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Bonny Donzella

Megan R. Gunnar*
William K. Krueger Cortisol and Vagal Tone
Jan Alwin
Institute of Child Development
University of Minnesota
Responses to Competitive
51 East River Road
Minneapolis, MN 55455 Challenge in Preschoolers:
Associations with
Temperament

Received 4 March 2000; accepted 27 June 2000

ABSTRACT: Sixty-one 3- to 5-year-old nursery school children participated in a study of tempera-


ment and stress responses to competition. Each child individually participated in a competition
against a familiar adult experimenter to determine who would win enough games to receive a prize.
After initially winning three games (Win Period), the children lost the next three games (Lose Period),
before winning the ®nal games and receiving the prize. Salivary cortisol, vagal tone, affect and turn-
taking behavior were measured in response to the competition and examined in relation to child
temperament using a teacher-report version of the Child Behavior Questionnaire. Behavioral
measures indicated that the procedures were emotionally engaging and the threat of losing was
aversive. Surgency (extroversion) was positively correlated with positive affect during Win periods
and tense/angry affect during the Lose period of the competition. Vagal tone decreased as the
children began to play against the adult and children who were more tense/angry while losing
showed additional suppression of vagal tone when they began to lose the competition. Most of the
children did not show a cortisol response to the competition; however, the 15% who increased
cortisol (responses >1 SD of classroom baselines) were described by teachers as more surgent and
lower in effortful control. All but one of these children who increased in cortisol was male. Cortisol
responsive children also displayed higher levels of tense/angry affect during the Lose period.
Surgent, extroverted children appear to be vulnerable to competition stress. ß 2000 John Wiley &
Sons, Inc. Dev Psychobiol 37: 209±220, 2000

Keywords: stress; temperament; cortisol; vagal tone

Temperamental differences in stress reactivity have behavioral problems of children (Boyce & Jemerin,
been argued to play a role in the physical health and 1990; Garmezy & Rutter, 1983; Jemerin & Boyce,
1990). In research on infants and young children, the
search for the stress reactive child has focused almost
*Correspondence to: Megan R. Gunnar exclusively on children who are shy, anxious, and fe-
E-mail: (gunnar@tc.umn.edu) arful (Biederman et al., 1993; Hirshfeld, Biederman,
Contract grant sponsor: National Institute of Child Health and
Human Development Brody, Faraone, & Rosenbaum, 1997; Kagan, 1994).
Contract grant number: HD16494 It is these children who are expected to have lower
Contract grant sponsor: National Institute of Mental Health thresholds for activating both sympathetic and neu-
Research Scientist Award (M.R.G)
Contract grant number: MH00946 roendocrine responses to novel, discrepant, and mil-
dly fear-eliciting events (Kagan, Reznick, & Snidman,
ß 2000 John Wiley & Sons, Inc. 1987). Evidence for the greater stress reactivity of
10982302, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S by Universitaet De Valencia, Wiley Online Library on [02/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
210 Donzella et al.

extremely shy, inhibited children is accumulating, surgent temperament is associated, at times, with
along with evidence that these children may be iden- greater cortisol responsivity, what has not been clear
ti®able early in infancy and that they may be at greater in the research on preschoolers is whether this is
risk for developing anxiety disorders (Rosenbaum because these children have a lower threshold to res-
et al., 1993; Schmidt & Fox, 1998; Schmidt et al., pond with elevated cortisol to particular situations. Or,
1997; Schmidt, Fox, Schulkin, & Gold, 1999). How- on the other hand, whether they tend to behave in
ever, not all of the research on infants and young ways that result in stressful social encounters or even
children is consistent with a focus on shyness or seek out stressful stimulation (Gunnar, Marvinney,
behavioral inhibition as the sole temperamental dispo- Isensee, & Fisch, 1988). The following study was
sition associated with stress vulnerability. This is designed to determine whether children who exhibit
particularly true in studies examining activity of the larger cortisol stress responses in reaction to a stressor
hypothalamic±pituitary±adrenocortical system in in- that they neither created nor sought are also more
fants and preschool children. surgent, extroverted children.
Maternal separation elevates cortisol, the hormone One theme that seems to unite the ®ndings des-
produced by the HPA system (Gunnar, Mangelsdorf, cribed above is that surgent children respond with
Larson, & Hertsgaard, 1989). While separation has more distress, frustration, or anger when they exper-
been viewed as a fear-eliciting stressor, increases in ience threats to their control over valued outcomes.
cortisol to separation do not correlate with parental Loss of control is known to be a potent stimulus of the
reports of infant ``distress to novelty'' (the scale that HPA axis in research on animals (Bohlin et al., 1985;
presumably re¯ects fearfulness), but rather with ``dis- Hanson, Larson, & Snowdon, 1976; Maier, Ryan,
tress to limitations'' (the scale that presumably ref- Barksdale, & Kalin, 1986). In research on adults,
lects anger and low frustration tolerance) (Gunnar, perceived control affects whether Type A coronary
Larson, Hertsgaard, Harris, & Brodersen, 1992). Ent- prone individuals experience heightened sympathetic
ering a new social group should be stressful for the and neuroendocrine responses to challenge, and thus
shy, inhibited child. However, in a study of 2-year-old are exposed to the combination of stress hormones
children beginning nursery school, shyness did not that might be the most damaging to the cardiovascular
predict rises in cortisol in the early weeks of school; system (Frankenhaeuser, 1979). Threats to control
instead, larger increases were noted for assertive, over valued outcomes might be expected to occur
aggressive children (de Haan, Gunnar, Tout, Hart, & frequently in preschool settings where children are
Stansbury, 1998). In a similar vein, studies of children exposed to the need to argue and negotiate over toys,
who are familiar with their peer group have repeatedly play themes, and activities (Laursen & Hartup, 1989).
found that larger rises in cortisol over the day and/or All such encounters would contain elements of
higher levels over days are noted for extremely sur- competition, which in studies of primate social groups
gent (e.g., extroverted, sensation-seeking) children has been identi®ed as an important source of stress
and those with poor self- or effortful control (Dettling, (Sapolsky, 1992).
Gunnar, & Donzella, 1999; Gunnar, Tout, de Haan, In the following study of preschool-aged children,
Pierce, & Stansbury, 1997; Tout, de Haan, Kipp- we examined whether competition that included a
Campbell, & Gunnar, 1998). period when the children were clearly at risk of losing
As with shy, inhibited temperament, a tendency to would produce elevations in cortisol for more surgent
approach novelty and seek sensation can be predicted children. In studies of adults, competition in the
from responses to stimulation early in infancy (Fox, context of sports and games has been shown to elevate
Henderson, Rubin, Calkins, & Schmidt, in press). cortisol (Suay et al., 1999). While elevations in stress
Children who later approach new situations and peo- hormones partly may be due to the physical exertion
ple with vigor, at 4 months of age tend to react with involved in many competitive sports, increases have
high motor activity and high positive affect to intense also been noted among coaches that appear unrelated
stimulation. This same stimulation elicits motor to physical exertion (Kugler, Reintjes, Tewes, &
activity combined with fussing and crying for infants Schedlowski, 1996). Individual differences in the
who tend later to be shy and inhibited. This type of magnitude of response to competition has been stu-
surgent, extroverted temperament is more stable over died in research on adults, with some evidence that
time than is shy, inhibited temperament (Fox et al., in larger increases are noted for individuals who are
press) and unless tempered by strong self-regulatory more emotionally engaged (Kugler et al., 1996).
abilities, is associated with aggressive behavior and Given this, we anticipated that surgent temperament
dif®culties in peer interaction by the early preschool might correlate positively with cortisol responses to
years (Rubin, Coplan, Fox, & Calkins, 1995). While challenge.
10982302, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S by Universitaet De Valencia, Wiley Online Library on [02/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Cortisol and Vagal Tone Responses 211

Experiencing the threat of potentially losing the preschool classrooms (4 morning, 2 afternoon classes)
competition was also expected to be emotionally cha- at a university laboratory nursery school. Only
llenging to children. Regulating behavior under these children pro®cient in English and without develop-
conditions might be expected to tax preschooler's mental delays, and emotional or behavioral problems
emerging emotion-regulatory abilities (Kopp, 1989). were asked to participate. A total of 73 children met
Effortful control has been hypothesized to be the these criteria of which 12 refused to participate. Based
dimension of temperament that in¯uences how well on teacher reports of child temperament (see below)
children can regulate behavioral and physiological children refusing to participate were described as
responsivity under conditions of high emotional shyer and sadder in temperament than those agreeing
challenge (Derryberry & Rothbart, 1997; Eisenberg to participate (shyness: M ˆ 3.3, SD ˆ 1.3 vs. 2.6,
et al., 1999). In previous research, we have found that SD ˆ 0.9; t (13.2) ˆ 1.77, p ˆ .10; sadness: M ˆ 3.9,
children who exhibit high cortisol levels in the SD ˆ .31 vs. 3.2, SD ˆ .67; t (31.2) ˆ 5.6, p < :01). Of
classroom are described by teachers and parents as those participating, there were 26 girls and 35 boys.
low in effortful control (Gunnar et al., 1997). Thus Most of the children were Caucasian (n ˆ 43), 11 were
effortful control, either directly or in interaction with Asian, and seven were Hispanic or of multi-racial
surgent, extroverted temperament might be related to heritage.
how intensely children respond to competition and the
threat of losing.
Procedures
In addition to neuroendocrine measures, stress
reactivity is also often studied using cardiovascular Two experimenters conducted all of the sessions.
measures (Al'Absi et al., 1997; Jemerin & Boyce, These experimenters participated in classroom activ-
1990; Lundberg, Westermark, & Rasch, 1993). Heart ities for several weeks to become familiar to the
rate (or conversely heart period) and indices of heart children. During this period, children were taken in
period variability have been used (Berntson et al., small groups on ``®eld trips'' to the testing room to
1997; Kagan et al., 1987). Of these, respiratory sinus familiarize them with the procedures and facilitate
arrhythmia or vagal tone, a measure that re¯ects the their informed assent. Part of the ®eld trip involved
parasympathetic input to the heart, has been measured demonstrating a small Nerf TM rocket that the children
in a number of studies of young children (Porges, would be allowed to launch if they participated in the
1992). Emotionally challenging tasks suppress chil- procedures and won the competition (see below). The
dren's heart periods (i.e., increase heart rate) and testing room was located within a few feet of the
vagal tone (Calkins, 1997). When restraint is used as preschool classrooms. The testing room was often
the stressor, larger suppressions in vagal tone are used for small-group activities and was a familiar area
noted for children who are more easily angered or for the children. Testing took place several months
frustrated (Calkins, 1997; Porges, 1996; Porges, into the school year. Thus, testing was performed once
Doussard-Roosevelt, Portales, & Suess, 1994). Thus, the children were familiar with the school, the setting,
in addition to measuring cortisol, we also measured the experimenters, and had been shown the events that
vagal tone. It was expected that children who exhi- would transpire.
bited signi®cant elevations in cortisol to the compe- While still in the classroom, the children were
titive game would be more surgent in temperament, asked individually if they wanted to play the games
perhaps less behaviorally regulated as indexed by the and get a chance to launch the rocket. Testing was
effortful control dimension of temperament, and more conducted during the freeplay period within 1.5 hr of
autonomically-responsive, as measured by suppres- the start of each nursery school day. Children were
sion of vagal tone, particularly during periods of the given an opportunity to decline participation on any
competition when it appeared that the child would given day. In many instances, children declined
lose. because they were already engaged in an activity that
they did not want to leave. They were allowed to do so
and were asked again on another day. If a child
declined repeatedly, the teacher was consulted. If the
METHOD teacher thought that the refusals might re¯ect anxiety,
the teacher offered to accompany the child to the
testing room. In several instances, children then
Participants
agreed to participate when the teacher walked with
The participants were 61 children, aged 3.74±5.76 them to the room. As noted above, 12 children refused
years (M ˆ 4.61, SD ˆ 0.51) who were drawn from six participation altogether.
10982302, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S by Universitaet De Valencia, Wiley Online Library on [02/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
212 Donzella et al.

Once in the testing room, 3 Ag/AgCl ECG sure that the children knew how close both they and
electrodes were placed in a triangular pattern on the the E were from winning or losing the competition.
child's chest for cardiac measurement. A baseline This was also reinforced by the Es comments follo-
measure of cardiac data was obtained while the E and wing each game. After the ®rst three wins the child's
child watched a 4-min segment of a familiar television avatar was one step away from the platform. The E
show (Sesame Street). The E and child then played the said, ``Look, all you need is one more win and your
competitive game. At the end of the game, the elect- guy will get to the top and you will get to launch the
rodes were removed and the child was allowed to rocket!'' After the next three losses the Es piece was
launch the rocket several times. The sessions took one step away, while the childs piece had descended to
approximately 30 min from leaving to returning to the the base of the pyramid. The E said, ``All I need is one
classroom and were videotaped unobtrusively for later more win and I will get to launch the rocket!'' At this
coding. The children returned to the classroom in time point many children were very disappointed and the E
to take part in saliva collection for cortisol determina- said, ``maybe we should change the rules. If you win
tion. Salivary cortisol was being collected in each the next game, you can move your guy up two steps.''
classroom from all children daily as a part of a study This allowed the children to reach the platform in two
of temperament, social behavior, and salivary cortisol wins. Shortening the ®nal win period to two games
(see Sebanc, Tout, Donzella, & Gunnar, 2000). Sam- was based on the reactions of several pilot subjects
ples collected on the day the child participated in the who appeared to be having dif®culty controlling their
competitive game were used to determine postgame emotions by the end of the Lose period. Once the child
cortisol concentrations and were compared to the became the overall winner, the E removed the elect-
median of the child's cortisol levels on nongame days. rodes and the child was permitted to launch the rocket.
The E and child played eight games of MemoryTM. Several launches were allowed with the goal that each
In this game, four pairs of pictures were laid out face child would be happy and satis®ed before returning to
down on a small board. Each player was allowed to the classroom.
turn over two pictures on each move. If the player
turned over two of the same picture, the player took
that pair off the board and was allowed another move. Measures
When two nonmatching pictures were turned over,
play shifted to the other player. The player with the Salivary Cortisol. Saliva for cortisol determination
most pairs won that game. Each board was precon- was obtained by having the children dip 2-in. long
structed and the E had memorized the placement of all cotton dental rolls into less than 1/16th of a teaspoon
pictures. This allowed the E to manipulate who won of sugar-sweetened Kool-AidTM drink mix crystals.
each game. The protocol called for the child to win the Children then placed the cotton rolls in their mouths
®rst three games, the E to win the next three, and the until saturated. The procedure took 5±10 min and was
child to win the ®nal two games. Keeping in mind the performed by all the children at a set time in each
differing skill levels among children, the number of classroom. The timing of the classroom collections
moves required for the children to win games differed. was within 10 min of the children's return to the
On average, though, with set up and transition each classroom after the competition. Only children who
game lasted 1 min. Each period of the game (Win I, provided samples with suf®cient saliva for assay could
Lose, Win II) lasted approximately 3 min. be included in the analysis: eight children were
Before the play started, the rules of the game were excluded for insuf®cient volume or for refusing to
demonstrated until the child showed clear under- provide saliva samples after the competition. Separate
standing. Both the E and child chose small ®gures multivariate analyses were computed for the cardiac
(avatars) to represent themselves. The E then showed data, behavioral data, and teacher report temperament
the child a two-sided pyramid. Each side consisted of measures analyzed in this report to determine whether
three 1 in. steps leading to a platform at the pinnacle. children who failed to provide postgame cortisol
The E and child placed their avatars at the base of the measures differed from those who did. In these analy-
pyramid, one on each side. The goal of playing the ses, gender and useable cortisol data served as
games was to get one's avatar to the platform at the between-subject factors and age was entered as the
top. The player reaching the top ®rst won the overall covariate. No signi®cant multivariate or follow-up
competition and got to launch the rocket. With each univariate effects for the useable cortisol factor were
game win, the avatar belonging to the winner climbed obtained. Baseline cortisol was determined from the
one step. With each loss, the player's avatar moved classroom cortisol data obtained on 25 days of saliva
down a step. The steps and avatars were used to make collection after the children were familiar with the
10982302, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S by Universitaet De Valencia, Wiley Online Library on [02/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Cortisol and Vagal Tone Responses 213

classroom (i.e., 4 months into the school year). Most (``yay''), laugh/giggle. Anger/frustration was scored
(50%) of the children contributed 18 or more saliva as 1: pout; 2: negative exclamation, arguing, or insis-
samples from which their median classroom cortisol tence on winning; 3: tantrumming, refusal to continue
level was determined and used as the measure of (``This is a dumb game!''). Only one child ever dis-
classroom baseline cortisol in the present study (See played the most intense level for anger/frustration,
Sebanc et al., 2000 for further analyses of these class- thus in practice this was a 3-point scale. Tense/an-
room data). xious was scored as 1: watchful, worried expression;
Once all the samples were collected, they were 2: slowing of approach when taking turn, rigid body
assayed using a modi®cation of the CIBA magic posture; and 3: freezing, prolonged hesitation when
cortisol assay (Kirschbaum, Strasburger, Jammers, & taking his/her turn. Sad was scored as 1: mild expre-
Hellhammer, 1989). All samples from a child were ssions of sadness including head down, shoulders
assayed in duplicate in the same assay batch. Samples sagging, vocalization of `oh no', mouth turned down
differing by 20% were re-assayed. Samples yielding at corners; and 2: more intense or prolonged sad ex-
values above 2.5 mg/dl were diluted. Those that failed pressions that might include watering of eyes, wiping
to dilute linearly were excluded from analysis. The eyes, pursing of mouth in apparent attempt not to cry,
correlation between duplicates was .96. The inter- and sharp gasps and deep sighs. Inter-coder agreements
intra-assay coef®cients of variation for control ranged from 89 to 97%. The scores for each category
samples were 12.0 and 6.37, respectively. of affect were averaged within the baseline and three
game periods (Win I, Lose, Win II) to yield three
Heart Period and Vagal Tone. Cardiac data were measures for each affect. Descriptive statistics were
acquired using the Vagal Tone Monitor-II (VTM-II, examined for these measures and showed that very
Delta-Biometrics, Inc., Bethesda, MD). Raw ECG few of the children ever expressed any overtly angry
data was digitized at 1 kHz and bandpass ®ltered at 5 affect and those that did often also exhibited higher
and 200 Hz, with a 3 dB cutoff. A computer algorithm levels of tense/anxious affect. The measure of anger/
detected R-spikes from the raw wave, and computed frustration was therefore combined with that of tense/
interbeat intervals (IBIs). MXedit software was used anxious to yield a tense/angry variable scored in each
to visually display the heart period data, to edit out- of the game periods.
liers, and to quantify mean IBI and the Vagal Tone A second set of coders scored the children's turn
Index (Porges, 1985). (Note: baseline Vagal Tone data taking behavior from the videotapes. On each of the
were reported in Sebanc et al., 2000). Baseline meas- children's moves, coders scored whether the child
ures of vagal tone and heart period were assessed took their turn without hesitation (0), paused or
during the 4-min Baseline period, and each of the 3- hesitated, as if thinking, when turning over the card
min test periods (Win I, Lose, Win II). At least 2 min but appeared to know it was his/her turn (1), or failed
of artifact-free data was required for each period in to move, had to be told or prompted (``it's your turn'')
order to compute average vagal tone and heart period (2). On each of the E's turn the observers scored
measures. Using this criteria, useable data during the whether the child waited and gave the E his/her turn
Baseline and Win I periods were obtained from 61 of (0), started approach to the cards but stopped without
the children, while 60 had useable data during the needing to be told (1), touched the cards but then did
Lose and Win II periods. not turn them over and did not interfere with E's turn
(2), or moved out of turn (3). A (3) was also scored if
Affect and Turn-Taking. One videotape containing the child obviously cheated during his/her turn as this
data on ®ve subjects was accidentally erased. Affect meant he/she interfered with the E's opportunity to
was scored for each game for the remaining 56 chil- win. A separate ``cheat'' scoring was not employed as
dren. One set of coders scored the children's affect so few children actually attempted this strategy. The
from the videotapes. Four categories of affect were mean coef®cient k for turn-taking measures was .86.
noted: positive; anger/frustration; tense/anxious; and Because of technical errors in taping (i.e., the chil-
sad. For each scale, 0 represented no evidence of the dren's hands were not visible) turn-taking data were
affect. Mixtures of affects were allowed within coding missing for two children.
intervals. Based on pilot data, positive and sad were
made into 3-point scales, while anger/frustration and Temperament. For each child, the head teacher in
tense/anxious were 4-point scales. Positive affect was each class completed a version of the child behavior
scored as 1: closed mouth smile, positive toned voca- questionnaire (CBQ; Ahadi, Rothbart, & Ye, 1993),
lization, or facial expression of interest or enthusiasm; modi®ed with help from M. Rothbart (see Gunnar,
and 2: open mouthed smile, happy vocalization et al., 1997). Key scales from the three higher order
10982302, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/1098-2302(2000)37:4<209::AID-DEV1>3.0.CO;2-S by Universitaet De Valencia, Wiley Online Library on [02/04/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
214 Donzella et al.

dimensions of the CBQ were retained with response Behavioral Responses


options reduced from 7 to 5 points. The items were
The three affect variables (positive, tense/angry, and
combined into their scales with each based on respo-
sad) scored in each of the Win I, Lose, and Win II
nses to at least ®ve items. Internal consistency of the
periods were analyzed ®rst with age. None of the
modi®ed scales was veri®ed by computing Cronba-
correlations with age was signi®cant. Separate 2
ch's a and comparing them to those reported for the
(Gender) repeated measures analyses for each affect
full CBQ (Ahadi et al., 1993). Alphas for the modi®ed
were computed for the Win I, Lose, and Win II periods
scales were highly comparable to those from the full
using Greenhouse±Geisser corrections when appro-
CBQ and ranged from .78 to .96. Based on previous
priate. The results showed that as expected, signi®cant
factor analyses (Ahadi et al., 1993), the scales were
game period effects were found for all three affect
averaged to yield measures of surgency or extrover-
measures, positive, F(3, 116) ˆ 28.7, p < :001, sad,
sion (average of high pleasure, impulsivity, activity
F(3,116) ˆ 24.6, p < :01 and tense/angry, F(3,116)
level and shyness, reverse scored), effortful control
ˆ 10.8, p < :01. Posthoc Newman±Keuls tests indi-
(mean of attention focusing and inhibitory control),
cated that, as expected, positive affect decreased from
and negative affectivity (mean of discomfort, anger,
Win I to Lose and then increased from Lose to Win II
and sadness). The teacher version of the CBQ also
with means of .83, .55, .88 (SDs .36±.39). Sad affect
yielded a scale for physical aggression. It is important
was rarely observed during the two win periods
to note that shyness loads negatively on the surgency
(Ms ˆ .02 and .04, SDs ˆ .14, .19) but was noted more
factor. Thus, lower surgency re¯ects higher shyness.
frequently during the Lose period, M ˆ .28, SD ˆ .28.
For tense/angry affect, a signi®cant main effect of
gender was noted, F (1,58) ˆ 7.1, p < :01, with boys
RESULTS
showing more tense/angry affect overall (M ˆ .18,
SD ˆ .23) than did girls (M ˆ .07, SD ˆ .12). For both
The data were ®rst examined to determine if the
sexes combined, there was a signi®cant increase in
procedures elicited the anticipated behavioral reac-
tense/angry affect from Win I (M ˆ .05, SD ˆ .15) to
tions. Second, the inter-correlations among the beha-
Lose (M ˆ .44, SD ˆ .41) and a decrease that did not
vioral measures were examined. Third, the vagal tone
achieve signi®cance in the Win II period (M ˆ .14,
and heart period data were examined to determine if
SD ˆ .25).
these measures were suppressed in response to the
Turn-taking behavior was analyzed next. Younger
competitive games, and whether they were more su-
children were more likely to move out of turn during
ppressed during the Lose period than during the
the Win periods: Win I, r (52) ˆ ÿ.46, p < :01, Win
periods when the child was winning the competition.
II, r (52) ˆ ÿ.32, p < :05. This correlation was not
Correlation between the cardiac measures and affect,
signi®cant during the Lose period, r (52) ˆ ÿ.22, ns.
behavior, and temperament measures was then com-
Age was not correlated with inhibiting/slowing
puted. After this, the cortisol data were examined for
actions on child moves during any period of the
main effects of trials. Then children were grouped by
games (rs .00 to ÿ.10). A 2 (Gender) by 3 (Trials)
whether or not they exhibited a signi®cant rise in
ANOVA with repeated measures on the second
cortisol in response to the game. Affect, behavior,
factor revealed a signi®cant trials effect for turn-
temperament, and cardiac responses were examined
taking on the Es moves, F(2, 116) ˆ 4.97, p < :01).
for differences between children exhibiting and those
Newman±Keuls posthoc tests indicated that child-
not exhibiting a cortisol response. Finally, individual
ren behaved more impulsively during the Lose
differences in surgency were used to predict a cortisol
period (M ˆ 0.75, SD ˆ .60) compared to Win I
response. Throughout, age and/or gender were consi-
period (M ˆ .34, SD ˆ .61), but the difference
dered as covariates. Gender differences are often
between Lose and Win II (M ˆ .56, SD ˆ .79) was
found for temperament measures, with girls showing
not signi®cant. No signi®cant trials or gender effects
greater effortful control (Ahadi, et al., 1993; Davis,
were noted for turn-taking behavior on child moves,
Donzella, Krueger, & Gunnar, 1999). Age might play
Fs < 1.0.
a role in children's behavioral and physiological res-
ponses to the competition, with younger children
potentially ®nding the competition more challenging.
Temperament Associations with Affect and
Vagal tone increases with age, due to changes in body
Turn-Taking Behaviors
size and metabolism, and in adults, gender differences
have been found in parasympathetic control over the Correlations, controlling for age where necessary,
heart (Rossy & Thayer, 1998). were computed between the teacher report measures
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Cortisol and Vagal Tone Responses 215

of surgency and effortful control temperament Cardiac-Behavior Associations


and the affect and turn-taking behaviors scored
Controlling for age, baseline vagal tone was not
during the competitive games. Surgency was posi-
associated signi®cantly with either of the two affect or
tively correlated with positive affect during winning,
two turn-taking behaviors assessed during either the
r (53) ˆ .28, p < :05, tense/angry affect during
Win or Lose periods. Neither was D Base to Win I.
losing, r (53) ˆ .29, p < :05, and failing to move
However, D Win I to Lose was signi®cantly associated
immediately when it was the child's turn
with tense/angry affect, r (53) ˆ .29, p < :05. To
during the Lose period, r (53) ˆ .29, p < :05. Con-
determine whether this correlation was due to children
trolling for age, effortful control was negatively
who suppressed vagal tone further when they began to
correlated with moving when it was the Es turn
lose the game, the change from win to lose was sub-
during the Win I period, partial r (52) ˆ ÿ.33,
divided to yield three groups: children whose change
p < :05. Negative affectivity was positively correlated
scores were  .5 SD below (suppressors) or above
with showing sad affect during the Lose period,
(increasers) the mean, versus those who were within .5
r (53) ˆ .36, p < :01.
SD of the mean. Newman±Keuls posthoc tests
comparing the means for these groups revealed that
Cardiac Measures only those who suppressed vagal tone from winning
to losing differed in tense/angry affect (M ˆ .76,
Age was signi®cantly and positively correlated with
SD ˆ .59, n ˆ 11) from both of the other groups
vagal tone and heart period in all of the segments of
(Ms ˆ .39, .33; SDs ˆ .39, .20, ns ˆ 26, 18).
the game, rs ranged from .32 to .54, dfs from 58 to 59,
ps < :05. Trials and gender effects were examined
using separate, repeated measures ANOVAs for vagal
Cortisol Response
tone and heart period. Gender was not a signi®cant
factor in either analysis, F(1,58) < 1:0, while both The cortisol data were examined next. Neither age nor
measures yielded a signi®cant trials effect, vagal tone, gender was associated with cortisol. To determine
F(3,172) ˆ 95.8, p < :001 and heart period, F(3,172) whether the response to the game differed for children
ˆ 152.8, p < :001. Posthoc Newman±Keuls tests tested in the morning (AM classes) versus afternoon
revealed that for vagal tone there was a signi®cant (PM classes) as might be expected given the circadian
decrease from Baseline (M ˆ 5.8, SD ˆ 1.2) to the rhythm in cortisol, we computed a 2 (AM vs. PM) by 2
Win I period (M ˆ 4.9, SD ˆ 1.2) but no changes were (classroom baseline vs. postgame) repeated measures
noted from this period to either the Lose (M ˆ 5.0, ANOVA. The interaction effect did not reach tradi-
SD ˆ 1.2) or Win II period (M ˆ 4.8, SD ˆ 1.1). A tional levels of signi®cance, F(1,51) ˆ 2.7, p ˆ .10.
similar result was obtained for Heart period (Ms The change scores (postgame ÿ classroom baseline)
590.7, 548.3, 544.8, 537.4, SDs ranged from 50.2 to for AM classes were M ˆ .00, SD ˆ .11 compared to
65.9). Heart period and vagal tone were highly PM classes, M ˆ .05, SD ˆ .14. As the standard
correlated during each phase of testing, rs > :76, dfs deviation in classroom medians was  .055, these
58 and 59, ps < :001. To reduce the number of varia- data indicated that on average the children did not
bles examined in subsequent analyses, the more spe- show a cortisol response to the competitive game.
ci®c measure, Vagal Tone, was retained and scores However, the purpose of the study was to identify
were computed re¯ecting the suppression of vagal children who did respond. Therefore, the range in
tone from Baseline to Win I and from Win I to Lose. change scores was examined. Although 85% of the
Positive numbers indicated suppression. Three vagal children either had lower cortisol levels following the
tone measures were thus included in later analyses: game or did not increase more than 1 SD (i.e., .05±
Baseline, D Base to Win I, and D Win I to Lose. Partial .06 mg/dl), 15% of the children (n ˆ 8) did show clear
correlations controlling for age were computed to evidence of higher cortisol levels following the game.
examine the relations among these variables. Base- The change scores for these children ranged from.08
line was positively correlated with D Base to Win I, to.53 mg/dl, with a mean of.24 mg/dl. We then exami-
partial r (57) ˆ .35, p < :01, but not with D Win I ned the ratio of change by dividing postgame cortisol
to Lose, partial r (57) ˆ .00, ns. Thus, children with by the child's typical classroom cortisol level. For the
higher baseline vagal tone suppressed vagal tone group who were considered to have responded, the
more to playing the competitive games, but did ratios ranged from 1.4 to 3.4 with a mean of 2.1 indi-
not show more or less suppression in vagal tone cating that these children had cortisol levels following
when they were losing as compared to winning the the game that were about two times their typical
competition. classroom levels. For the remaining children, the
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216 Donzella et al.

average ratio was .91, SD ˆ .29, indicating little if any Table 1. Behavior, Temperament, and Cardiac Activity
change from their classroom levels. To make sure that for Children who Exhibited Elevations in Cortisol
exhibiting a signi®cant rise in cortisol was not merely during a Competitive Gamea
due to having unusually low classroom baseline levels Rise in Cortisol to Game
(i.e., law of initial values), a t-test on the classroom
cortisol levels was computed that yielded a nonsigni- NO YES
®cant trend, t (10.1) ˆ 1.85, p < :10. However, rather
Behaviors during lose period n ˆ 38 nˆ8
than having low classroom levels, children who Tense/Angry* .44 .78
increased cortisol levels following the game tended (.36) (.62)
to have slightly higher classroom cortisol baselines, Sad .34 .12
M ˆ .22 mg/dl, SD ˆ .04 compared to the other chil- (.31) (.13)
dren, M ˆ .19 mg/dl, SD ˆ .06. To rule out the possi- Impulsive during Es turns .59 .85
bility that time-of-day (i.e., AM or PM nursery school (.49) (.83)
classes) affected cortisol response the number of Inhibited during Cs turns .03 .20
children exhibiting a response was analyzed by AM (.12) (.55)
versus PM classes. The result was not signi®cant, w2 Cardiac Data n ˆ 43 nˆ8
(1) ˆ .10, ns. There was some indication, however, Baseline vagal tone 5.9 5.4
that gender affected the results as seven of the eight (1.1) (1.7)
children who showed a cortisol response were boys, D Win to lose‡vagal tone ÿ.11 .21
w2 (1) ˆ 3.1, p ˆ .06. (.44) (.55)
Teacher report CBQ n ˆ 45 nˆ8
Cortisol Responders Versus (in standard scores)
Non-Responders Surgency* .04 .74
(.81) (.77)
To examine cardiac and behavioral factors associated Effortful control .23 ÿ.36
with the rise in cortisol, a multivariate analysis of (.65) (1.48)
variance was performed, controlling for age, entering Negative affectivity .02 ÿ.60
the measures shown in Table 1. The multivariate effect (.95) (.91)
for cortisol response was signi®cant, F(10,34) ˆ 2.85, Aggression ÿ.15 .24
(.86) (.82)
p < :01. Follow-up univariate tests with Bonferroni
corrections yielded three signi®cant differences. *Signi®cant univariate effect.
Children who elevated cortisol had signi®cantly more a
Means and (standard deviations) exhibited for all available
surgent temperament, F(1,49) ˆ 15.0, p < :01 and cases.
lower effortful control temperament, F(1,49) ˆ 5.8,
p < :05. They were also more tense/angry during the
Lose period, F(1,49) ˆ 7.4, p < :01 (see Table 1).
Because all, but one, of the cortisol responding
children were males, the MANOVA was repeated To determine whether cortisol responding children
for the three signi®cant variables entering only boys to differed from the other children prior to the Lose
be certain that the difference noted for cortisol period, another MANOVA was conducted on the
responding children did not merely re¯ect gender affect measures, behavioral responses, and cardiac
differences. The result was still signi®cant, Hotelling data obtained during the Win I period. The multi-
F(3, 28) ˆ 4.65, p < :009; however, only the tempera- variate effect for cortisol response was not signi®cant,
ment variables remained signi®cant after Bonferroni F(5,40) ˆ 0.40, ns, nor were any of the follow-up
correction. Because the temperament measures univariate tests (all Fs < 1:0). Finally, we examined
were computed from more narrow-band scales, we whether the children who exhibited a rise in cortisol
computed a third MANOVA entering the scales used were highly surgent children who were in addition
to compute surgency and effortful control. The also low in effortful control. Seven of the eight
follow-up univariate tests indicated that cortisol cortisol responding children scored above the median
responders scored higher on high pleasure or sensa- on surgency, however, of these children, only three
tion seeking, F(1,48) ˆ 4.82, p < :05; impulsivity, scored below the median on effortful control, The w2
F(1,48) ˆ 9.19, p < :004; activity level, F(1,48) ˆ (1) ˆ 2.1, ns. Thus, there was no evidence that only
5.51, p < :02; and lower on inhibitory control, poorly regulated surgent children were likely to
F(1,48) ˆ 5.1, p < :05. exhibit a rise in cortisol.
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Cortisol and Vagal Tone Responses 217

Individual Differences in Surgent ests that they were emotionally engaged in the
Temperament and Cortisol Response competition and found the threat of losing aversive.
Affect and behavior during the competition re¯ec-
Next, we addressed the question of whether individual
ted teacher's perceptions of the children's tempera-
differences in surgent temperament could distinguish
ment. Teacher-reported negative affectivity was
cortisol responding children. We focused on surgency
correlated with expression of more sad affect during
because of the interest in surgent versus shy/inhibited
the Lose period, while teacher-reported effortful con-
temperaments and stress reactivity. In the above cor-
trol was negatively correlated with impulsive moving
tisol analysis, 15% of the sample showed a clear cor-
on the Es turn, even after controlling for the effects of
tisol response. Therefore, children were split into two
age. Critically for the present analysis, teacher-
temperament groups: high surgent children scored in
reported surgency correlated with greater displays of
the top 15% on surgency, and normal/low surgent
positive affect when the children were winning and
children scored in the other 85% on that factor. A
greater displays of tense/angry affect when they were
crosstabulation analysis compared surgency (high vs.
losing. This raises the possibility that the reason surg-
normal/low) with cortisol response (Yes vs. No), two-
ency and cortisol elevations were associated is that
tailed Fisher's exact test ˆ .02. High surgent children
highly surgent children were more engaged in the
are more likely to show a cortisol response to this
competition than the other children and thus experi-
challenge than were normal to low surgent children.
enced the threat of losing as more aversive. Surgent
children, however, did not appear to be more impul-
sive when losing, instead they became more cautious
DISCUSSION and seemingly tense when they started to lose the
competition.
Most of the research on stress reactivity in young The cardiac measures also showed changes in res-
children has focused on shy, anxious, inhibited chil- ponse to the competition. The most signi®cant change
dren. While these studies have yielded important ®n- was from baseline to playing the game. On average,
dings, the results of the present study clearly indicate decreases in vagal tone and heart period (i.e., incre-
that shy, inhibited temperament is not the only ased heart rates) were noted when the children began
disposition associated with increased cortisol and car- to play against the experimenter. Additional decre-
diac reactivity. In addition, surgent temperament is ases, however, were not noted for most of the children
associated with increased cortisol reactivity, at least to when they began to lose the competition. The change
stressors such as the one used in the present study. in vagal tone from winning to losing was, nonetheless,
Indeed, as shyness loads negatively on the surgency associated with tense/angry affect, and this was parti-
factor, the results raise the possibility that less surgent, cularly the case for children who lowered vagal tone
more shy children may be somewhat protected from (  .5 SD) from winning to losing.
cortisol and cardiac reactivity to certain stressors. Despite the degree of emotional engagement
Interpretation of these data depends, however, on our observed, for most of the children the competition
understanding the nature of the competition stressor was not suf®ciently stressful to elevate salivary cor-
employed in this study and on the behavioral cor- tisol concentrations. This is, perhaps, not surprising as
relates of temperament that were observed. Thus, it was the period of time when they were losing the
prior to discussing the primary ®nding of this study, game that was expected to be stressful and this period
data pertaining to the children's responses to the game was brief, lasting only about 3 min. For the remainder
and temperament-behavior associations will be dis- of the time, the children were winning and most were
cussed. expressing positive affect. Indeed, it is less striking
The game was designed to engage and elicit that most children failed to elevate cortisol than that
negative emotions to the threat of potentially losing 15% did show clear evidence of a cortisol response.
the competition. Positive emotional expressions decr- An increase of 1 SD in cortisol was de®ned as a cor-
eased for all the children during the Lose period, while tisol response. For the children classi®ed as res-
sad and tense/angry emotional expression increased. ponding, the typical increase in cortisol doubled their
Children also behaved more impulsively when they classroom level. For one child, indeed, postgame
were losing. That is, they were signi®cantly more levels were three times that child's typical level in the
likely to move when it was the adult's turn. The chil- classroom. These were quite striking increases. The
dren's positive affect during the periods when they average increase in cortisol for these responding
were winning the game and their heightened impul- children was roughly half that reported for adult men
siveness and negative emotionality when losing sugg- in response to stressors like the Trier Social Stress
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218 Donzella et al.

Test (Hellhammer, Buchtal, Gutberlet, & Kirsch- have been conducted with preschoolers attempting to
baum, 1997; Kirschbaum, et al., 1995) and somewhat identify the antecedents of later coronary prone
larger than that reported in ambulatory studies of behavior patterns. Generally, these studies have not
adults (Smyth, et al., 1998). There is no way to been successful in producing physiological responses
determine that the increases were to the period of that correlate with Type A as assessed on question-
losing the game as opposed to simply playing naires such as the MYTH (Matthews & Angulo, 1980;
competitively against an adult. However, the fact that Murray, Matthews, Blake, Prineas, & Gillum, 1986).
the increases were associated with emotional expres- It is possible that the children who showed elevations
sion during the Lose period and not with emotionality in cortisol in this study would score as more Type A
during the times when the children were winning than the other children, however, without including
supports the idea that it was the threat of losing that measures of Type A behavior we cannot know the
activated the HPA system for these children. degree of overlap.
The children showing a cortisol response were Several limitations qualify the ®ndings reported for
described as more surgent by their teachers. They this study. First, we do not know the test±retest relia-
were also distinguished by being lower in effortful bility or generalizability of these ®ndings. The compe-
control. However, there was no evidence that highly tition in the present game was formal, in the sense that
surgent children also needed to be low in effortful there would be a clear winner and loser and a prize
control to produce these reactions. Both scores on that was or was not obtained. Such formal competi-
surgency and effortful control appeared to contribute tions are often avoided in preschool classrooms.
to the likelihood of large cortisol responses to this However, preschool children are often observed to
competitive situation. These results are consistent compete informally. Informal competitions include
with other data on cortisol-temperament associations things like trying to see who makes it ®rst to the
among preschoolers where both surgency and effort- playground or who can go faster on one's tricycle. We
ful control have been found to predict cortisol levels do not know whether more surgent children exhibit
and reactivity when children are in peer group settings cortisol responses to such informal competitions and,
(Gunnar et al., 1997). thus, whether or not the present results generalize to
Although activation of the HPA axis was expected situations occurring frequently in young children's
to be associated with suppression of vagal tone, this lives outside the laboratory context. Second, there
was not observed. The means were in the expected were a number of children who refused to play the
direction, but there was suf®cient variation to produce game. These children were described as more shy and
a null effect statistically. There was also no evidence dysphoric by their teachers. We do not know whether
that changes in vagal tone either from baseline to these children might have shown elevations in cortisol
winning the game or from winning to losing were had they been required to participate. However, the
associated with teacher-reported surgency or effortful fact that shyness appeared to predict avoidance of a
control. Vagal tone may not have been the most competitive situation may indicate why shy children
sensitive measure to use as it re¯ects the parasym- have not always been found to have higher cortisol
pathetic and not the sympathetic regulation of heart levels in preschool peer group settings. Finally,
rate. In other studies, measures of sympathetic because we did not test children in situations designed
input, such as preejection period (PEP) have been to be stressful for different temperament types, we can
shown to covary more with activation of the HPA axis say little about the relations between context,
(Berntson, Cacioppo, Binkley, Uchino, & Quigley, temperament, and cortisol responsivity. It might be
1993). that surgency is the critical temperament dimension
In several ways the physiological and behavioral affecting cortisol responses to competition stress,
responses of these children are reminiscent of the while shyness might be the critical temperament dim-
Type A, coronary prone behavior pattern described in ension for responsivity to strange or novel events.
the literature on coronary heart disease (Lundberg, Because shyness contributes negatively to the sur-
Rasch, & Westermark, 1991). This is especially the gency dimension of temperament, this might mean
case as tense and angry affect was observed both that children who are vulnerable to one kind of stre-
among the children who showed cortisol elevations ssor are somewhat protected from the other. However,
and those who exhibited vagal tone suppression. without testing children in several situations designed
Because we did not design the study as an assessment to provoke stress reactions for different reasons, we
of Type A behavior in children, we did not include cannot draw any conclusions on this point. None-
questionnaires that might assess this disposition. theless, with these limitations in mind, the present
Studies of cortisol, heart rate, and blood pressure results do strongly argue for expanding our analysis of
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Cortisol and Vagal Tone Responses 219

stress reactive temperament beyond a narrow focus on de Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stansbury,
the shy, inhibited, or fearful child. K. (1998). Familiar and novel contexts yield different
associations between cortisol and behavior among 2-year-
olds. Developmental Psychobiology, 31(1), 93±101.
Derryberry, D., & Rothbart, M. (1997). Reactive and
NOTES
effortful processes in the organization of temperament.
Development and Psychopathology, 9(4), 633±652.
Portions of these data were presented at the 1998 American
Dettling, A., Gunnar, M. R., & Donzella, B. (1999). Cortisol
Psychosomatic Society meeting and the 1999 Society for
levels of young children in full-day childcare centers:
Research in Child Development meeting. The authors thank
Relations with age and temperament. Psychoneuroendo-
the teachers and children in the Shirley Moore Laboratory
crinology, 24(5), 505±518.
Nursery School for their participation in this research, and
Eisenberg, N., Fabes, R., Shepard, S., Guthrie, I., Murphy,
Tonya E. Sponem and Sarah K. Lane for their help with
B., & Reiser, M. (1999). Parental reactions to children's
behavioral coding and vagal tone collection.
negative emotions: Longitudinal relations to quality of
children's social functioning. Child Development, 70(2),
513±534.
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