The Behavioral Arousal Threshold in Infant Sleep as a Function of Time and Sleep State

Author(s): Katalin Schmidt and Beverly Birns

Source: Child Development, Vol. 42, No. 1 (Mar., 1971), pp. 269-277
Published by: Wiley on behalf of the Society for Research in Child Development
Stable URL: http://www.jstor.org/stable/1127081
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 THE BEHAVIORAL AROUSAL THRESHOLD IN
INFANT SLEEP AS A FUNCTION OF TIME AND
SLEEP STATE

KATALIN SCHMIDT and BEVERLY BIRNS

Albert Einstein College of Medicine of Yeshiva University

SCHMIDT, KATALIN, and BIRNS, BEVERLY. The Behavioral Arousal

Threshold in Infant Sleep as a Function of Time and Sleep State. CHILD
DEVELOPMENT, 1971, 42, 269-277. In a group of 14 infants the behavioral
arousal threshold (BAT) for a cold thermal stimulus was found to be sig-
nificantly higher in the second quiet sleep epoch than in the first quiet sleep
epoch. This finding points to the importance of the time effect concerning the
BAT in infant sleep. The BAT in quiet sleep versus active sleep was not
significantly different for the same stimulus. The role of different modalities
of stimulation and individual differences as determinants of responsiveness
during neonatal sleep states is discussed.

Prior to 1950 the behavioral arousal threshold (BAT) in infant

sleep had been investigated either in relation to time elapsed since the
onset of sleep or in relation to activity level. Canestrini (1913) found that
the neonate is least responsive to stimulation 45-60 minutes after falling
asleep, while Wagner (1937) concluded that the baby sleeps "deepest"
when he is motionless and breathes regularly. These early sleep studies
did not recognize sleep states.
In 1955 Aserinsky and Kleitman described predictable recurrent
dual cycles of "rest-activity" during the course of sleep. This observation
has been confirmed by numerous investigators -and has been explored

This study has been supported by USPHS grant 5T1-MH-6418 and MH 11988-04.
The authors wish to express thanks to Mrs. S. Toscano and Mr. J. Ronch for carrying out
the statistical analysis, and to Dr. I. Mandel for statistical consultations. Fruitful discus-
sions with Dr. W. H. Bridger were most helpful. Thanks are also due to Mrs. Newton for
valuable technical assistance. Dr. Schmidt's address: Albert Einstein College of Medicine,
Department of Psychiatry, Bronx, New York 10461.
[Child Development, 1971, 42, 269-277. @ 1971 by the Society for Research in Child Development, Inc.
All rights reserved.]

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CHILD DEVELOPMENT

using physiological measures such as EEG, HR, respiration, EMG

(Dreyfus-Brisac 1966, pp. 286-306; Monod & Pajot 1965; Prechtl,
Akiyama, Zinkin, & Grant 1968; Roffwarg, Muzio, & Dement 1966).
At the present time, infant sleep is divided into active and quiet sleep.
Although no uniform behavioral or EEG definitions of the neonatal sleep
states have been reached so far, generally active sleep is characterized by
both rapid and slow eye movements, variable motor activity, increased
and uneven functioning of the autonomic nervous system, and a low
voltage, fast EEG pattern. Absence of eye movements, regular respira-
tion and heart rate, high voltage, slow or "trace alternant" EEG, and a
generally quiescent state characterize quiet sleep. The "rest-activity"
cycle thus consists of an active and a quiet sleep state. A feeding-to-
feeding sleep interval in the neonate usually comprises three to four such
cycles.
The development of physiological measures permitted the clarifica-
tion of the concept of sleep states and made it feasible to examine re-
sponsiveness during infant sleep as a function of both time elapsed since
onset of sleep and sleep states. The present study compared the BAT in
the neonate in the first, second, and third quiet sleep epochs to see the
effect of the time factor on responsiveness during quiet sleep. Also, an
attempt was made to compare responsiveness in quiet versus active sleep.

METHOD

The Ss were 14 full-term neonates from the nursery of the Bronx

Municipal Hospital Center ranging in age from 2 to 5 days. Testing took
place in a laboratory adjacent to the nurseries.
All Ss had Apgar scores of 9 or 10. In addition, Prechtl's neurological
examination was administered to exclude subjects suspected of CNS
damage (Prechtl & Beintema 1964). The infants were brought to the
laboratory just before the 10 A.M. feeding at which time they were awake
and crying. They were fed by the experimenters and kept awake during
the feeding. Immediately after feeding they were returned to their bas-
sinettes and allowed to go to sleep.
The sleep states were defined by behavioral observations. "Quiet
sleep" was defined as a 60-second interval during which there were no
eye movements and respiration was predominantly regular. A 60-second
period during which eye movements and irregular respiration were ob-
served was labeled "active sleep." Those 60-second periods fitting neither
description were labeled "intermediate." This behavioral classification
differed somewhat from the classification for quiet sleep of Parmelee,
Schulte, Akiyama, Wenner, Schultz, and Stern (1968) which requires
absence of motor activity in addition to regular respiration and absence

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 KATALIN SCHMIDT AND BEVERLY BIRNS

of eye movements. In agreement with other authors (Dreyfus-Brisac

1966, pp. 286-306; Roffwarg et al. 1966), the infant was considered to be
in quiet sleep even in the presence of occasional jerky limb movements
and rhythmical mouthing of low amplitude as long as the major criteria
of predominantly regular respiration and absence of eye movements
were met. However, to conform with the existing convention, the stimu-
lus was applied during quiet sleep only if the infant met the requirements
of Parmelee et al. (1968) 30 seconds prior to stimulation. Our classifica-
tion was used only to measure the length of sleep states. The stimulus
was not applied during active sleep periods containing gross body move-
ments because of the difficulty of assessing changes in activity level at
such times. During quiet sleep those 60-second periods with startles and
jerks were also excluded.
Prior to starting the experiment, 95 percent rater reliability con-
cerning the identification of the sleep states was established. The experi-
mental design was as follows: 4 minutes after the onset of the respective
sleep epoch a cold disk was placed on the Ss abdomen for 5 seconds. The
behavioral motor response was rated during the 5-second stimulus and
the 5-second poststimulus period. The interstimulus periods were alter-
nately 2 and 4 minutes. In case of startles, jerks, or gross body move-
ments the stimulus application was postponed until a 30-second period
devoid of such activities was obtained. The stimulus was applied four to
six times depending on the length of the sleep state.
The BAT was measured by the following response scale:
0 or NR. No response, no change compared with prestimulus level.
1. One jerky movement or a minimal increase of general activity.
?. A partial or full startle or a moderate increase in general activity.
3. A full startle and some additional evidence of awakening, or a large increase of general
activity.
4. Awakening and crying, but returning to sleep within 3 minutes.
5. Awakening and staying awake over a 3-minute period.

The qualitatively different motor patterns of the two states are

reflected in this response scale. Quiet sleep responses were jerky or
startle-like, while in active sleep the pattern of response was usually an
increase in general activity. This scale is analogous to that used by Birns
(1965). Two observers rated five Ss on these response measures to estab-
lish rater reliability. Reliability was significant at p < .001 when tested
against the null hypothesis that their interrater agreement equals 0
(z = 8.19) (binomial test [Siegel 1956]). The nine additional Ss were
rated by the first author only.
The cold disk was a quarter to which a handle had been soldered.
The handle was covered with rubber to avoid heat conduction from the
experimenter's hand. The disk was kept on ice between stimulus applica-
tions. The ice was kept in a large thermos to avoid temperature change.

271

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CHILD DEVELOPMENT

RESULTS

Several comparisons of the BAT were made. Responsiveness during

the first and second quiet sleep epochs was compared to see whether the
BAT was affected by the time factor, that is, by the time elapsed since
the onset of the feeding-to-feeding sleep period.
Table 1 presents the means of behavioral responsiveness during the
first and second quiet sleep epochs for all Ss and during the second and
third active sleep epochs for 12 Ss. Means were calculated by adding the
behavioral response values for a given sleep state and dividing them by
the number of the 5-second periods rated. There was a statistically signif-
icant difference in responsiveness between the first and second quiet
sleep epochs (Wilcoxon matched-pairs signed ranks test, T = 0.00,
p < .005, N = 14), the second quiet sleep being less responsive. The
overall means for these two sleep epochs were 1.82 and 1.01, respectively.
If the frequency of "no responses" obtained in these sleep states is
compared the difference is also significant (sign test, p = .006, N = 11).
The second quiet sleep contains a greater number of "no responses."
All Ss had an active sleep period prior to the first quiet sleep epoch.
These active sleep periods were short (mean 19.1 minutes, SD 8.42 min-
utes) compared with the successive active sleep epochs. Since the onset of
sleep could not be exactly determined, these are only approximate values.
Criteria for the onset of sleep in the present study were: eyes closed and
lack of periodic opening and closing of eyes. Thus, for most Ss the first
quiet sleep epoch began within the first half-hour of sleep, whereas the
second quiet sleep, which began after an intervening active sleep period,
took place during the second hour.
The importance of the time factor during the middle of the feeding-
to-feeding sleep period was examined by comparing the means of be-
havioral responsiveness during the second and third quiet sleep epochs.
This evaluation involved the selection of seven Ss who slept more than
3.5 hours and had four epochs of quiet sleep. In these seven Ss, the
second quiet sleep epoch took place during the second hour, while the
third quiet sleep began in the first half of the third hour. Table 2 presents
the means of behavioral response values during these sleep states. The
difference was not statistically significant (Wilcoxon matched-pairs
signed ranks test, T = 14.50, p > .05, N = 7). The overall mean for the
seven Ss for the second quiet sleep epoch was 0.98; for third quiet sleep,
0.92. Thus the time factor was decisive in determining the responsiveness
of an early quiet sleep epoch versus a quiet sleep epoch appearing toward
the middle of the feeding-to-feeding sleep period. However, for the
second and third quiet sleep epochs, both appearing within the middle of
the feeding-to-feeding sleep period, the time factor had a negligible

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CHILD DEVELOPMENT

TABLE 2
MEANS OF BAT DURING SECOND AND THIRD QUIET SLEEP EPOCHS

SECOND QUIET SLEEP THIRD QUIET SLEEP

No Re- Means of Number of No Re- Means of Number of

Ss sponse BRVa Ratings sponse BRVa Ratings

1......... 5 0.62 8 5 0.87 8

2......... 0 1.5 8 3 0.5 8
3......... 1 1.19 8 0 1.66 6
4......... 9 0.1 10 9 0.33 12
5 ......... 3 0.7 10 2 1.0 8
6 ......... 0 2.12 8 1 1.62 8
7 ......... 2 0.75 8 3 0.5 8

" Behavioral response values.

effect on responsiveness. Examining the effect of time on a final quiet

sleep epoch was not possible because of technical difficulties.
To determine the BAT difference between active and quiet sleep,
the BAT means of the second quiet sleep epoch were compared with the
BAT means of both the preceding and the following active sleep epochs.
The BAT means of these sleep epochs are presented in table 1. For this
evaluation 12 Ss who had four active sleep epochs were selected. Thus
none of the evaluated active sleep epochs were final active sleep epochs.
There was no significant BAT difference between active and quiet
sleep (Wilcoxon matched-pairs signed ranks test: for the second quiet
versus the second active sleep, T = 19.00, p > .05, N = 12; for the
second quiet versus the third active sleep, T = 23.00, p > .05, N = 12).
The overall means for 12 Ss were: second active sleep, 1.27; second quiet
sleep, 0.98; third active sleep, 1.13. There was no significant BAT differ-
ence between the second and the third active sleep epochs (Wilcoxon
matched-pairs signed ranks test, T = 30.50, p > .05, N = 12).
Since within a sleep epoch repeated stimulation of one modality was
employed, a test for the possibility of habituation or sensitization was
performed as described by Wilcoxon and Wilcox (1964, p. 11). There
were no significant trial differences within either the quiet or the active
sleep epochs (all p values > .05).

DISCUSSION

In the present experiment a significant difference in the BAT was

found for a cold thermal stimulus between the first and the second
quiet sleep epochs. Since the BAT in relation to both duration and state
of sleep had not been previously explored in neonatal sleep studies, it is

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 KATALIN SCHMIDT AND BEVERLY BIRNS

not known if this finding can be generalized for other modalities of

stimulation. However, the results of the present study suggest that in
the assessment of responsiveness during sleep not only state but temporal
factors should be considered. This finding is important in investigating
individual differences in sensitivity among infants and the effects of dif-
ferent modalities of stimulation during sleep.
Individual differences in responsiveness during sleep in early in-
fancy may have predictive value in terms of future personality traits.
Bergman and Escalona (1949) considered unusual sensitivity in infancy
as a possible presursor of deviant ego development. Birns (1965) found
stable individual differences in responsiveness during the first days of
life but did not analyze the data as a function of state. During the present
experiment it was noted that there was a considerable range of the BAT
among Ss within a given sleep epoch. During the second quiet sleep
epoch, for example, some Ss were relatively insensitive, while others
like Ss 2 and 6 exhibited a startle response almost every time they were
stimulated. It would be interesting to determine the consistency of indi-
vidual responsiveness during sleep and to see how it relates to the infants'
sensitivity during wakefulness.
In the present study the BAT in active sleep did not differ signifi-
cantly from the BAT in quiet sleep. However, no general conclusions can
be drawn concerning responsiveness of neonatal sleep states on the basis
of data obtained by using a single modality of stimulation. Hutt, von
Bernuth, Lenard, Hutt, and Prechtl (1968) and Wolff (1967) demonstrat-
ed that for auditory stimuli infants are significantly more responsive in
active ("irregular") than in quiet ("regular") sleep. However, Wolff also
found that painful or tactile stimuli did not produce differential respon-
siveness in terms of regular versus irregular sleep. Thus it appears that
the modality of stimulation is an important determinant of the neonatal
sleep state-arousal threshold relationship.
In the full-term neonate, characteristic peaks of the auditory evoked
responses (AER) diminish in magnitude during active sleep as compared
with quiet sleep (Akiyama, Schulte, Schultz, & Parmelee 1969; Weitz-
man, Fischbein, & Graziani 1965). In terms of behavioral responses the
reverse pattern has been found for the same modality of stimulation. An
explanation of the relationship of the AER and behavioral responses
would require a better physiological understanding of the evoked re-
sponses (Rechtschaffen, Hauri, & Zeitlin 1966). The presence of the
evoked potentials indicates the capacity of the brain to register external
stimuli, but the neurophysiological significance of these potentials has
not been fully elucidated.
A comparison of adult and infant sleep state-arousal threshold
relationships introduces a new factor which has been shown to influence
the results in the adult studies, that is, the response class chosen. Adult

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CHILD DEVELOPMENT

REM sleep is behaviorally a "deep" state if measured by the response of

pressing a microswitch in response to an auditory signal (Williams,
Hammack, Daly, Dement, & Lubin 1964), but it becomes a "light"
sleep state when for the same modality of stimulation the response class
chosen is full awakening (Goodenough, Lewis, Shapiro, Jaret, & Sleser
1965; Rechtschaffen et al. 1966).
There are inherent difficulties in using the same type of arousal
response for organisms of different levels of maturity. It would be very
difficult, for example, to use full awakening as the response to stimulation
in infant sleep studies. The neonate does not readily wake up even when
an intense stimulus is applied late in the course of sleep, and once re-
peatedly awakened does not easily return to sleep. Thus in all neonatal
studies discussed the response class measured was change in activity
level. Since the BAT of the sleep states as measured by one type of
response does not necessarily predict the BAT of the sleep states as
measured by another type of response, it is not possible to compare the
available results on infant and adult sleep state-arousal threshold
relationships.

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