Developmental Psychology Copyright 1991 by the American Psychological Association, Inc.

1991. Vol. 27, No. 3, 432-439 0012-1649/91/$3.00

Infant Cardiac Activity:

Developmental Changes and Relations With Attachment
Carroll E. Izard Stephen W Porges
University of Delaware University of Maryland

Robert E Simons, Q Maurice Haynes, Ben Cohen

Christopher Hyde, and Maria Parisi State University of New York, Buffalo
University of Delaware

In this study the stability over thefirst13 months of life of measures of infant cardiac activity (heart
period and heart-period variability), their relations with each other, and their relations with a
continuous-variable index of infant-mother attachment were investigated. The indexes of cardiac
activity changed in an orderly way with development (increasing heart-rate variability, decreasing
heart rate). There were moderate to high intercorrelations among the cardiac measures, particu-
larly those indexing heart-rate variability (i.e., vagal tone, heart-period variance, and heart-period
range). Regression analyses showed that the measures of heart-rate variability at 3,6, and 9 months
were significant predictors of the continuous-variable index of security. The higher the infants'
heart-rate variability, the higher were their attachment insecurity scores. Analyses of whether the
conventional secure/insecure classification was related to the early infant cardiac measures indi-
cated that measures of heart-rate variability were significantly higher in the insecure children.

Recently, researchers have investigated the relation between
attachment classification and measures of temperament
(Belsky & Rovine, 1987; Bretherton, CConnell, &Tracey, 1980;
Miyake, Chen, & Campos, 1985). This research has demon-
strated a relation between concurrent measures of tempera-
ment and attachment and suggests that temperament, assessed
during early infancy, may be a reliable predictor of attachment
classification. For example, Miyake et al. (1985) reported that
infant irritability measured at 3 months of age was predictive of
patterns of resistant behavior during reunion in the strange
situation at 1 year. These findings suggest that temperament
may contribute significantly to the prediction of the quality of
attachment.
Neurophysiological processes may underlie the construct of
temperament and mediate aspects of the relation between tem-
perament and attachment. Contemporary theoretical perspec-
tives have conceptualized temperament as a psychobiological
construct (e.g., Goldsmith & Campos, 1982; Rothbart & Derry-
berry, 1981; Thomas & Chess, 1977). For example, Rothbart
and Derryberry defined temperament in terms of constitu-
tional differences in physiological reactivity and self-regulation
of reactivity. Thus, children's approach and avoidant behaviors,
observed in the strange-situation procedure (Ainsworth, Ble-
This research was supported by National Institute of Mental Health
Grant MH42O5OO3 to Carroll E. Izard and HD-22628 (National Insti-
tute of Child Health and Human Development) to Stephen W Porges.
Special thanks to Sharon L. Antonio, Michelle Claypool, Scott Lem-
pert, John Brown, Marion C. Hyson, Gail Chisholm, Teri L. Brown,
and Shannon Voirol for their assistance with this project.
Correspondence concerning this article should be addressed to
Carroll E. Izard, University of Delaware, Department of Psychology,
220 Wolf Hall, Newark, Delaware 19716.
432
har, Waters, & Wall, 1978), may be a manifestation of individ-
ual differences in physiological reactivity.
For the most part, investigations of physiological reactivity
have involved base-level measures of autonomic activity, partic-
ularly heart-rate patterns (i.e., heart rate, heart-rate variability,
and cardiac vagal tone). Such studies assume that baseline mea-
sures of heart-rate patterns convey information regarding stable
neurophysiological mechanisms potentiating autonomic and
behavioral reactivity. That is, it is assumed that the heart-rate
patterns reflect homeostatic mechanisms mediated by brain-
stem structures. It is also assumed that basal patterns of cardiac
activity index the organism's potential to react to stimulation by
transitory inhibition of homeostatic processes and to self-regu-
late by the reinstatement of homeostasis.
The specific central structures mediating both the auto-
nomic and behavioral dimensions of temperament have been
debated. For example, Kagan, Reznick, and Snidman (1987)
argued that heart-rate patterns reflect both sympathetic and
parasympathetic activity and that the relative contribution of
each can be detected through spectral analysis. In contrast,
Porges (in press) maintained that with current technology,
heart-rate patterns can be effective only in providing an index
of parasympathetic tone through the vagus. This view is sup-
ported by Saul, Rea, Eckberg, Berger, and Cohen (1990), who
demonstrated that heart-rate oscillations do not provide an ac-
curate measure of mean cardiac sympathetic activity.
Despite the different theoretical underpinnings of the re-
search programs, both Kagan and Porges rely heavily on beat-
to-beat variability in heart rate to mark individual differences
in temperament. Both would agree that heart-rate patterns are a
complicated and often idiosyncratic time series, with the beat-
to-beat pattern continuously influenced by the changing neural
influence from the brainstem to the heart.
There are two basic approaches to quantification of heart
 INFANT CARDIAC ACTIVITY
rate variability: (a) the use of descriptive statistics (i.e,, mean,
standard deviation, etc.), and (b) the modeling of the heart-rate
pattern to extract a component determined by a known physio-
logical mechanism (e.g., respiratory sinus arrhythmia). Exam-
ples of the descriptive approach would include Kagan's use of
heart-period mean and variability (Kagan et al., 1987) and the
attempts of Yen, Forsythe, and Hon (1973) to partition heart-
rate variability into two distinct components that emphasize
short-term (fast) and long-term (slow) variability. The short-
term variability is generally calculated as a standard deviation
or the mean absolute difference between sequential heart beats
and is assumed to be associated with vagal influences. Long-
term variability is generally calculated as the maximum heart
rate minus minimum heart rate (i.e., range) and is assumed to
reflect the balance between sympathetic and vagal influences.
To a limited degree, short-term variability has been demon-
strated to be related to vagal influences, but long-term variabil-
ity has not been empirically demonstrated to be related to spe-
cific sympathetic influences or to the vagus.
Porges (1985), on the other hand, has chosen to model the
heart-rate pattern to extract an accurate measure of the ampli-
tude of respiratory sinus arrhythmia as an index of cardiac
vagal tone (V). This method deals with the nonstationary quali-
ties of the baseline heart-rate pattern (a violation of an assump-
tion necessary for spectral analyses and time-domain niters),
the effect of the duration of data sampled, and the interactive
effects of sympathetic, parasympathetic, and endocrine sys-
tems on the heart. This method has been validated in numerous
studies across different laboratories (Billman & Dujardin, in
press; Dellinger, Taylor, & Porges, 1987; Jansen & Dellinger,
1988) and has been demonstrated to be associated with the
dimensions of temperament: reactivity, self-regulation, and ex-
pressivity (Field, Healy, Goldstein, Perry, & Bendell, 1988; Fox,
1989; Porter, Porges, & Marshall, 1988).
Although temperament dimensions have recently been
linked to both neurophysiological mechanisms and attachment
behaviors, the relations between physiological response pat-
terns and attachment has not been directly investigated. There-
fore, this study was designed to examine the stability of four
indexes of infants' cardiac activity (heart period, X heart-pe-
riod variance, and heart-period range) and to explore relations
among individual differences in these cardiac activity patterns,
assessed longitudinally (at 3,4,5,6, and 9 months), and attach-
ment behavior assessed in the Ainsworth strange situation
(Ainsworth et al., 1978) at 13 months.
Of special interest in our study is the developmental course of
the relations between heart-rate patterns and attachment.
Stifter, Fox, and Porges (1989), for example, have reported that
an early (5 months) measure of V was more strongly related to
expressivity than a later measure of V (10 months). In a similar
manner, as mentioned earlier, Miyake et al. (1985) found that
infant irritability measured at 3 months was predictive of resis-
tant reunion patterns in the strange situation at 1 year. Given
the strong association of V with both irritability/reactivity (Co-
hen, 1988; Healy, 1989; Porges, in press) and expressivity (Stifter
et al., 1989), our study is particularly concerned with early in-
fancy (3- to 4.5-month) measures of cardiac function and subse-
quent level of attachment security, although relations between
later (6-, 9-, and 13-month) heart-rate measurements and attach-
ment will also be assessed.
433
Method
Subjects
The infants were from White, middle-class families. Their mothers
were recruited from birth announcements in local newspapers to par-
ticipate in a longitudinal project on emotional development. Infants
involved in this study were seen periodically from 2.5 to 63 months of
age. Heart-rate data from this study were obtained during the 3-, 4.5-,
6-, 9-, and 13-month visits, and the attachment classification was ob-
tained during the 13-month visit. Eighty-eight mother-infant dyads
participated through the first year of the project, but because of the
difficulty in obtaining psychophysiological data free from movement
and recording artifact, the number of subjects represented at each age
were different.
Procedure
During the 3-, 4.5-, 6-, and 9-month visits, the session began by plac-
ing the recording electrodes on the infant and then escorting both
mother and infant into the experimental room for 4 min of heart-rate
recording. During these 4 min, the mother was asked to sit down and
hold the infant as quietly as possible. After the recording was com-
pleted , the electrodes were detached and the mothers were prepared for
subsequent mother-infant interaction procedures in which infant emo-
tion-expression data were obtained (those data are not part of this
report). During the 13-month visit, the heart-rate recording occurred
after the strange-situation procedure to preserve the integrity of the
standardized strange-situation assessment.
The strange situation. When infants were 13 months of age, the
Ainsworth strange-situation procedure (Ainsworth et al., 1978) was
used to provide a measure of quality of attachment. This standardized
procedure is composed of eight 3-minute episodes designed to assess
the quality of the child's attachment to the mother. The "strangers"
involved in this procedure were all White, female undergraduate re-
search assistants. They had been specially trained in using standard-
ized instructions.
The play area for the strange situation was a 2.7 X 2.7 m carpeted
section of a room, with (standardized) toys in the middle of the play
area. This area was separated from the rest of the room by one Plexi-
glas barrier 65 cm high (with a door for mother's entrance and exit) and
two wooden barriers, each 125 cm high. A window-sized two-way
mirror in one wall enabled videotaping of the session. Mother sat in a
chair toward the left side of the play area, while the stranger entered
and sat on the right side.
The strange-situation procedure was videotaped by two Panasonic
WV-34R black/white cameras; one recorded a wide-angle view of the
entire play area and the other recorded close-ups of the child's face. A
digital counter, measuring time in tenths of a second, facilitated video
synchronization as well as precise coding of other behaviors. A micro-
phone attached to the ceiling above the play area recorded vocaliza-
tions from child, mother, and stranger.
Attachment classification. The child's behavior during the strange
situation was coded using the standardized method developed by
Ainsworth et al. (1978). A judgment was then made based on the num-
ber and intensity of certain behaviors (such as proximity- and contact-
seeking behavior, contact-maintaining behavior, resistant behavior,
avoidant behavior, search behavior, and distance interactions) as to
whether the child demonstrated a secure (B) or insecure attachment (A
or C) to the mother.1 A secure child (B) responds positively to the
1
Our primary coder was trained by Dante Cicchetti during a sum-
mer at Harvard University. Our other coders were trained by the pri-
mary coder, and they also obtained reliability with precoded tapes
supplied by Everett Waters of State University of New York at Stoney-
brook.
434 IZARD, PORGES, SIMONS, HAYNES, HYDE, PARISI, COHEN
mother, seeking and maintaining contact with her, as well as receiving
comfort at reunion. Type B children exhibit little or no resistant behav-
ior and are able to use their mothers as a 'secure base' from which to
explore the environment. Insecure/avoidant children (A) show little or
no tendency to seek proximity or contact with mothers, even during
reunion episodes. Type A children may ignore mothers or exhibit more
salient avoidant behaviors such as turning away, looking away, or with-
drawing from mothers. Type A children typically demonstrate few
search behaviors and little or no distress at separation. Insecure/resis-
tant children (C) tend to display angry resistant behaviors toward their
mothers. Type C children demonstrate limited exploration of their
surroundings, and they are difficult to soothe after separation. Sixteen
infants were classified independently by two coders. They agreed on 14
of 16 (88%) of the cases.
Heart-rate recording and quantification. To obtain the heart-rate
measures, an electrocardiogram was recorded by placing three Med
Associates 4 mm Ag-AgCl disposable electrodes on the infant's chest
(left lowerribcage, right lower rib cage, and under the left clavicle). The
EKG was amplified with a Grass Model 7D Polygraph via a 7P4
preamplifier. Polygraphic output was continuously monitored
throughout the 4 min to detect movement artifact. The EKG was
stored on analog tape on a Vetter Model C-4 FM tape recorder for
subsequent off-line analysis on a PDP11/23 laboratory computer. The
computer (a) detected the peak of the R-wave for each cardiac cycle and
(b) timed the interval (heart period) between successive heart beats to
the nearest msec. The data file of successive heart periods for each
subject was manually edited for artifact and analyzed for mean heart
period, Y heart-period variance, and heart-period range using soft-
ware based on the Porges algorithms (Delta-Biometrics, Bethesda).
The procedures for estimating V (Porges, 1985) consist of the follow-
ing steps: (a) The heart periods were converted into time-based data by
sampling during successive 250 msec intervals; (b) the time-based data
were detrended with a 21-point moving cubic polynomial to remove
the influence of non-stationarities in the trend and slow periodicities
on the amplitude of respiratory sinus arrhythmia; (c) the detrended
data were processed by a digital band-pass filter to remove sources of
variance outside the frequency band characteristic of spontaneous
breathing for the infant (.24 to 1.04 Hz or approximately 15 to 60
breaths/min); and (d) the natural logarithm of the band-passed vari-
ance was calculated and used as the measure of cardiac vagal tone or V
Heart-period variance was calculated as the natural logarithm of the
variance of all heart periods within each 30-sec epoch. Heart-period
range was calculated as the maximum heart period minus the mini-
mum heart period within each 30-sec epoch.
To increase the statistical stability of V and the other cardiac mea-
sures (heart period, heart-period range, and the natural logarithm of
heart-period variance), values were calculated for sequential 30-sec
epochs, and the mean of these epochs within the 4-min baseline condi-
tion were used in the statistical analyses. Heart-period variance and
range measures are greatly influenced by the duration of data being
analyzed, and when calculated over longer epochs, they are influenced
by slower heart-rate trends. Thus, the calculation of variance or range
over 30 sec is usually different than over a 4-min period. The partition-
ing of the 4-min data collection period into 30-sec epochs functions to
filter some of the slow heart-rate activity that may contribute to vari-
ance and range. Therefore, our measures of range and heart-period
variance may not be generalizable to other reports in which these mea-
sures were calculated over longer intervals. Moreover, because the
slower heart-rate activity is not clearly vagal and reflects interactions
with the sympathetic nervous system, its removal reduces the non-
vagal influences on these measures. Thus, one would expect vagal
influences to be the primary contribution to all our measures of heart-
rate variability. Correlations of the heart-period variance and range
measures with the vagal tone index will enable the evaluation of the
vagal contribution to these measures.
Results
Cardiac Activity: Developmental Trends
Table 1 contains data for the four cardiac measures (X heart-
period [HP] variance, HP range, and mean HP) recorded dur-
ing thefivelaboratory visits (at 3,4.5,6,9, and 13 months). The
first column of means and standard deviations is for all subjects
with cardiac data at each age. The second column of means and
standard deviations is for the 25 subjects whose cardiac data
were intact for all five visits. As the table indicates, the data
from the subset of 25 subjects with complete data are quite
similar to the data set for the entire sample.
To assess statistically the changes in cardiac activity that oc-
cur with development and not dilute the potential influence of
stable individual differences on the developmental trends, the
data for each cardiac index from the 25 subjects with complete
cardiac data were subjected to a repeated-measures multivar-
iate analysis of variance (MANOVA) to explore changes in car-
diac activity as a function of age. The effect of age was signifi-
cant for all four cardiac measures. V:F(4,96) = 12.86,p<.001;
HP variance: F(4, 96) = 8.88, p < .001; HP range: F{4, 96) =
11.33, p < .001; and mean HP: F(4, 96) = 22.25, p < .001, all
increased from the 3-month to the 13-month visit. Age-related
increases in the first three indexes reflect developmental in-
creases in heart-rate variability; the increase in mean HP indi-
cates an age-related slowing of heart rate. For the first three
measures, there was no significant change between 3 and 4.5
months, yet the data recorded at each subsequent age were sig-
nificantly different from the average of all previous ages (reverse
Helmert contrasts; Finn, 1974, pp. 228ff). The effect of age on
mean HP was associated with contrasts revealing no significant
differences between the 3- and 4.5-month visits, followed by age
differences indicating significant heart-rate slowing through
the 13-month visit.
Stability of the Cardiac Indexes
Table 2 shows the intra-index stability (the correlation of each
cardiac index with itself) for each combination of age points. As
the data indicate, early measures of V (3 and 4.5 months) were
related to all subsequent measures of V Five of the cross-age
correlations for V were significant, whereas only two were signif-
icant for HP variance, one for mean HP, and none for HP range.
Relations Among Cardiac Indexes
Table 3 shows the inter-index correlations among the cardiac
indexes for all subjects who had complete cardiac data at 3 and
4.5 months of age and the corresponding matrix for ages 6 and 9
months. As the table indicates, there were high inter-index
correlations among the three indexes of heart-rate variability (Y
HP variance, and HP range) within each age level.
Cardiac Activity and Attachment Security
Of the 54 children with heart-rate measures at 3 and 4.5
months (early infancy) and an attachment classification at 13
months, 40 children were securely attached (B) and 14 children
were insecurely attached: 8 insecure/avoidant (A) and 6 inse-
cure/resistant (C). To obtain a continuous index of the level of
 INFANT CARDIAC ACTIVITY 435
Table 1 with a significant F change (p < .021) was V at 3 months. With
Means and Standard Deviations on All Subjects at Each Age the probability for eliminating a variable set at. 16, HP at 4.5
and on 25 Subjects with Cardiac Data at All Ages months was retained in thefinalequation, p< .15. Both V and
HP were positively correlated with attachment insecurity
N = 25 scores.
Cardiac Age A similar regression analysis for the cardiac indexes at 6 and
measure (in months) N M SO M SD
9 months yielded R = .51, F(3,32) = 3.69, p< .022. HP variance
Vagal tone 3.0 86 2.53 .80 2.51 .72 at 6 and 9 months and heart-periodrangeat 6 months produced
4.5 83 2.76 .81 2.67 .50 significant F changes. HP variance and range were positively
6.0 58 2.96 .93 3.07 .99
9.0 54 3.49 .81 3.51 .85 correlated with level of attachment insecurity.
13.0 47 3.61 .76 3.62 .73 A stepwise regression with backward selection was used to
HP variance 3.0 86 5.19 .65 5.24 .63 test the concomitant relation between the four 13-month in-
4.5 83 5.22 .72 5.21 .46 dexes of cardiac activity and the 13-month attachment security
6.0 58 5.56 .91 5.74 1.00 (discriminant function) scores yielded R = .30, F(i, 44) = 4.39,
9.0 54 5.87 .54 5.90 .53
13.0 47 5.98 .60 5.98 .52 p < .042. HP variance produced the only significant F change.
HP range 3.0 86 62.29 18.38 64.96 18.25 MANOVAs were used to examine the relations of the conven-
4.5 83 65.02 21.23 64.00 15.79 tional qualitative categories of secure and insecure attachment
6.0 58 72.23 20.68 73.93 19.08 (independent variable) to the cardiac measures (dependent vari-
9.0 54 84.47 19.11 84.78 19.05
13.0 47 87.00 18.95 88.22 17.68 able). In the MANOVA for the 3 and 4.5 month data, the multi-
Mean HP 3.0 86 392.83 29.01 393.84 22.00 variate effect approached significance, Wilks's X = .757, F(S,
4.5 83 395.86 25.22 397.46 20.92 45) = 1.81, p < . 10. The univariate FsQ, 52) for V at 3 and 4.5
6.0 58 408.09 24.89 411.10 24.47 months, and HP variance at 3 months were significant, ps <
9.0 54 423.63 23.82 423.98 21.73 .036, .004, and .030, respectively. The insecurely attached group
13.0 47 446.76 34.93 449.91 39.53
had higher means on V and HP variance than did the securely
Note. HP = heart period. attached group. The results of the MANOVA for the cardiac
indexes at 6 and 9 months were nonsignificant. The MANOVA
for the 13-month cardiac indexes revealed a nonsignificant
attachment security, all the attachment classification data from multivariate effect. For HP variance there was a significant uni-
the parent project (N = 81; Bs = 59, As = 12, Cs = 10) were used variate effect, F(\, 44) = 4.51, p < .039. However, all the univar-
in deriving discriminant function scores for each infant. For iate analyses for the secure/insecure groups must be treated
this purpose, the insecure subgroups (A and C) were combined. with caution because the multivariate effects were not clearly
Following a scheme described by Richters, Waters, and Vaughn significant.
(1988), we used ratings on selected interactive behaviors (prox- MANOVAs were also run to evaluate possible differential
imity seeking, contact maintaining, contact resistance, and relations of attachment types A (insecure/avoidant) and C (inse-
proximity avoidance) and frequency of crying in Reunion Epi- cure ambivalent/resistant) to cardiac functioning.2 The results
sodes 5 and 8 as independent variables in a discriminant func- were generally similar to those just described for the secure/in-
tion analysis to distinguish secure and insecure infants (as clas- secure dichotomy, except in the case of the data at 3 and 4.5
sified by the coders). We obtained a single discriminant func- months, where there was a significant multivariate effect,
tion, \ = .393, F(9, 71) = 12.17, p < .0001, that correctly Wilks's A = 1.96, F{\6, 90) = 1.96, p < .025, and a significant
identified 95% (56 of 59) of the infants classified as secure and univariate effect for V at 4.5 months (p< .014). However, Tu-
86% (19 of 22) classified as insecure, for an overall success rate key range tests revealed no significant differences bejtween A
of 93%. The infants1 scores on the linear discriminant function and C infants on V or any of the other indexes of cardiac func-
were used as a continuous-variable index of attachment secu- tioning at any age. B infants could be differentiated from the A
rity. In the distribution of security scores, the higher the score and C infants, but no differences in cardiac functioning could
the higher the likelihood the infant was classified as insecure. be discerned between the latter two groups described behav-
Because of our special interest in very early measures of car- iorally as insecurely attached. (See Table 4.)
diac activity and our need to maximize statistical power, the
efficacy of the indexes of cardiac activity at 3 and 4.5 months Discussion
and those at 6 and 9 months in predicting attachment security
was tested in separate regression analyses. The four cardiac The results generally confirmed our expectations. There were
indexes at 3 months together with the four indexes at 4.5 developmental changes over the first year of life for all four
months were regressed on the continuous measure of attach-
ment security derived from the behavioral ratings in the Strange
2
Situation at 13 months. The relatively large set of independent Examination of the distributions of the cardiac measures for at-
variables (k = 8) dictated the use of stepwise regression with tachment classes revealed no outliers. There were considerable nono-
backward selection to minimize capitalization on chance (Ap- verlapping areas in the distributions for the secure (B) and insecure (A
pelbaum & McCall, 1983). Residual analyses showed that the and C) infants. For example, for Vat 4.5 months, 71% of Bs had values
less than 2.86, whereas only 14% of Cs and 33% of As had values this
assumptions underlying regression were met and there were no
low. Nevertheless, these multivariate analyses of variance must be in-
outliers. The results of the stepwise regression were as follows: terpreted with caution because of the small cell size when the insecure
R = .35, F(2,51) = 3.63, p<. 034. The only variable associated group was split.
436 IZARD, PORGES, SIMONS, HAYNES, HYDE, PARISI, COHEN

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 INFANT CARDIAC ACTIVITY 437

measures of cardiac functioning. Of the four measures, V and

HP variance proved to be the most reliable and the best predic-
tors of attachment security.
X! The use of discriminant function analysis to derive a continu-
o ous-variable index of attachment security probably contributed
a to the detection of significant relations between this develop-
mental outcome measure and indexes of cardiac functioning.
Preliminary regression analyses with conventional attachment
r*1 —
u classes (either secure/insecure or A/B/C) as dependent variable
produced weaker results and failed to identify some of the car-
II diac indexes that proved significant in the analyses reported
m here. Regression analysis with a continuous rather than a cate-
gorical dependent variable is more robust because the underly-
ing assumptions are better satisfied. As indicated earlier, resid-
3 ual analyses with the continuous variable as criterion showed
that the assumptions underlying regression analysis were met.
o Furthermore, the continuous-variable index of security tends to
compensate for error in the clinical judgment that enters into
classification, particularly for marginal cases or in some of the
decisions between classifications Q and B4 or between A2
and B ( .
II
03
Developmental Changes in Cardiac Activity
The developmental changes in cardiac functioning were pre-
cisely as expected. All four measures of cardiac activity in-
creased with age (increasing X HP variance, and HP range re-
flecting increasing heart-rate variability, and the increasing HP
reflecting a slowing of heart rate). The age-related increases
manifested in the three indexes of heart-rate variability appear
o — — to be mediated, at least in part, by a maturational increase in
4 vagal tone (Porges & Fox, 1986). These developmental data,
therefore, are consistent with Porges's view that the vagal con-
II
u trol of the heart indexes individual differences in nervous sys-
£ tem capacity to mediate physiological and behavioral reactivity
II
(Porges, 1976, in press). The increase in heart-rate variability
parallels the normal developmental increase in the infant's ca-
pacity to self-regulate. As self-regulation approaches asymptote,
•3
heart-rate variability should become more stable and a more
reliable measure of individual differences.
Of all the cardiac measures, the vagal tone index appeared to
be the most stable (Table 2). However, the stability of the vagal
tone index or any other autonomic measures is dependent on
maturation. Stifter and Fox (1990) have reported that neonatal
5U
V is not related to subsequent developmental assessments, al-
though they reported significant relations between 5- and 14-
months V In the older child, Fox and Field (1989) have reported
test-retest correlations above .80 with preschool children re-
corded 6 months apart. In a similar manner, there are data
(S. W Porges, personal communication, July 1990) demonstrat-
ing significant relations in infants between 9 and 20 months
14 during baseline and during an attention-demanding task. For
the present data, assessed during baseline conditions, the aver-
X! S age of all 10 cross-age V correlations was .34, and the average for
Si the 7 cross-age correlations for V at 3 and 4.5 months was .39.
The other heart-rate variability measures were less stable than
V These findings are consistent with the literature.

Vagal Influences and Attachment Security

a u u B
31S The cardiac data demonstrate the following two points: (a)
CO u that all measures of heart-rate variability used in this study
438 IZARD, PORGES, SIMONS, HAYNES, HYDE, PARIS!, COHEN
reflect vagal mechanisms and (b) that greater vagal mediation
of heart-rate activity is a characteristic of the insecure infant,
regardless of the method of indexing attachment security The
methods used to quantify heart-period variance and range in
this study produced values that were highly correlated with the
validated vagal tone index. Regression analyses evaluating at-
tachment as a continuous variable and MANOY^s evaluating
attachment by the conventional three-group classification
scheme (i£., A, B, C) consistently demonstrated across the
various ages that infant measures of heart-rate variability are
related to attachment. The data demonstrated that insecure
infants, regardless of whether they were classified as A or C or
identified by high scores on the continuous-variable index, had
higher scores on heart-rate variability That V was the signifi-
cant predictor of attachment security at age 3 months, and HP
variance the significant predictor at 6 and 9 months, suggest
that there may be a shift from largely parasympathetic modula-
tion of HR variability in early infancy to a combination of
parasympathetic and sympathetic influences at later ages.
Heart-rate level measured with HP was not consistently re-
lated to attachment security. The only measure of HP that con-
tributed to the prediction of insecurity scores was that at 3
months when mean HP scores were higher (lower heart rates)
for As than they were for Bs and Cs. The contribution was
marginal (p< .15).
These results support the work of other researchers who have
found that infants' physiological and behavioral characteristics
affect their attachment status (Belsky & Rovine, 1987; Brether-
ton, O'Conneil, & Tracy; 1980; Miyake et al., 1985). Miyake et al.
found that infant irritability measured at 3 months of age was
predictive of resistant reunion patterns in the strange situation
at 1 year, a particularly important finding, given the strong
association of heart-rate variability and irritability/reactivity
(e.g., Porges, in press). In addition, Belsky and Rovine (1987)
have found temperament and possible autonomic activity dif-
ferences (tremulousness, amount of startle, and motor matu-
rity) between A,-B2 and B3-Q infants.
The meaning of the positive relation between heart-rate vari-
ability and attachment insecurity is not yet clear. The idea that
children with high heart-rate variability (in this case, V) are
more behaviorally reactive to distressing situations (DiPietro.
Larson, & Porges, 1987; Porter et al., 1988) is partially sup-
ported in that insecure/resistant (C) children have high heart-
rate variability, and it was type C infants who showed the great-
est amount of negative emotion in the strange situation (Shiller,
Izard, & Hembree, 1986). The idea is not supported by our
finding relating to msecure/avoidant (A) children. They had
higher heart-rate variability than secure (B) children at all ages
except 6 months, yet they also expressed significantly less nega-
tive emotion in the strange situation than insecure/resistant
children (Termine & Izard, 1989).
Since ambivalent/resistant (C) children have a long latency to
sooth and resume play during the final reunion episode (Ains-
worth et al., 1978; Shiller et al., 1986), their behavior might
contribute to the cardiac activity monitored at 13-months. How-
ever, the findings do not support this contention, because an
increase in physical activity (crying, clinging, resisting, and rest-
less behavior) following the strange situation and a break would
not produce the observed higher vagal tone. Rather, increased
metabolic demands associated with increased activity results in
lower vagal tone. Thus, any increase in motor activity would
result in an attenuation of V, suggesting that our estimate of V
forC infants was conservative. Our data showed astrong similar-
ity in the level of the vagal tone index in the two insecure
groups.
Although it is only speculation, it is plausible that avoidant
(A) children react physiologically but suppress negative emotion
expressions as an early coping mechanism (Ainsworth et al.,
1978; Main & Weston, 1982; Izard, 1990). When nonhuman
primate infants were separated from their mothers, some
showed no overt behavioral reactions but had markedly in-
creased cortisol levels, a physiological measure of stress
(Suomi, 1987). Observers might have concluded that these in-
fants were not distressed, but physiological data indicated oth-
erwise. Avoidance behavior has been conceptualized as an
adaptive reaction of A children that allows them to maintain
control over potentially disorganizing and distressing experi-
ences (Main & Weston, 1982).
Our findings relating to avoidant (A) infants indicate that
they have a relatively high level of parasympathetic tone. This
high parasympathetic tone may be related to autonomic reactiv-
ity and subjective experience, yet they express relatively little
negative emotion under the stressful conditions of the strange
situation. In this regard, avoidant (A) infants differ from both
secure (B) and insecure/resistant (C) infants in the manner in
which they regulate emotion or respond to autonomic activity
Recent studies with hospitalized patients suggest that some
young children have a style of emotion regulation similar to
that of avoidant infants (Knight et al., 1979; Siegel, 1981). Never-
theless, all our speculation regarding A-C differences in the
relations between autonomic function and affective expression
must be regarded as highly tentative because of the small num-
ber in each of these classes.
The widely held view of temperament as a psychobiological
construct reflects the belief that differences in physiological
processes (i.e., sensory thresholds and reactivity) may be re-
flected in individual differences in behavioral reactivity. Our
results provide evidence of a link between physiological pro-
cesses and the behaviors that index infant-mother attachment.
The evidence indicating that psychobiological factors contrib-
ute to the development of the infant-mother attachment is in
accordance with the findings of a number of temperament re-
searchers (Campos, Barrett, Lamb, Goldsmith, & Stenberg,
1983; Chess & Thomas, 1982; Kagan, 1982). Future research
should be directed toward resolving the issues raised by these
findings and developing a more complete understanding of
how the concepts of heart-rate variability, attachment, and tem-
perament are interrelated.
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Received January 20,1990
Revision received October 24,1990
Accepted October 24,1990 •