were taken as a sustained period of
minimal large body movements, closed eyes and no
other overt signs of wakefulness. When the animal was
243
AUDITORY STIMULI AND SLEEP RESPIRATION
asleep the respiration rates were measured by counting
respiratory movements of the flank. After the animal
had been asleep for a prearranged, randomly varied
number of minutes, an experimental cycle was begun.
The delay between sleep onset and the initiation of the
experimental cycle was randomized to prevent confounding due to regular variation in the respiratory
rate during the sleep cycle.
An experimental cycle consisted of four 5-min periods, each separated by a I-min transition. The respiration rate was recorded for each minute of each
period. The first and third periods were baseline conditions during which no auditory stimuli were broadcast. During the second period, the auditory stimuli
were broadcast at a rate either 5 stimuli/min faster or
5 stimuli/min slower than the average respiration rate
for the preceding baseline period. During the fourth
period the auditory stimulus was broadcast at a rate
that deviated from the preceding baseline respiratory
rate by 5 sounds/min in the opposite direction to the
deviation used in the second period. Whether the second period sound rate was faster or slower than baseline respiration rate was varied, giving either an ABAC
or ACAB design. The full minute of the transition
period was used to gradually increase the volume of
the auditory stimulus to maximum prior to the stimulus condition, or to decrease the stimulus to silent
prior to the baseline condition. If the animal remained
asleep following completion of an experimental cycle,
a second cycle was begun. Recording was terminated
if the animal showed any signs of waking.
Results
Table 1 presents the means and standard deviations
of the respiration rate in all experimental stages. The
data set consists of six complete cycles and four cycles
that were terminated prior to completion of all conditions.
A two-factor [experimental stage x trial (block factor)] ANOVA, with respiration rate as the dependent
variable, showed a significant difference between the
respiration rate in the four conditions [F(3, 163) = 3.72;
p < 0.02]. Planned comparisons on the data showed
that the respiration rate during the period of faster
stimulation was significantly faster than the respiration
rate during the preceding baseline period [F(l, 163) =
13.35; p < 0.01]. The mean increase in rate was 4.02
breaths/min with the auditory stimulus being set at 5
breaths/min faster.
The respiration rate in the slower stimulation condition was faster than the rate during the preceding
baseline period, but this effect did not reach significance at the 5% level [F(l, 163) = 1.42]. Analytical comparison showed that the respiration rate in the slower
TABLE 1. Infant dog sleep respiration rate during baseline
and auditory stimulus
Stimulus
conditiona
Baseline F
Faster stimulus
Baseline S
Slower stimulus
Respiration rate (breaths/min)
Mean
SD
30.30
34.32
30.34
31.64
5.24
7.28
4.28
6.78
a Faster stimulus = a period with an auditory stimulus rate of 5
repetitions/min faster than the baseline respiration rate. Slower stimulus = a period with an auditory stimulus rate of 5 repetitions/min
slower than the baseline respiration rate. Baseline F = a period of
no auditory stimulus, preceding the faster stimulus period. Baseline
S = a period of no auditory stimulus, preceding the slower stimulus
period.
stimulation condition was significantly slower than the
respiration rate in the faster stimulation condition
[F(l,163) = 5.34; p < 0.03].
The respiration rates in the first and second control
periods were not significantly different [F(l,163) =
0.05], which suggests that the timing of condition presentation was successfully randomized with respect to
any in the sleep respiration pattern related to the sleep
cycle.
Discussion
This experiment demonstrated that infant dogs
showed a change in sleep respiration rate when presented with a repetitive audible signal at a rate similar
to, but different from, their breathing rate. Introduction of a stimulus at a rate 5 sounds/min faster than
the preceding respiration rate appeared to lead to an
increase in the average respiratory rate. Introduction
of a stimulus at a rate lower than the preceding respiration rate led to a small but not statistically significant increase in the respiration rate.
These results indicate that sleep respiration rates in
young animals can be modified by a repetitive auditory
stimulus. No evidence was found of a decrease in the
respiration rate in response to slower stimuli. This indicates that the puppies did not entrain to environmental stimuli slower than their intrinsic breathing
rate. The data are consistent with either an arousal or
partial entrainment model of respiration modification.
A slower stimulus rate could cause less arousal than a
faster stimulus. Alternatively partial entrainment might
occur if the animal's intrinsic respiratory control mechanisms buffered against the respiration rate being lowered by environmental stimuli, but would allow stimuli
to initiate breaths.
The present study was designed as a pilot study and
has a number of limitations and possibilities for extension. First, the appropriateness of the daytime
sleep of young dogs as a model for at-risk infant huSleep, Vol. 14, No.3, 1991
244
M. W. STEWART AND L. A. STEWART
mans has not been shown. For this reason, in Study 2 ration rate and that presentation of an irregular stimthe nocturnal sleep of a diurnally active animal, pigs, ulus at a mean rate slower than baseline respiration
which have a respiratory physiology similar to humans rate would also lead to a change in the respiration rate.
(16), was studied. The subjects were studied at an age An increase in respiration rate in response to an irregwhen their respiratory system maturation was com- ular signal would be consistent with an arousal or parparable to that of human infants most at risk for cot tial entrainment effect. Respiratory slowing, or no
death (16).
change, in response to an irregular signal could be conA further limitation was the absence of monitoring sistent with a full entrainment effect because the subject
of the phase of sleep [rapid eye movement (REM) or would be unlikely to entrain to an irregular stimulus.
nonrapid eye movement (NREM)]. The effect of differing stages of sleep across the stimulation conditions Method
was randomized in the present design but the efficacy
of auditory stimulation in different sleep stages could
Subjects. Two 5-wk-old land-race-Iarge-white cross
not be assessed. SIDS has not been clearly demon- piglets, one male and one female, were obtained from
strated to be associated with any particular stage IDf a commercial piggery. The subjects were the lowest
sleep but respiratory patterns do vary with differing weight of approximately 40 similar-aged piglets, all of
sleep stages. Phillipsen et al. (17) reported that, f4)f which had been weaned for at least 8 days.
dogs, NREM sleep respiration patterns were slowe:r,
Apparatus. The animals were housed in pens in heatdeeper and less variable than wakefulness, whereas ed, naturally lit university buildings for the duration
REM sleep respiratory patterns were more rapid, shal- of the study. The piglets shared a 2.5-m x 2.5-m pen
low and irregular. Apneic periods have been reported during the day. Testing was carried out in a 2-m x
during both REM (18) and NREM sleep (19). ExplID- 2-m night pen in a separate temperature-controlled
ration of the interaction between sleep phase and the room. The pigs were fed in the day pen on a standard
effect of auditory stimulation would be valuable.
composite feed provided by the piggery. No food was
Finally, the time lag for a response to the auditory available in the night pen. Water was available in both
stimulus and the effect of habituation to the stimulus pens, ad libitum.
A BBC computer was used to produce the auditory
have not been addressed by the present study. These
are important issues in relation to the clinical utility stimulus, to monitor and display the respiratory waveof the technique. Some of these issues were addressed form, to store all data and to calculate the respiratory
rate.
in the second study in this series.
The auditory stimulus consisted of a lA-sec envelope
of white noise with a 0.6-sec attack and a O.S-sec
STUDY 2: INFANT PIGS
decay. The auditory stimulus sounded similar to a wave
This study aimed to partially replicate the pilot study breaking, similar to sleep breathing sounds and was
and to extend it in a number of methodologically and delivered to the animal, from a speaker adjacent to the
theoretically important areas. The nocturnal sleep of pen, at a sound intensity of approximately 60 dB sound
an animal with a respiratory system more similar to pressure level (normal conversational speech volume).
Respiration was monitored by a diode temperature
that of humans was studied, and data for NREM and
transducer
taped to the snout of the animal. A purposeREM sleep were treated separately.
built
signal
conditioner was used to amplify and adjust
A computer system was used to monitor respiration
the
D.C.
level
of the transducer output. The output
patterns and to generate the auditory stimulus. The
from
the
signal
conditioner was digitized by the BBC
experimental design was altered in that the order of
computer
at
a
sample
rate of 10 samples/sec. The digstimulus presentation was completely randomized and
itized
signal
was
stored
on disk, printed out later and
prestimulus and poststimulus baselines were obtained
processed
to
allow
on-screen
display ofthe respiratory
for all stimulus periods to allow the carry-over em:ct
waveform
and
the
respiratory
rate. The sleep status
of the stimulus to be more effectively studied.
(REM
or
NREM)
was
keyed
in
by the observer and
The use of a regular auditory stimulus faster than
the baseline respiration rate was retained from the pre- stored.
vious experiment. However, the regular stimulus, which
Measures. Helfand et al. (20) defined criteria for diswas slower than the baseline respiration rate, was re- tinguishing between REM and NREM sleep in human
placed by an irregular auditory stimulus also slower adults. Their behavioral ratings correlated well with
EEG ratings (91 % and 92% accuracy for REM and
than the baseline rate.
The hypotheses for the current experiment were that NREM, respectively). These criteria (20), similar to
presentation of stimuli at a rate faster than the baseline those used with newborn infants previously (S), were
stimulus rate would lead to an increase in the respi- adapted for use with the pig. The interrater reliability
Sleep, Vol. 14, No.3, 1991
AUDITORY STIMULI AND SLEEP RESPIRATION
245
TABLE 2. Infant pig sleep respiration rate during baseline and auditory stimulus
Respiration rate (breaths/min)
Sleep
phase/
stimulus
NREM
Regular
Random
REM
Regular
Random
Baseline I
Baseline 2
Stimulus
Mean (SO)
n
Mean (SO)
n
Mean (SO)
n
16.3 (3.8)
16.6(4.1)
80
39
19.4 (4.5)
19.3 (5.0)
100
53
15.7 (3.8)
17.1 (4.8)
42
21.3 (5.5)
18.3 (4.0)
31
13
21.5 (5.0)
25.0 (6.1)
16
13
23.5 (5.3)
21.9 (4.8)
29
8
was assessed for two observers on 105 occasions. The
interrater agreement was 98.1 %, kappa = 0.95, indicating a high level of reliability of ratings.
Procedure. No testing was carried out for the first
three nights, to allow the animals to settle into their
new environment. Testing was carried out over nine
nights and was aborted (due to the pig not settling, or
equipment malfunction) on four nights. All testing was
carried out between 9 p.m. and 3 a.m. One to six
(median = 3) experimental cycles were completed each
night.
In the evening, one animal was moved to the night
pen, provided with water and left to settle for between
2 and 4 hr. When the experimenter returned, if the
animal was asleep, the transducer was gently taped to
the animal's snout. This procedure appeared to disrupt
sleep only minimally or not at all. If the animal awoke,
the experimenter left the room and sleep was usually
quickly reestablished.
The experimental session consisted of periods of auditory stimulus presentation preceded and followed by
a baseline period. Two patterns of stimulus presentations were utilized: regular and random. An identical
auditory stimulus was used in both conditions. During
the regular condition, the stimulus was presented at a
regular interstimulus interval set to be approximately
5 stimuli/min faster than the mean baseline respiration
rate. During the random condition the stimuli occurred
after a randomly varying interval, with a mean rate of
approximately 7 stimuli/min slower than the mean
baseline respiration rate. One pattern of stimulus presentation was used per stimulus period. The order of
stimulus pattern was randomly chosen.
In baseline periods, the respiration waveform and
sleep stage were monitored and recorded. The mean
baseline respiration rate was used to set the stimulus
rate for the subsequent stimulus condition. In the experimental periods, the stimulus was broadcast and
the respiration and sleep stage data were recorded. The
maintenance and phase of sleep (REM/NREM) were
monitored approximately every 30 sec. Baseline and
stimulus periods ran for a minimum of5 min ofNREM
72
sleep. Periods of REM tended to be short (e.g. 2 min)
and intermittent. When REM occurred the current
stimulus condition was extended to allow a minimum
of 2-3 min of NREM data in the postREM phase.
Data collection continued until the animal woke or
the observer terminated the session. Following termination of data collection, the experimenter removed
the sensor and left the pig in the night pen. In the
morning the pig was returned to the day pen. Both pigs
were fed after midday in the day pen.
Data analysis. The respiration rate per minute was
subsequently ascertained from a paper printout of the
respiratory waveform. The data were divided into three
experimental stages: the 5 min prior to stimulus presentation (pre stimulus control), during stimulus presentation and the 5 min following stimulus presentation (poststimulus control). Analysis was primarily by
ANOVA. The data were collapsed across subjects due
to the small number of data points in the REM cells.
Results
Effect of auditory stimulus. Table 2 shows the average respiration rate per minute, during REM and
NREM sleep, for each experimental stage and each
stimulus condition. A 3-factor ANOV A (2 sleep phases
x 2 stimulus patterns x 3 experimental stages) was
performed with the respiration rate as the dependent
variable. A significant main effect was found for sleep
phase [F(1,484) = 69.6; p < 0.0001]. The respiration
rate was higher during REM than during NREM sleep
(means = 21.9 and 17.4 breaths/min, respectively). A
significant main effect was found for experimental stage
[F(2,484) = 12.4; p < 0.0001]. The respiration rate
was significantly higher during presentation of an auditory stimulus than during either the preceding or
following baseline. The 3-way (sleep phase x stimulus
pattern x experimental stage) interaction was significant [F(2,484) = 4.4; p < 0.02]. The small cell sizes
for the REM data set make this effect difficult to interpret. The stimulus pattern x experimental stage interaction was not significant, indicating a similar reSleep, Vol. 14, No.3, 1991
246
~"
~
~
8-
'"
Oi
M. W. STEWART AND L. A. STEWART
22
21
2Q
19
a:
18
.2
17
.~
16
a:
'"
15
Random stim.
c
ri!
Regular S'im.
123451234512345
Baseline (pre)
Stimulus On
Baseline (post)
Condition and Minute
FIG. 1. Change in infant pig NREM sleep respiration rate over
time, in the presence (stimulus on) and absence (baseline) of an
auditory stimulus presented at a regular rate or at a randomly variable rate. Data for two animals recorded for 24 experimental cycles.
Each mean calculated from n = 16 for regular stimulus and n =, 8
for random stimulus.
sponse to the auditory stimulus regardless of pattern
of stimulus presentation. The other main effects and
interactions were not significant.
Slightly less REM sleep was recorded during auditory stimulation (REM for 16% of total sleep time)
than during baseline (REM for 26% of sleep time) [chi
square (n = 496, df = 2) = 6.5; p < 0.05].
Casual observation suggested that the increase in
respiratory rate was related in part to a more regular
respiratory pattern in the presence of the auditory stimulus, although the data available did not allow for statistical confirmation ofthis. Observation ofthe animal
during sleep revealed no pattern of behavioral signs of
arousal in the presence of the auditory stimulus.
Habituation. To explore habituation to the signal
over time, a 3-factor ANOVA (2 stimulus patterns x
3 experimental stages x 5-min time periods) was performed with the NREM respiration rate as the dependent variable. There were insufficient REM data to
allow inclusion in the analysis. Figure 1 shows the
pattern of change in NREM respiration rate over time
for each stimulus condition. The main effects for minute [F(4,323) = 0.36] and the minute x stimulus pattern interaction [F(8,323) = 0.51] were not significant.
Analysis of simple main effects showed no significant
differences in the respiration rate over the 5 min during
presentation of the regular stimulus [F(4,79) = 0.65],
or during presentation of the random stimulus [F(4,39)
= 0.49]. These results indicate no significant delay in
the onset of the effect, despite the apparently smaller
effect in the first minute, suggested by Fig. 1. The results
suggest no significant habituation to the stimulus over
the 5-min period.
Discussion
The results corroborate the findings of Study 1 and
further indicate that an appropriate auditory stimulus
Sleep, Vol. 14, No.3, 1991
needs to be neither faster than the intrinsic breathing
rate, nor regular to increase the respiration rate. These
findings are consistent with an arousal model or a partial entrainment model of respiratory modification, but
clearly indicate that full entrainment with the stimulus
is not important. No other signs of arousal due to the
presence of the stimulus were noted. This is consistent
with previous literature (14) indicating that for human
children (mean age = 10.3) loud stimuli (mean = 105
dB sound pressure level) were necessary to cause even
partial or momentary arousal. Furthermore, the results
indicate that the modification of the respiration rate
happens quite quickly and is maintained for at least 5
min.
The present study showed that, consistent with previous observations of dogs (17), the respiration rate
during REM sleep was more rapid than during NREM
sleep. The consistency between the present respiratory
findings and previous studies using physiological (EEG,
EMG) determination of sleep state, the high interrater
agreement in the present study and the high level of
agreement for behavioral and physiological sleep phase
monitoring (20) offer multiple lines of support for the
validity of the behavioral sleep phase rating system
used. The qualitative recognition of respiration during
REM sleep as shallower and less regular than during
NREM sleep was also consistent with previous literature (17).
GENERAL DISCUSSION
These studies set out to examine the effect of auditory stimulation on the sleep respiration rate of infant
animals. The results show that the presence of a repetitive auditory stimulus tended to increase the sleep
respiration rate, irrespective of whether the stimulus
was faster or slower than the intrinsic respiration rate,
and regardless of the regularity of the stimulus. Introduction of a slower or irregular stimulus did not lead
to a reduction in the respiration rate of the sleeping
animal. The respiratory rate increased quickly after the
introduction of the stimulus. Habituation to the stimulus did not occur within the 5 min for which the
stimulus was maintained.
Three mechanisms that might account for such modification of the respiratory rate were proposed above.
These were 1) full entrainment in which the respiratory
pattern synchronizes with the auditory signal; 2) partial
entrainment, in which the animal breathes largely independently but the timing of some breaths is modified
by the auditory stimulus; or 3) arousal, in which the
auditory stimulus decreases the depth of sleep, resulting in an increased respiration rate. The results of the
present experiment are consistent with either the partial entrainment or the arousal explanation, but do not
AUDITORY STIMULI AND SLEEP RESPIRATION
support the wide role ofa full entrainment mechanism.
Behavioral observations indicated that the animals were
not aroused to waking by the stimulus. This is consistent with previous human research indicating that children are not easily roused to wakefulness by auditory
stimuli (14), and that arousal to wakefulness is not
necessary for a respiratory response to an auditory
stimulus (8,12). However, an indication that proportionately less REM sleep occurred when the auditory
stimulus was present may suggest that auditory stimuli
can alter the sleep state without necessarily rousing the
subject.
Regardless of the mechanism, the study indicates
that auditory stimulation may offer a technique for
increasing the respiration rate during sleep. The findings are consistent with the research reviewed by McKenna (12), suggesting that a variety of environmental
stimuli may alter the respiratory patterns of infants,
and that presence of the same environmental stimuli
may be associated with lower rates of SIDS. Auditory
stimulation is noninvasive and, in conjunction with a
suitable noninvasive respiration monitoring system,
could form a useful home-based hypoxia prevention
system for at-risk infants that may enhance the efficacy
of conventional apnea alarms. A system is envisaged
in which periods of apnea that were of duration shorter
than the alarm interval (e.g. lO-20 sec), such as might
occur during pathologically slow respiration or periodic breathing, would trigger the repetitive auditory
stimuli. Auditory stimulus presentation would continue until a short time (e.g. 2 min) after cessation of the
apneic periods. If an apnea was sustained beyond the
alarm interval, the alarm would be sounded, as for the
normal apnea alarm.
The present studies leave a number of questions unanswered. It has not been established that the same
results will be obtained from human infants. The appropriateness of the animal models to human infants
at risk for SIDS is controvertible (12). However, the
comparable effects demonstrated across two animal
species are promising.
The present study has used the respiratory rate as
the sole parameter of respiratory function. An increase
in respiratory rate may not correspond to a decrease
in hypoxia. The study could be extended by attention
to other respiratory physiological parameters.
Another question concerns the effect of stimulus presentation on the sleep cycle of the infant. Repeated
disruption of the sleep cycle could result if the stimulus
caused a change in sleep phase, and if the conditions
in a particular sleep phase (e.g. REM sleep) regularly
initiated presentation of the auditory stimulus. However, the risk of such disruption, if it were to occur,
needs to be offset against the benefit gained from a
reduction in chronic hypoxia.
247
In summary, the present experiment suggests than
an increase in the rate of respiration during sleep can
be achieved by auditory stimulation at a rate similar
to the respiration rate. This effect may be able to be
used to prevent infants from becoming hypoxic during
sleep, which may reduce their risk of mortality due to
SIDS. Further research is required to test the generalizability of the findings from the present model to
human infants at risk for SIDS and also to clarify further the effects of auditory stimulation during different
stages of sleep.
Acknowledgements: The authors thank Dr. Russell Gray
for his advice and assistance with the study design; Mr. and
Mrs. D. McNaughton for providing experimental subjects;
John Teppett, Dept. of Biomedical Engineering, Wellington
Hospital, for biomedical consultation; William van der Vliet,
for computer programming; and Barry Dingwall and his staff
for superb technical assistance.
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perspective. J Pediatr 1987; 110:669-78.
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