Journal of Comparative and Physiological Psychology

1962, Vol. 55, No. 1, 9-13

RESPONSE DECREMENT WITH REPEATED ELICITATION OF

HUMAN NEONATAL CARDIAC ACCELERATION TO SOUND1
ALEXANDER K. BARTOSHUK
Brown University

The human neonate's relatively poor neuro- be investigated by a sensory preconditioning

muscular development poses a serious barrier paradigm (Seidel, 1959) to determine how
to behavioral research which requires the S habituation to certain stimuli alters subsequent
to perform precise head, trunk, and limb conditioning to these stimuli.
movements. I t would be desirable, therefore, This brief outline suggests how physiological
to explore more extensively the usefulness of measures could provide objective response
physiological measures. A program could be measures for the study of some psychological
formulated to investigate some features of the variables in research on human neonates.
ontogenetic development of functions involving Within this general context, the purpose of the
the specific and diffuse projection systems in present experiment was to examine some
the human infant from birth onward. Ellingson factors which determine the degree of activa-
(1958), e.g., obtained diffuse blocking of tion produced in the human neonate by an
arousal responses in the human neonatal EEG. auditory stimulus. Intertrial interval was
Cardiac acceleration, which provides another chosen for study because this neglected vari-
possible indication of arousal, has been found able could help to clarify the -distinction
in human neonates stimulated with an between "fatigue" and habituation.
airstream (Bridger & Reiser, 1959). The Heart rate was selected as a response measure
relevance of arousal responses for psychological for this initial study because it met two prin-
studies may be illustrated by the experiment cipal requirements. Preliminary observations
of Sharpless and Jasper (1956). They inves- indicated that heart rate was probably one of
tigated how a brief auditory stimulus, initially the most reliable physiological measures
capable of arousing an adult sleeping cat, lost readily obtainable from the human neonate.
this ability when it was presented repeatedly The large (1 mv.) QRS complex of the electro-
at intervals which usually lasted several cardiogram occurs regularly, can be counted
minutes. Their data indicated that the habitua- readily even during limb movements, and the
tion of the arousal response occurred to the heart rate is independent of electrode resistance
experimental stimulus, but that other auditory or position. Surface electromyograms and
stimuli could effectively awaken the animal. EEGs are generally of low amplitude (e.g.,
Cortical evoked responses to an auditory below 75 m/x) and require special integrators
stimulus remained unaltered when arousal for adequate quantification. Respiration and
responses were habituated. Thus, habituation skin conductance measures from limbs are
of arousal apparently did not depend on subject to movement artifacts. Because studies
changes in the specific auditory pathways. which employ multiple physiological recordings
Hebb (1958) has noted that these data on might appear to capitalize on particular
habituation may represent some form of measures after the experiment, it was decided
learning phenomenon. This possibility could to select heart rate as the single most promising
1 measure for an initial study of stimulus effects
This investigation was supported by a Research
Grant No. 3-B-9019 from the National Institute of on the human neonate. Secondly, preliminary
Neurological Diseases and Blindness, United States observations revealed heart rates as low as 70
Public Health Service, to the Institute for Health beats per minute during sleep (inferred from
Sciences at Brown University as part of a National behavior and EEG) and as high as 175 beats
Collaborative Project investigating neurological defects
and their assessment in infancy. The author wishes to per minute during extreme excitement. Cardiac
express his thanks to G. L. Brooks, Director of the acceleration was elicited by auditory and
project at Brown, for his interest in and support of photic stimuli, as well as weak electrical
this research. The cooperation of the staff of the stimulation of a limb. These preliminary
Providence Lying-in Hospital and the assistance of
Allen Flaxman with collection of data are gratefully observations were the basis for the working
acknowledged. hypothesis that cardiac acceleration to sound
9
10 ALEXANDER K. BARTOSHUK

represents an arousal effect which may show compare the present test stimulus with tones of known
some of the properties of habituation reported intensity under the same recording conditions. The
voltage applied to the speaker in the present experiment
by Sharpless and Jasper (1956) in a completely produced an auditory stimulus 85 db. above the adult
different context. auditory threshold.
The specific objectives were to determine Electrodes were attached to each limb and the
whether (a) heart rate acceleration was reliably electrocardiograms were recorded from the three stand-
ard combinations of right arm to left arm, right arm
elicited by auditory stimulation of human to left leg, and left arm to left leg. The right leg was
neonates, (b) whether the cardiac response was grounded. Several tracings were taken simultaneously
related "to age and sex, (c) whether repeated on a Grass Polygraph. Paper speed was 1 cm. per second.
stimulation produced a response decrement, All heart rate measures were derived from the average
and (d) to study the effect of intertrial interval rate for the five beats immediately before stimulus.
onset or five beats immediately after termination of
on the response decrement as a means for the stimulus.
attempting a differentiation between "fatigue"
and habituation. Treatment of Data
The correlation between absolute heart rate change
METHOD and the heart rate immediately preceding stimulation
Subjects made it necessary to adjust statistically for differences
in prestimulus heart rate. Therefore the pre- and post-
All 5s were born at the Providence Lying-in levels were transformed into / scores and used to cal-
Hospital. They were clinic cases exclusively because culate a response measure (also expressed as a / score)
private patients were not available for this study. AH which partialed out the correlation between pre- and
infants were fullterm. Prematures and infants with postlevels. These t scores were essential for the statis-
known abnormalities were excluded. Two 5s were tical analysis of interindividual differences in responses
excluded because their electrocardiograms were tech- (Lacey, 1956). In order to analyze the response decre-
nically inadequate. Otherwise, infants were included ment from Trial 1 to 40, the regression line of heart
as they became available. rate response on prestimulus heart rate on Trial 1 was
used to calculate the expected response on Trial 40«
Experimental Design for each observed prestimulus heart rate. Differences
All 5s were tested individually at the Providence between predicted and observed responses were used
Lying-in Hospital in a room used solely for this study. to test the reliability of the response decrement. The
Intraindividual differences in heart rate responses were ratios of observed/predicted responses were used to
studied by presenting the same auditory stimulus 40 estimate the curves for the development of the response
times at regular intervals. The effect of the interval decrement across trials, expressed as percentage of
between stimuli was studied by using the intervals initial response. It should be noted that the regression
15, 30, and 60 sec. on independent groups of 40 5s lines for Trials 1 and 40 do not intersect at exactly
each. In order to study the variable of age, each of the the point of zero response. Consequently, the statistic
above groups of 40 5s had four subgroups of 10 5s "percentage of initial response" varies with prelevels.
who were 1, 2, 3, and 4 days old, respectively. Finally, However, for the group mean prelevels involved in
all subgroups of 10 5s consisted of five females and Figures 1 and 2, this source of error is less than 10%.
five males. In summary, there were 120 human neo- All levels of confidence are based on two-tailed tests.
nates allocated into subgroups so that there were
five 5s within each of the 24 conditions resulting from RESULTS
4 ages, 3 stimulus intervals, and 2 sexes. Each 5 was The mean cardiac acceleration of 11.3 beats
tested only in 1 session. per minute for 120 5s on Trial 1 and the
Apparatus and Procedure negative correlation of —.54 between response
and prelevel were highly significant (p < .001).
The pulses emitted from the synchronization circuit
of the Grass Photic Stimulator were amplified and
The standard deviation of responses was 9.1
used to activate a speaker placed 18 in. above the beats per minute, which is high because of the
infant's head. A 1-sec. train of 50 clicks per second correlation between response and prelevels.
was presented manually at equal intervals. Onset and Some of the mean heart rates immediately
termination of the stimulus were indicated auto- preceding stimulation are shown in Table 1.
matically on the polygraph by recording the syn-
chronization pulses from the stimulator. Although The standard deviation of prelevels was
duration of the stimulus was controlled manually usually about 16 beats per minute. It should
rather than automatically, the polygraph tracing made be added that the increase in prelevel from
it possible to anticipate termination of 1 sec. quite Trial 1 to 40 for the 15- and 30-sec. groups
accurately (usually within 0.1 sec). The same stimulus combined was greater (p < .05) than that for
intensity was used for all 5s. The present apparatus
could not be used to obtain an auditory threshold. the 60-sec. group.
However, after the experiment it was possible to Cardiac acceleration on Trial 1 was greater
 RESPONSE DECREMENT IN HUMAN NEONATES 11

TABLE 1
UJ
MEAN PRESTIMULATION HEART RATES ( B E A T S / M I N ) <
z /)
0
Q.
C/>
Trial Significance of trial UJ
comparisons <r
Group _i

l 2 40 Ti vs. Ti vs. 12 vs.

T2 T40 T40
<
t-

z
0-47 HOURS
15 sec. 122.7 130.4 129.5 .001 .01 u_
30 sec. 121.0 125.4 127.3 .05 .01 0 48-96 HOURS
60 sec. 121.7 127.6 120.6 .01 .05
All 121.8 127.8 125.8 .001
BLOCKS OF THREE TRIALS
FIG. 1. Effect of age on mean response decrement
than zero for each of the four age groups
curves for Stimuli 2 to 40.
studied. Equally significant (p < .001) was
the result of an analysis of variance which
showed a reliable effect of days, such that older
5s had larger responses. The effects of sex and
of days-by-sex interaction were not reliable.
Comparisons between individual days revealed
that responses on Day 4 were greater than
on any earlier day (p < .01); similarly,
responses were greater on Day 3 than on
Days 2 or 1 (p < .05); Days 1 and 2 did not
differ from each other. Although these results
were based on / scores, reliable (p < .05) age
differences were found when we analyzed all
BLOCKS OF THREE TRIALS
possible pairs of 5s of different ages but with
FIG. 2. Effect of interstimulus interval on mean
identical prestimulation heart rates. A com- response decrement curves for Stimuli 2 to 40.
parison of 13 such matched pairs revealed
larger responses on Day 4 than on Day 3; tionately large between Trials 1 and 2 and
another 13 matched pairs revealed greater very gradual thereafter. The response decre-
responses on Day 4 than on Day 2. ment from Trial 1 to 2 is reliable (p < .001)
The mean response for 120 6s to the fortieth and unrelated to age or stimulus interval. The
stimulus was an acceleration of 5.2 beats per subsequent gradual development of a further
minute (p < .001). This response was reliable decrement over trials from 2 to 40 is reliable
(p < .01) for the three subgroups with 15-, (p < .001) by an over-all test.
30-, and 60-sec. intervals. Responses observed
DISCUSSION
on Trial 40 were smaller than predicted from
the fortieth prelevel on the basis of the regres- The response decrement cannot be explained
sion line for Trial 1. The mean discrepancy readily by any gradual over-all reduction in
was 4.9 beats per minute (p < .001). More- activation level during the experiment because
over, 7 of 120 5s had identical heart rates mean heart rate was higher before the fortieth
before Stimuli 1 and 40, and therefore they than the first stimulus. Moreover, the response
did not require any statistical adjustment for decrement was present in 5s with identical
prelevel. These 5s also had less (p < .05) heart rates before the first and last stimuli.
cardiac acceleration on Trial 40. If the response decrement at 60-sec. intervals
When the response decrement across trials were due to neural fatigue or synaptic refrac-
was analyzed as percentage of initial response toriness, the 15-sec. interval would have
(see method for derivation), the response allowed less time for recovery and should have
decrement curves did not reveal any reliable produced a greater response decrement.
differences due to age (Fig. 1) or stimulus Although the response decrement might have
interval (Fig. 2). The development of the varied in this way had a wider range of inter-
response decrement appeared to be dispropor- trial intervals been used, the fact remains that
12 ALEXANDER K. BARTOSHUK

there was no such difference between 15- and tion (e.g., as illustrated by data of Brown,
60-sec. intertrial intervals. This and other Kalish, & Farber, 1951) are complementary
considerations indicate that the response aspects of a basic process whereby the arousal
decrement cannot be interpreted as due to effect of a stimulus is modified through
sensory fatigue. Apparently there are no data learning.
on human neonatal cortical evoked responses The response decrement findings necessitate
to sound. In the visual system, however, one further distinction. Sharpless and Jasper
Ellingson's (1958) human neonatal data show (1956) hypothesized two types of activation
that to obtain reliable serial cortical evoked reactions which they considered similar to
responses to flashes of light, it was sometimes Sokolov's (1954) distinction between the
necessary to use an inter-flash interval of 3 phasic and tonic forms of the "orienting
sec. or more. Our intervals of 15, 30, and 60 reflex." The phasic arousal reaction has a
sec. appear to be sufficiently long to minimize short latency, a brief duration which rarely
the likelihood of sensory fatigue. Moreover, outlasts the stimulus by more than 15 sec,
the stimulus intensity of 85 db. is not exces- and it is very resistant to habituation; con-
sively strong. With intervals of 15 and 30 sec, versely, the tonic reaction may last seconds
and adult 5s, Coombs (1938) invoked a central or minutes and habituates rapidly. The two
mechanism to account for adaptation of the normally occur together and are difficult to>
GSR to sound. Adequate control for fatigue distinguish except under special conditions,
in the receptor system is available in at least such as partial habituation when a phasic
one study which showed that acoustic habitua- reaction occurs without the tonic one. Brain
tion of arousal occurred without any reduction lesions can also differentiate the two forms of
in the cortical evoked response (Sharpless & activation. When the direct auditory innerva-
Jasper, 1956). They also obtained evidence tion of the thalamus was severed, the arousal
that the specificity of habituation of arousal to reactions to intense tones had long latencies
tones depends on the diencephalic and mes- and habituated rapidly. Conversely, damage
encephalic activating systems, and that the to the mesencephalic reticular system, which
cortex is not essential. An increase in stimulus leaves the sensory pathways to the thalamus
intensity produced dishabituation which argues intact, is associated with brief arousal only
against neural fatigue in the reticular forma- (Lindsley, Schreiner, Knowles, & Magoun,
tion. A more convincing argument against 1950). Habituation of arousal apparently has
fatigue is that after habituation to a standard not been studied in the latter preparation.
distribution of progressively decreasing fre- Nonetheless these data show that it is possible
quencies, the same frequencies and intensities to differentiate between phasic and tonic
but in reversed order produced dishabituation arousal. This distinction also appears to be
provided cortical auditory areas were intact relevant to our data on neonates who received
(Sharpless & Jasper, 1956). A related finding the stimulus once every minute. The response
with sleeping human 5s is that they showed immediately after the stimulus was reduced
E E G responses to a tape recording of their but still reliably present on the fortieth trial.
own name, except when played backwards, This agrees with the Sharpless and Jasper
and were less responsive to other names finding that the phasic reaction is resistant to
(Oswald, Taylor, & Triesman, 1960). These habituation. Conversely, the mean prestimulus
results support the hypothesis that habituation levels of the early trials increased and re-
of arousal involves some process or processes mained at a level reliably above the initial pre-
similar to those of learning phenomena. If it level. Later, by the fortieth trial, they had
can be shown that our neonatal data on a returned to the initial prelevel. In this case
response decrement across trials represent the prelevels are determined 58 sec. after the
previous stimulus and may be considered as a
similar habituation, this may provide the
test for a tonic arousal reaction. Our data,
means for studying some aspects of learning
interpreted in this way, agree with the con-
in the human neonate. Initially one could study
clusion of Sharpless and Jasper that the tonic
the extent that habituation to one stimulus is
arousal reaction habituates more readily than
generalized to other stimuli. Further research
the phasic one.
problems could be generated from the hypoth-
esis that habituation and conditioned activa- The finding that heart rate acceleration to
 RESPONSE DECREMENT I N HUMAN NEONATES 13

sound increased reliably during the initial by Trial 40 the prestimulus heart rate had
96 hr. after birth requires brief comment. This returned to the initial prestimulus rate, b u t
increased responsiveness with age resembles that the increase in the immediate response
the decrease in electrotactual thresholds with to sound was still reliable. These findings
age (Lipsitt & Levy, 1959). The parallelism appear to be consistent with the conclusion
of results in different modalities suggests that of Sharpless and Jasper (1956) that the tonic
we should not too readily attribute our results arousal reaction habituates more readily than
entirely to a gradual disappearance of amniotic the phasic one.
fluid from the middle ear (Zubek & Solberg, Because our response decrement curves
1954). An alternative hypothesis is suggested (Fig. 2) were similar for three interstimulus
by the demonstration that in adults electro- intervals, they cannot be attributed readily to
myographic reactions to sound were related neural fatigue. The possibility that the re-
to the prior activation level, as inferred from sponse decrement may represent some form of
E E G data (Bartoshuk, 1959). In the present learning is briefly considered.
study, after we partialled out interindividual
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