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Habituation of Heart Rate Response to Repeated Auditory Stimulation during the First

Five Days of Life


Author(s): Frances K. Graham, Rachel K. Clifton and Helen M. Hatton
Source: Child Development, Vol. 39, No. 1 (Mar., 1968), pp. 35-52
Published by: Wiley on behalf of the Society for Research in Child Development
Stable URL: http://www.jstor.org/stable/1127356
Accessed: 27-06-2016 11:58 UTC

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HABITUATION OF HEART RATE RESPONSE TO
REPEATED AUDITORY STIMULATION DURING
THE FIRST FIVE DAYS OF LIFE
FRANCES K. GRAHAM
University of Wisconsin
RACHEL K. CLIFTON
University of Iowa
HELEN M. HATTON
University of Wisconsin

10 newborns were stimulated for 5 successive days with a moderately


intense sound. They responded with rapid acceleration of heart rate (HR)
which returned to, but not below, prestimulus levels. Although the response
was more prolonged on early trials of the first day than on any later trials
or days, there was no significant intersession decrement. Rather, both
prestimulus HR and peak HR change, adjusted for prestimulus level, rose
significantly across days. Age controls showed that these changes were due
to age and not to the repeated stimulation. Some habituation did occur
within sessions. It was suggested that the relatively slow intrasession habitua-
tion and the absence of intersession habituation might be a function of the
type of HR response evoked.

Response decrement following repetition of a nonsignal, nonreinforcing


stimulus can be readily demonstrated in adult humans and infrahuman
organisms and has also been reported in newborns. This phenomenon is
usually termed "habituation," and several writers have suggested that it
should be defined as a simple form of learning not to respond to stimuli
that are without significance to the organism (Hebb, 1958; John, 1961;
Rosvold, 1959; Thorpe, 1963). Important considerations in the arguments

This research was supported by grants MH02011, HD01490, and K3-MH-21,


762 from the National Institutes of Health and by a postdoctoral Public Health
Fellowship to Rachel K. Clifton; computer services were provided through grant
FR00249 to the Biomedical Computing Division and a National Science Founda-
tion grant through the University of Wisconsin Research Committee. A portion of
the research was presented at the biennial meeting of the Society for Research in
Child Development, Minneapolis, March, 1965. F. K. Graham's address: Uni-
versity Hospitals, Madison, Wisconsin 53706.

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CHILD DEVELOPMENT

favoring a learning definition are that "habituation" can be distinguished


from sensory adaptation and neural refractoriness and that it can be shown
to persist over long periods of time. While these criteria have been met in a
number of adult and infrahuman studies, demonstrations of habituation in
the newborn have generally employed relatively brief interstimulus intervals
(ISI) and have measured changes only during a single session.
The present study measured heart rate (HR) changes in response to
an auditory stimulus repeated 15 times daily for 5 successive days.
Response decrements due to sensory adaptation and neural refractoriness
were ruled out by long ISI. Five to 10 seconds should be sufficient allowance
for the slower conduction time and longer refractory periods in newborns
(Ellingson, 1958; Scheibel & Scheibel, 1964), but longer intervals are
necessary in HR studies to avoid presenting a stimulus during the response
to a previous stimulus. Responses can apparently last as long as 20 seconds
with stimuli of 10 seconds (Chase, 1965). Still longer intervals are de-
sirable to maintain prestimulus levels approximately constant and thus to
avoid confounding changes in activation level with changes in response.
Since Bartoshuk (1962b) obtained significant increase in prestimulus levels
when using a 60-second interval, a 90-second interval was chosen for the
present study. However, 90 seconds proved to be unnecessarily long, since
prestimulus levels then decreased over trials. An interval of 75 seconds
might have been more nearly optimal, but no general rule can be stated;
optimal intervals undoubtedly vary depending upon the intensity, duration,
and other characteristics of stimulation.
Attention was paid to possible changes, over the 5-day period, in form
and duration of response as well as to changes in amplitude of response.
Late components were of special interest, first, because the adult response
apparently shows a late component that has not been observed in newborn
studies and, second, because there is evidence that late components habituate
more rapidly than early components and thus are more sensitive indicators
of a habituation process.
While a number of investigators have reported that the newborn HR
response is an acceleration, there have been no reports of deceleration
below prestimulus level following the initial acceleration. Such a diphasic
response of acceleration followed by deceleration has been found in adults
(Davis, Buchwald, & Frankmann, 1955; Geer, 1964; Lang & Hnatiow,
1962), and Lipton and Steinschneider (1964) noted its appearance in
infants by 23' months of age. Because newborn studies have generally
not used methods of measuring the response which could reveal late
components, it remains uncertain whether the relatively more mature
diphasic response is present in the newborn period or, if not present in the
newborn's earliest responses to stimulation, whether it would develop during
the course of several days of stimulation.
Late components were of interest, in the second place, because the

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GRAHAM, CLIFTON, AND HATTON

work of Sharpless and Jasper (1956) and Sokolov (1963) suggests that
tonic or long latency aspects of response habituate more quickly than
phasic or short latency aspects. This seems to be true whether or not the
long latency component differs qualitatively from the short latency compo-
nent. With the EEG alpha-blocking response, for example, decrement occurs
first at the end of the response and moves forward (Sharpless & Jasper,
1956). A similar phenomenon has been observed in habituation of an
accelerative HR response in dogs (Soltysik, Jaworska, Kowalski, & Radom,
1961) and in newborns (Keen, Chase, & Graham, 1965). In this latter
study, latency of onset of the acceleration response was unaffected by
repeated stimulation, but a reduction in the length of the response persisted
for 24 hours. The adult studies where a diphasic response occurred also
found that the later decelerative phase was the more susceptible to
habituation.

METHOD

Subjects
Twenty-six full-term newborns from the obstetrical service of the
University Hospitals, Madison, Wisconsin, served as Ss. The infants were
products of uncomplicated low forceps or spontaneous deliveries, and their
condition at birth was normal as judged by an Apgar score of 6.0 or higher
(Apgar, 1953). To obtain Ss for 5 consecutive days of testing, it was
necessary to restrict the sample to offspring of mothers who were residents
of a state juvenile home. This selective factor resulted in lower maternal
age (. = 16.8 years, s = 2.7 years) and more primiparae (N = 21)
than would be expected in a random hospital sample. There were 18
white and 8 Negro infants.
Thirteen other Ss were replaced because of apparatus failure (4);
early departure from the hospital (3); and crying, regurgitation, or move-
ment leading to illegible records (6). Infants were replaced if the record was
illegible for 10 seconds following any of the first three stimuli, on any two
consecutive trials, or on more than three trials of any session.
The 26 Ss were divided into an experimental group of 16 Ss and a
control group of 10 Ss, each group having equal numbers of males and
females. The experimental group was tested at approximately 24-hour
intervals on successive days beginning between 28.5 and 48 hours of age.
The total group of 16 Ss was available for three sessions, and 10 of these
Ss were available for an additional two sessions. The sessions were designated
Days 1 through 5, although average age was 37, 60, 84, 106, and 129
hours, respectively. Most of the data analyses are based on the 10 Ss
tested for 5 days. This subsample was composed of 6 males and 4 females,
and average age on Days 1 through 3 was 35, 58, and 81 hours. Subse-
quently, the 10 age-control Ss were tested on two sessions, corresponding to

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CHILD DEVELOPMENT

Days 3 and 5 of the experimental group. Average age on the first session was
84 hours and, on the second session, 130.5 hours.

Apparatus

The laboratory was an air-conditioned, quiet basement room with


temperature maintained at 76-78 degrees Fahrenheit. Stimulus onset and
offset, the EKG, and changes in thoracic circumference were automatically
recorded on a Gilson polygraph operated at a paper speed of 30 mm/sec.
Stimulus duration and ISI were controlled by Hunter timers. The stimulus
was a rough-sounding buzz of 300 p.p.s., with on-off time approximately
one to nine, produced by recording on tape the rectangular wave output
of a pulse generator. Stimulus intensity was 75 db. re 0.0002 dynes/cm2,
measured by a General Radio Type 1551-C Sound Level meter placed
at the site of the S's head. Resting sound level was 43 db. with equipment
operating. The EKG was detected by Welsh suction electrodes attached
1.5 inches apart on the midline of the chest. The respiration transducer was
a Parks Electronics 1-inch mercury strain gauge taped at the costal margin.

Procedure

Within 2 hours of the preceding feeding, an infant was transported


to the laboratory in a mobile crib, which also served as the testing unit.
The S was placed in a supine position, and limbs were swaddled to reduce
movement, a procedure shown by Lipton, Steinschneider, and Richmond
(1960) to reduce resting HR level without limiting the range of HR re-
sponse to stimulation. The Ss who became irritable during the session were
offered a pacifier in order to maintain a relatively constant state within the
course of a session.
Procedure was the same on all days and for both experimental and
control Ss. Recording of HR and respiration began 2 minutes before and
continued for 2 minutes after 15 stimulations with the 10-second auditory
stimulus. The ISI was 90 seconds from offset of one stimulus to onset of the
next. Ratings of the infant's state were also made before the first, sixth,
and eleventh trials. Two observers independently recorded amount of
vocalization, limb movement, and whether eyes were open or closed, and
then rated overall state on an eight-point scale.

Response Measurement

Heart rate.--The distance between every third R wave of the EKG


was manually read to the nearest half millimeter for 1 second preceding
and 20 seconds following stimulus onset. At a paper speed of 30 mm/sec,
the reading error was + 17 msec. The initial poststimulus cycle was defined
as the first R-R interval having more than one-half of its duration occurring

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GRAHAM, CLIFTON, AND HATTON

after stimulus onset. When stimulus onset bisected an R-R interval, that
interval was not included as either a prestimulus or a poststimulus cycle.
For each S on each trial, readings were transformed to average HR, in beats
per minute (bpm), during the first prestimulus second and during each of
the 20 poststimulus seconds. These data were averaged into three-trial
blocks, and the blocked data were used in statistical analyses and graphing.
State ratings.-The eight points on the overall state scale were de-
scribed as deep sleep, regular sleep, irregular sleep, drowsiness, alert in-
activity, alert activity, noncrying motor agitation, and agitated crying.
These were expressed as scores from 1.0 to 8.0, with deep sleep assigned a
score of 1.0. Scores of the two observers correlated .78 with one another and
were averaged to yield the final score.
Respiration.-These data were not analyzed. Efforts to find a relation
between HR and respiration were unsuccessful in an earlier experiment
(Chase, 1965).

RESULTS

Prestimulus Changes

Heart rate.-The general course of resting-level HR during the first


year of life is an abrupt drop immediately after birth with gradual increase
to about 3 months of age. At this time, rate begins to decline and continues
to do so until adult levels are attained at about 16 years (Ziegler, 1951,
pp. 18, 44). The present study indicates that significant changes occur even
within the first 5 days of life. Figure 1 shows a marked rise across days
on all trial-block curves. The curves are based on data from the 10 experi-
mental group infants tested for 5 days. Within each day, prestimulus HR
tended to decrease as a session progressed. An ANOVA on these data showed
that both the day and trial-block effects were significant (days F = 3.85,
error MS = 439.7; trials F =, 3.48, error MS = 49.9; df 4, 36; p < 0.5)
and that the linear component accounted for most of the variance (linear
days F = 11.18, p < .01; linear trials F = 6.61, p < .05). There were no
other significant trends or significant interactions.
In a comparison of Days 3 and 5 of the 10 control and 10 experimental
Ss, the same trends were present but neither the days nor trials effects were
significant. Of more importance, there was no significant difference between
control and experimental groups. Controls showed the same high prestimulus
rates as the experimental group, and the latter group's significant rise in
prestimulus level from Day 1 to Day 5 cannot, therefore, be attributed to
the repeated stimulations.
These findings caution experimenters that inclusion of newborn Ss
varying in age by only a few hours may necessitate control for an "initial
level" effect. The reasons for such marked change may be various. Weight
loss, recovery from the rapid drop in HR shortly after birth (Contis & Lind,

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CHILD DEVELOPMENT

140

..TB I

124- ..----TB
.... TB 53

I II I

I 2 3 4 5
DAYS

FIc. 1.-Prestimulus HR on five successive trial blocks (TB) and five suc-
cessive days (N = 10).

1963), and recovery from the effects of birth stress and depressant drugs
are among the complicating factors present during this period. It is also
possible that infants may gradually "wake up" and become more alert in the
days following birth.
State ratings.--Average State Ratings, by trial and by day, are given
in Table 1 for the 10 experimental Ss. An ANOVA showed a significant
change across trials (F = 12.90, error MS = .47; df 2, 18; p < .001)
but no significant trend across days. In agreement with the HR decrease
during each session, there was a corresponding shift toward greater drowsi-
ness in the course of single sessions, but there was no evidence for in-

TABLE 1
MEAN STATE RATINGS DURING EXPERIMENTAL SESSIONS
ON FIVE DAYs (N = 10)

PRECEDING TRIALS

DAY 1 6 11 MEAN

Day 1.................. 4.10 4.25 3.65 4.00


Day 2.................. 4.70 4.15 3.95 4.27
Day 3.................. 4.80 4.15 4.25 4.40
Day 4.................. 4.65 4.15 3.55 4.12
Day 5.................. 4.35 4.10 3.70 4.05
Mean................ 4.52 4.16 3.82

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GRAHAM, CLIFTON, AND HATTON

creasing wakefulness as infants grew older, at least during the periods rated.
The range of means is narrow; infants were typically in a state between
irregular sleep and alert inactivity.

Poststimulus Changes

HR response curves.-The average response on all trial blocks and days


was HR acceleration beginning within 2 seconds of stimulus onset. On the
majority of trials, acceleration began within the first second and reached a
peak by the fourth second, after which there was a decrease to approximately
the prestimulus level. The response is illustrated in Figures 2 and 3, which
show curves for three of the five trial blocks on Days 1 and 5, respectively.
Scores are plotted at the midpoints of the intervals they represent.
Although response curves occasionally dipped below the prestimulus
level, there was no significant HR decrease on any trial block of any day.
This was tested by t tests for significance of the difference between each
poststimulus second and the prestimulus second. All significant changes
were increases, and, with the exception of two trial blocks on Day 3, the
only significant changes occurred during the first 8 seconds.
It appeared from inspection of response curves that two characteristics
of the response might be changing across days or trials-duration of the
accelerative wave and amplitude of the peak acceleration. These character-
istics were therefore considered further.
Response duration.-To test the significance of any change in response

135

129 . ..
-127

125 TB I
. TB3
....... TB 5
123

.5 35 65 95 125 155 185

SECONDS
FIc. 2.-Second-by-second HR for 1 second preceding and 20 seconds fol-
lowing stimulation on three trial blocks (TB) of Day 1 (N = 10).

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CHILD DEVELOPMENT

144

14

14
00

138 6\
40 / 'of
. \

_ _ .

134 -.. \ : 0
-TB I
-----TB 3
13 ........TB 5

*.5 35 65 95 125 155 185


SECONDS

FIG. 3.-Second-by-second HR for 1 second preceding and 20 seconds fol-


lowing stimulation on three trial blocks (TB) of Day 5 (N = 10).

duration, the duration of the accelerative wave and the latency to peak
amplitude were measured. The latter score is analogous to the measure used
by Keen et al. (1965) but is expressed in seconds to peak amplitude rather
than in number of beats to peak. The duration score should be a more
sensitive measure, since it considers the time course of the full response.
A peak was defined as the fastest HR per second within a wave of
acceleration beginning not later than 3 seconds following stimulus onset
and ending when, after 2 successive seconds of deceleration, HR either fell
below the prestimulus level or reversed trend. Peak latency was the number
of seconds from the stimulus onset to the peak, and the duration score was
the number of seconds from the beginning to the end of the wave. Computer
programs were written so that these criteria could be assigned consistently,
and the computer output was checked against observer judgment to test
validity of the programs. In agreement with Lipton, Steinschneider, and
Richmond (1961), neither time measure was related to prestimulus level;
the regression coefficients equaled .00 in both cases.
There were no significant changes in either measure as a function of
trial blocks or days when response on all 5 days was analyzed. However,
the major response decrement occurred within the first few trials of the
first day, and inclusion of data from 5 days might be expected to dilute
the trend. Therefore, the variance in duration scores on Days 1 and 2 only
was analyzed, using the data of all 16 Ss tested on both days (see Fig. 4).
The main effect of trial blocks was significant (F =3.98, error MS =
7.94; df 4,60; p < .01) and was due to the expected reduction across

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GRAHAM, CLIFTON, AND HATTON

cr
S . DAY \

z
IoI I
6. DAY I

5.0

I 2 3 4 5
TRIAL-BLOCKS

FIG. 4.-Duration of acceleration response wave on five successive trial blocks


and 2 successive days (N = 16).

trials within each day. The interaction with days was not significant, how-
ever, and the data thus failed to replicate the Keen et al. experiment.
It should be noted that neither peak latency nor duration scores are
altogether satisfactory measures. Comparison of Figures 2 and 4 shows that
the average duration score of 9.25 seconds on the first trial block (Fig. 4)
is considerably shorter than 16.5 seconds, the duration of the wave obtained
by averaging HR at each second (Fig. 2). This may be due to the fact
that averaging cancels out sinus arrhythmia fluctuations in the group
curves, but the fluctuations remain as noise which cannot be separated
from response in the individual S curves.
Peak amplitude.-Because prestimulus HR varied significantly within
and among sessions and because peak response is dependent upon pre-
stimulus level, it was necessary to adjust peak scores for this effect. The
pooled regression coefficient was used to make the adjustment, since re-
gressions proved to be linear and to be homogeneous across trial blocks
and days for both the 10 experimental Ss and 10 control Ss (F = 0.99,
error MS = 32.42; df 34,280). The exact adjusting equation was adjusted
difference (AD) = D - (-.22) (X - 133.2) where D = peak HR -
prestimulus HR, -.22 = bDx or the regression of peak change on pre-
stimulus level, X = prestimulus HR, and 133.2 = X over all days and
trials. As is typical of both adult and infant data, the regression coefficient
reflected an initial level effect such that the higher the prestimulus HR,
the smaller the change in peak HR (e.g., Bridger & Reiser, 1959; J. I.
Lacey, 1956).

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CHILD DEVELOPMENT

Bartoshuk (1962b) reported increasing amplitude of response with


increasing age during the newborn period, and this was confirmed in the
present study (Fig. 5). An ANOVA using data for the 10 experimental
Ss on all 5 days showed a significant days effect (F = 10.59, error MS
= 30.54; df 4,36; p < .001) which was largely due to a linearly in-
creasing response amplitude across days (F = 19.55, error MS = 57.02;
df 1,9; p < .005). Habituation across trials within days, also reported by

ot
o-
L W
I I
I

0, 5..TB2I
"W" ._TB1
-TB3

D 1 ...TB4
.......TB85

S 2 3 4 5
DAYS

Fic. 5.--Adjusted peak responses on five successive trial blocks (TB) and
5 successive days (N = 10).

Bartoshuk, was not evident in a trials effect, overall, but was reflected in
the difference between trial block 1 and the remaining trials (F = 5.04,
error MS = 16.6; df 1,36; p < .05). Bartoshuk's data also indicated that
the greatest decrement in response occurred between the first two trials.
The absence of a significant days X trial blocks interaction suggests that
the course of habituation did not differ from day to day.
The increase in peak response across days is clear (Fig. 5), but it
might be due either to sensitization as a result of repeated stimulations or
to age alone. A comparison with the control Ss indicates that the increase
is a function of age and does not depend upon repeated stimulation. An
ANOVA on adjusted peak difference scores of the 10 control and 10 experi-
mental Ss on Days 3 and 5 showed no difference between the groups
(F = 0.75, error MS = 128.22), although there was the expected signifi-
cant effect of days (F = 5.31, error MS = 59.13; df 1,18; p < .05).

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GRAHAM, CLIFTON, AND HATTON

DISCUSSION

The typical newborn HR response to brief stimuli appears to be an


acceleration beginning within 2 seconds of stimulus onset and returning,
after a variable number of seconds, to approximately prestimulus levels.
This response has been found in a number of studies using a variety of
stimuli (e.g. Bartoshuk, 1962b; Bridger & Reiser, 1959; Davis, Crowell, &
Chun, 1965; Keen et al., 1965; Lipton et al., 1961). It differs from the
typical adult response in two respects; first, it shows no decrease below pre-
stimulus levels, and second, the period of acceleration is longer. Despite
efforts in the present experiment to measure the response in enough detail
and for a period long enough to assure detection of any decelerative com-
ponent, none could be demonstrated, either on initial trials or after 5 days
of stimulation.
This response does not appear to habituate to any marked extent.
No evidence of intersession decrement was found in the present study, al-
though previous work showed a significant reduction in response duration
which persisted from postnatal Day 1 to Day 2 and was due to a prolonged
response on the first trials of the first day; there was no difference among
responses on the remaining trials (Keen et al., 1965). Response in the present
study was also longer on trial block 1 of Day 1 than on subsequent trial
blocks or days, but it was less prolonged than initial response in the Keen
et al. study. It appears, therefore, that, while unusual prolongation of
response may be susceptible to intersession habituation, if a sufficiently
prolonged response does not occur on the first trials, no intersession habitua-
tion will be evident; once reduction of the prolonged response has occurred,
there appears to be no further change which persists across sessions.
It might be argued that any tendency for habituation to persist across
days is masked in newborns by the opposed tendency for increased alert-
ness. There is good evidence that the general state of the newborn does
change during the first few postnatal days. Change has been reported in a
variety of systems: skin conductance level (Kaye, 1964); electro-tactual
thresholds (Graham, Matarazzo, & Caldwell, 1956; Lipsitt & Levy, 1959);
olfactory thresholds (Lipsitt, Engen, & Kaye, 1963); sensori-motor and
visual responses (Graham et al., 1956); general activity and wakefulness
(Campbell, 1967; Irwin, 1930). The rising prestimulus HR of the present
study may also reflect a general increase in alertness. Although response
measures were chosen or adjusted to be independent of prestimulus level,
response could still be related to general state, since any prestimulus level-
state correlation would presumably be less than perfect. However, if there
were a state effect on HR response, it would be expected to reduce accelera-
tive changes rather than increase them (Lewis, Bartels, & Goldberg, 1967).
Thus, a habituation process should be exaggerated, not masked, by increased
alertness. In fact, the probability is small that state changes affected inter-
session HR changes in the present experiment, since, not only were response

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CHILD DEVELOPMENT

measures independent of prestimulus levels, but state ratings themselves


did not change across sessions.
Intrasession habituation did occur in the present experiment, but the
decrement in both peak amplitude and duration was small and was not
present on all days. Bartoshuk (1962a, 1962b) and Bridger (1961) have
previously reported within-session habituation of HR acceleration. Bridger
does not provide sufficient quantitative data to permit comparison, but
Bartoshuk found decrements, with ISI's of 15, 30, and 60 seconds, that are
within the range obtained in the present study. In the Bartoshuk experi-
ments, response on trials 12-14 was approximately 62 per cent of response
on the first trial; there was an additional decrement of about 10 per cent
after 40 trials. In the present study, response on trials 13-15 of Days 1
through 5 was 84, 55, 102, 74, and 69 per cent, respectively, of first-trial
response. While Bartoshuk obtained more pronounced habituation with a
6-second ISI, he indicated that interpretation of the effect was difficult be-
cause only on trial 1 was there a reliable response, and prestimulus HR on
subsequent trials was higher than on trial 1. As noted earlier, a 6-second
interval is probably too short to allow completion of a HR response. If a
stimulus is presented during response to a previous stimulus, little additional
response may be evident to the second stimulus.
If habituation is a form of learning not to respond, it might be
expected that newborns would show relatively slow and incomplete habitua-
tion. However, some newborn responses appear to habituate more rapidly
than HR. Eisenberg, Coursin, and Rupp (1966) reported that behavioral
responding, including body movements, grimacing, eye blinks, and so on,
completely ceased in 20-37 presentations of a patterned auditory stimulus
at 10-second ISI's. Engen and Lipsitt (1965) and Engen, Lipsitt, and Kaye
(1963) also found a marked reduction in activity and respiratory responses
with 10 repetitions of olfactory stimuli given at least 1 minute apart. In
the former study, the percentage of response was near zero to a "pleasant"
stimulus and around 35-40 per cent to an "unpleasant" one. In the latter
study, the percentage of response decreased to zero with one stimulus and to
less than 25 per cent with two other stimuli. More specific responses have
also been investigated. Wertheimer (1961) found complete habituation of
eye movements in response to click after 52 trials at eight trials per minute.
Bronshtein, Anotonva, Kamenetskaya, Luppova, and Sytova (1958) re-
ported that "most infants" required only four to five trials to habituate a
sucking-cessation response. Keen (1964) was unable to obtain such rapid
habituation but also found it difficult to elicit the response in any high
proportion of infants even on the initial stimulations.
It appears, then, that newborn HR responses show little or no inter-
session habituation and relatively slow intrasession habituation compared
to other newborn responses. An important question is how this compares
with habituation in adult subjects. While information on intersession change

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GRAHAM, CLIFTON, AND HATTON

is limited, that which is available suggests that adult accelerative responses


also fail to habituate across days (Galbrecht, Dykman, Rees, & Suzuki,
1965). This is in contrast to skin resistance changes (Davis, 1934; Galbrecht
et al., 1965; Montagu, 1963) and other responses (Thorpe, 1963). As regards
intrasession decrement, Graham and Clifton (1966) reviewed the evidence
showing that HR deceleration habituates rapidly, often within a few trials,
while HR acceleration is relatively resistant to habituation.
Viewed in this light, relatively slow habituation of HR responses in the
newborn might be due to the type of response evoked, that is, accelerative,
rather than to retardation in the habituation process per se. Why the re-
sponse should be typically accelerative is a question for which there may be
more than one answer, but any answer requires some hypothesis about the
difference between accelerative and decelerative responses. J. I. Lacey
(1959) has proposed that the direction of HR change is a function of what
might be called "receptivity requirements" of a situation, that is, whether
there is a need to limit or to enhance sensitivity to stimulation. He has
cited neurophysiological evidence that HR increase should be associated
with reduction in sensitivity and HR decrease with greater sensitivity
(J. I. Lacey, 1967; Lacey & Lacey, 1958). He has also offered evidence
from psychological experiments which involved relatively complex stimuli
(Lacey, Kagan, Lacey, & Moss, 1962; Lacey & Lacey, 1964, 1966).
Graham and Clifton (1966) concluded that studies of response to simple,
nonsignal stimuli further supported the hypothesis, and they suggested that
the Laceys' work could be reconciled with Russian investigations (Sokolov,
1963) by assuming that HR deceleration was a component of the "orienting
reflex" and HR acceleration a component of a "defense" or "startle" reflex.
Two recent studies provide additional confirmation (Chase, Graham, &
Graham, in press; Ginsberg & Thysell, 1966).
Assuming this functional distinction between accelerative and decel-
erative HR responses, three possible explanations for the common appearance
of accelerative HR responses in the newborn are considered: (1) neural
mechanisms for producing a decelerative orienting response may be in-
completely developed; (2) newborn thresholds for elicitation of acceleration
may be lower than adult thresholds; and (3) suitable conditions for evoking
decelerative responses may not have been provided.
An explanation in terms of neural development is speculative. It is
known that higher brain structures of the newborn are relatively less devel-
oped than lower brain structures but, unfortunately, the role of higher and
lower structures in controlling HR decelerative and accelerative responses
to sensory stimuli is not well understood. There are centers at medullary,
diencephalic, mesencephalic, and telencephalic levels which can affect HR
changes (Bard, 1960), but the pathways involved in particular responses
cannot be fully specified. However, if the functional distinction can be
maintained between a decelerative response associated with enhanced sen-

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CHILD DEVELOPMENT

sitivity, implying attention and active processing of stimuli, and an accelera-


tive response associated with protective reflexes, then control by higher and
lower brain mechanisms, respectively, would be compatible with general
functional-structural relations in the nervous system. The possibility that
reflex vagal responsiveness is relatively hypoactive in the newborn should
also be considered. However, evidence is conflicting. Lipton, Steinschneider,
and Richmond (1965) reviewed early autonomic functioning and indicated
that, contrary to some previous opinion, there is little evidence that either
sympathetic or parasympathetic systems are dominant in the newborn. On
the other hand, they reconsidered the question in a later paper (Lipton,
Steinschneider, & Richmond, 1966) and "leaned toward the hypothesis"
that vagal hypoactivity might be responsible for long HR acceleration in
the newborn.
Lower startle thresholds in the newborn may offer an additional
explanation of the accelerative response. While many newborn studies have
employed stimuli such as loud sounds and blasts of air which might evoke
startle at any age, this could not be sufficient explanation in itself, since an
identical stimulus can elicit deceleration in adults and acceleration in new-
borns (Chase, 1965; Rudolph, 1965). It would have to be assumed, there-
fore, that, if the accelerative HR response is part of a startle reflex, the new-
born has a lower threshold for startle. This is reasonable and is supported
by studies of behavioral startle (Landis & Hunt, 1939).
A third possibility is that newborns have not been tested either in a
sufficiently aroused state or with stimuli which would be most appropriate
for evoking deceleration. Newborns are frequently asleep or drowsy, and if
deceleration is associated with attention and requires the participation of
the higher nervous centers, the response should be difficult to elicit during
such states. There is some evidence for this. More frequent or larger
accelerative responses apparently do occur during sleep (Hord, Lubin, &
Johnson, 1966; Lewis et al., 1967), although it is not clear whether, with
prestimulus level controlled, the particular stimuli used can evoke de-
celeration in the waking state. In any case, stimuli suitable for eliciting
the "attention" of older infants or adults might be inappropriate with new-
borns. If, as suggested above, newborns have a lower threshold for startle,.
minimal criteria for studying "attention" responses should be the use of low-
intensity stimuli with gradual onsets.
Further experimentation is needed, therefore, before it could be con-
cluded that newborns are incapable of decelerative "orienting" responses
or of rapid habituation. It is possible that with an immature nervous system,
rarely capable of being fully aroused, the most easily elicited responses
are protective reflexes controlled by lower brain centers. Study of these is
important but, if more mature HR responses could be evoked under special
conditions, a new approach would be available for studying "higher"
functions in the neonate.

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GRAHAM, CLIFTON, AND HATTON

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