Child Development, May/June 2002, Volume 73, Number 3, Pages 718–733
Temperament, Tympanum, and Temperature:
Four Provisional Studies of the Biobehavioral Correlates
of Tympanic Membrane Temperature Asymmetries
W. Thomas Boyce, Marilyn J. Essex, Abbey Alkon, Nancy A. Smider, Tyler Pickrell, and Jerome Kagan
Previous research in both humans and nonhuman primates suggests that subtle asymmetries in tympanic
membrane (TM) temperatures may be related to aspects of cognition and socioaffective behavior. Such associations could plausibly reflect lateralities in cerebral blood flow that support side-to-side differences in regional
cortical activation. Asymmetries in activation of the left and right frontal cortex, for example, are correlates of
temperamental differences in child behavior and markers of risk status for affective and anxiety disorders.
Tympanic membrane temperatures might thus reflect the neural asymmetries that subserve individual differences in temperament and behavior. This report merged findings from four geographically and demographically distinctive studies, which utilized identical thermometry methods to examine associations between TM
temperature asymmetries and biobehavioral attributes of 4- to 8-year-old children (N 468). The four studies
produced shared patterns of associations that linked TM temperature lateralities to individual differences in
behavior and socioaffective difficulties. Warmer left TMs were associated with “surgent,” affectively positive
behaviors, whereas warmer right TMs were related to problematic, affectively negative behaviors. Taken together, these findings suggest that asymmetries in TM temperatures could be associated with behavior problems that signal risk for developmental psychopathology.
INTRODUCTION
Core body temperature has been recognized as a sign
of specific disease states since the Alexandrian civilization of the third century B.C. (Stein, 1991). Thermoregulation was regarded by Claude Bernard as
one component of the homeostatic systems ensuring
a stable and optimal milieu intérieur (Pickering, 1961).
In the mid-20th century, Sokolov (1963) examined
peripheral skin temperature as a measure of autonomic reactivity, and later investigators (Levenson,
Ekman, & Friesen, 1990; Mizukami, Kobayashi,
Iwata, & Ishii, 1989; Svebak, Storfjell, & Dalen, 1982)
studied skin temperature changes in response to
emotion-evocative events. Further, recognition of lateralization among neural structures and functions
(Davidson, 1988; Davidson & Fox, 1989; Fox, 1991)
spawned additional research on skin temperature
asymmetries as markers of biobehavioral patterns of
response and reactivity (Chang, 1993; Kagan, 1994;
Kagan et al., 1995; Rimm-Kaufman & Kagan, 1996).
Measurement of tympanic membrane (TM) temperature using infrared thermometry has come into
clinical use, especially in pediatric medicine, for both
practical and theoretical reasons. Using one of several
inexpensive, commercially available TM thermometers, core body temperature can be ascertained nearly
instantaneously and with minimal discomfort to children. Tympanic membrane temperatures demonstrate strong correlations with concurrent tempera-
ture measures in the pulmonary artery (Milewski,
Ferguson, & Terndrup, 1991), rectum (Kenney, 1990),
and mouth (Talo, Macknin, & Medendorp, 1991), suggesting that TM thermometry is a valid analog of core
body temperature. Further, blood supply to the TM is
supported by the same vasculature that perfuses the
hypothalamus, the principal neural “clearinghouse”
involved in psychobiological stress responses; and
the frontal cortex, a cerebral center for the processing
of emotional information (Benzinger & Taylor, 1963;
Chrousos & Gold, 1992). Finally, TM thermometry is
uniquely positioned as a lateralized measure of core
body temperature, distinct from the midline locations
that characterize all other sites for core temperature
assessment.
Using lateralized measures of peripheral temperature, recent studies have identified previously
undiscovered asymmetries in both resting and reactive skin temperatures. Infants, toddlers, and adolescents, for example, all show a physiologic bias toward
a slightly cooler left forehead relative to the right
(Kagan, 1994). On the other hand, greater cooling of
the right forehead, relative to the left, is more characteristic of shy, inhibited preschool children following
unfamiliar events (Kagan, 1994). When challenged by
stressors, adults show a drop in finger temperatures
© 2002 by the Society for Research in Child Development, Inc.
All rights reserved. 0009-3920/2002/7303-0004
Boyce et al.
of approximately .3C, and when finger temperatures are measured on both hands, the left is typically
cooler than the right (Kagan, 1994). These findings
may be accounted for by asymmetries in patterns of
sympathetic arousal, including laterality in the alphaadrenergically mediated microcirculation responsible
for fluctuations in skin temperature (Randall, McNally, Cowan, Caliguiri, & Rohse, 1957; Rowell,
1986b; Yanowitz, Preston, & Abildskov, 1966).
Somatic, Neural, and Cerebral Asymmetries
Structural and functional asymmetries of significance for biological and psychosocial processes have
also been observed in human anatomy, the autonomic
nervous system (ANS), and cerebral neural circuitry.
Although symmetry around a central axis is the rule
among anatomically complex organisms, there also
appear to be frequent lateralities in somatic and physiologic features. Even snails, a rare example of a “higher”
animal with a nonbilateral form, show a marked evolutionary predisposition to a dextral (right-handed, or
clockwise, coiling), rather than sinistral, shell asymmetry (Gould, 1995). The degree of human somatic
symmetry appears to be a heritable dimension of
physical attractiveness (Livshits & Kobyliansky, 1991),
and fluctuating somatic asymmetry, defined as deviation from morphological symmetry due to genetic
and environmental perturbations during ontogeny,
may influence sexual selection in human and nonhuman species (Thornhill & Gangestad, 1994). Such tangible bodily asymmetries are likely related, in part, to
known left–right lateralities in gene expression during fetal development (Robertson, 1997).
Beyond such structural asymmetries, functional
asymmetries have also been documented in both the
human ANS and central nervous system (CNS). For
example, the sympathetic division of the ANS is more
reactive on the right side of the body than on the left.
Stimulation of the right stellate ganglion produces
greater accelerations in heart rate than stimulation on
the left (Kagan, 1994); and right, but not left, stellate
ganglion blockade results in heart rate deceleration
(Rogers, 1978). Within the CNS, symmetrical hemispheric activation in certain cortical regions appears
to be an important substrate for the regulation of positive and negative emotions in early development
(Davidson & Fox, 1989; Fox, 1991; Hagemann, Naumann, Becker, Maier, & Bartussek, 1998). Disturbances in an infant’s early social environment, such as
the interpersonal difficulties attending maternal depression, appear to influence the development of the
infant prefrontal cortex, which is involved in emotion
regulation and expression (Dawson, Hessl, & Frey,
719
1994). Infants of depressed mothers (Dawson, Frey,
Panagiotides, Osterling, & Hessl, 1997), as well as
depressed adults (Schaffer, Davidson, & Saron, 1983)
and participants with past depressive symptoms
(Henriques & Davidson, 1990), all exhibit reduced left
frontal electroencephalographic (EEG) activity.
These observations suggest that left prefrontal cortical activation is associated with positive emotions,
such as joy and interest, whereas right prefrontal activation is linked to negative emotions, such as distress,
fear, and disgust. In quartet play groups, moreover,
socially competent children exhibited greater left
frontal activation, whereas children displaying a predisposition to social withdrawal and problematic behavior showed greater right frontal activation (Fox et
al., 1995). Of central importance to the orientation
of the present work, however, is the finding that, although asymmetrical cortical activation is characteristic of affectively negative processes, such processes
also produce bilateral activation of the prefrontal
cortex. Dawson (1994) found, for example, that expressions of negative emotionality in toddlers evoked
relative right prefrontal EEG activation, but such
asymmetry was overlaid on an even more prominent
bilateral prefrontal activation. Thus, emotional dysregulation has been associated with both bilaterally
exaggerated and dextrally asymmetrical prefrontal
activation. Such observations are consistent with
Gray’s (1982, 1987) proposal that two oppositional
brain systems, one appetitive and the other aversive,
form the motivational substrates of human behavior.
Brain asymmetries have also been implicated in aspects of immune surveillance. Changes in lymphocyte proliferation and natural killer cell (NKC) activity in adolescent males were associated with negative
life events in one study (Liang, Jemerin, Tschann,
Wara, & Boyce, 1997), for example, but only among
individuals with greater left frontal activation. In
other research (Kang et al., 1991), women with greater
right frontal activation showed lower NKC activity
than did counterparts with greater left frontal activation. Such relations between CNS asymmetries and
immune function are thought to be attributable, in
part, to lateralization in the cerebral control of cortisol
secretion (Wittling & Schweiger, 1993), a powerful
immunoregulatory process. Consistent with this suggestion is recent evidence that extreme asymmetry
in activation of the right frontal cortex is associated
with plasma cortisol concentrations in young rhesus
macaques (Kalin, Larson, Shelton, & Davidson, 1998).
These observations of immunologic and adrenocortical correlates of CNS asymmetries may be linked to
the cortical asymmetries in emotion dysregulation by
virtue of known associations between depression
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Child Development
and immune dysfunction (Leonard & Miller, 1995)
and between affective and immune-mediated disorders (Cohen, Pine, Must, Kasen, & Brook, 1998).
Perhaps related to peripheral and central neural
asymmetries and their physiologic correlates are several observable lateralities in emotional expression and
subjective bodily complaints. Comparisons of facial
expressions in composite left- and right-sided faces
have shown, for example, that emotions are expressed
with greater intensity on the left side of the face (Sackheim, Gur, & Saucy, 1978). Other studies have found
that positive emotions are more readily expressed on
the right side of the face, whereas negative emotion is
projected more prominently on the left (Schiff & MacDonald, 1990). These results are consistent with known
lateralities in emotion regulatory processes, summarized above, and with the contralateral control of facial
musculature involved in emotion expression. Moreover, among adults with affective, anxiety, and somatization disorders, somatic symptoms occur significantly
more often on the left side of the body, suggesting
greater involvement of the right cerebral hemisphere
in symptom formation (Min & Lee, 1997).
Cerebral Circulation
As in the periphery, the ANS controls the dynamics
of cranial circulation, in interaction with the fastigial
nucleus of the cerebellum (Branston, 1995; Reis &
Golanov, 1997). Cerebral blood flow is controlled both
by noradrenergic sympathetic innervation from the
stellate ganglion and by cholinergic parasympathetic
nerve fibers emanating from the otic ganglion. Autonomic innervation of cerebral arteries may play an
even greater role in regulating cerebrovascular tone
in young children than it does in adults (Bevan et al.,
1998). In contrast to the peripheral circulation, total
blood flow to the brain remains relatively constant
under a broad variety of circumstances and conditions. Nonetheless, regional flow to the CNS shifts
markedly in response to changes in regional neural
activity, suggesting that side-to-side asymmetries in
blood flow may accompany emotion-related fluctuations in lateral cortical activation (Rowell, 1986a).
Both - and -adrenergic receptors are involved in
the maintenance of neurogenic tone in the cerebral
vascular bed (Gomez, 1976). Regulatory effects occur,
as well, in the reverse direction, with the left and right
cerebral hemispheres having differential effects on
the ANS. Heart rate increases after left hemisphere inactivation with amobarbital, for example, but decreases following right-sided inactivation (Zamrini et
al., 1990). Similarly, ligation of the right middle cerebral artery, but not the left, results in decreased nor-
epinephrine in both the cortex and brain stem of
laboratory animals (Robinson & Coyle, 1980). These
circulatory dynamics in response to cortical events
and regional activations led Kagan to suggest that activation of the amygdala–frontal cortical circuitry
may be responsible for both the sympathetically
driven cooling of the right forehead and the greater
right frontal EEG activation found in fearful, inhibited children (Kagan, 1994).
Hypotheses and Research Questions
Taken together, the prefatory observations summarized above suggest that (1) individual differences in
emotion regulation and expression are subserved by
activation asymmetries in the prefrontal cortex, (2)
side-to-side differences in cortical activation are supported by autonomically mediated lateralities in cerebral blood flow, and (3) such circulatory lateralities
may be reflected in temperature asymmetries in the
TMs, which are perfused by the same arterial circuits
that supply distal cortical structures. Importantly,
many of the physiological links in this neuroanatomical “story” are provisional in character and suggest
an array of testable, but as yet unproven hypotheses.
The particular subset of those hypotheses that were
addressed by the work reported in this article focused
on plausible associations between individual differences in emotion-related child behavior and patterns
of left and right TM temperatures. More specifically,
implementation of the current studies was based
on the previously noted findings that prefrontal
cortical EEG activation during expression of negative
emotion is characterized by two concurrent but
distinctive phenomena: (1) the asymmetrical, rightdominated activation of the prefrontal cortex, superimposed on (2) an even more pronounced bilateral
activation of both right and left frontal regions (Dawson, 1994). Two hypotheses corresponding to these
cortical phenomena were tested in the four reported
studies; these hypotheses were as follows:
Hypothesis 1: Temperature patterns that reflect
warmer right TMs will be associated with problematic, affectively negative behaviors; whereas
patterns that reflect warmer left TMs will be associated with socially competent, affectively
positive behaviors.
Hypothesis 2: Temperature patterns that reflect
bilaterally warmer TMs will be associated
with problematic, affectively negative behaviors;
whereas patterns that reflect bilaterally cooler
TMs will be associated with socially competent,
affectively positive behaviors.
Boyce et al.
721
Table 1 Patterns of Association Predicted by Hypotheses 1 and 2
Left Tympanic
Membrane
Right Tympanic
Membrane
T
(Left Right)
Hypothesis 1
Problematic, affectively
negative behavior
Socially competent,
affectively positive behavior
↓
OR
↑
OR
↓
↑
OR
↓
OR
↑
Hypothesis 2
Problematic, affectively
negative behavior
Socially competent, affectively
positive behavior
↑
AND
↑
AND
—
↓
AND
↓
AND
—
Note: See text for actual hypotheses. ↑ designates expected positive associations; ↓ designates expected inverse associations.
Table 1 explicates the patterns of association predicted by Hypotheses 1 and 2. It was anticipated
based on Hypothesis 1, for example, that problem
behaviors would be inversely associated with left
TM temperatures or difference scores (T, left right
temperature), or positively associated with right TM
temperatures. Hypothesis 2 predicted that problem
behaviors would also be associated with a TM temperature pattern characterized by higher left and right
temperatures, but with no differences in T. Problem
behaviors, under the measurement constraints of
these studies, might include anger expression, fearfulness, stress reactivity, hostility, shyness, or other
forms of internalizing or externalizing behavior. In
contrast, socially competent behaviors, according to
the predictions of Hypotheses 1 and 2, would be associated with the opposite patterns of TM temperature
magnitudes. Socially competent behavior, in the
studies presented in this article, comprised measures
such as inhibitory control, prosocial behavior, attentional focus, and soothability. The two hypotheses
were addressed by three different laboratory groups,
employing common instrumentation, inclusion and
exclusion criteria, and measurement approaches, in
samples of children from San Francisco and Berkeley,
CA; Madison, WI; and Boston, MA.
GENERAL METHODS
Study Participants
Each of the four study samples was recruited as
part of a larger and ongoing multisite program of
research conducted by the MacArthur Foundation
Research Network on Psychopathology and Development. The San Francisco sample consisted of 37
children (17 boys, 20 girls), 4.5 to 5.5 years of age, who
were enrolled in a study of stress responses associated with beginning kindergarten (for a detailed
study description, see Boyce, Adams, et al., 1995). The
Berkeley sample, comprising 79 children (43 boys, 36
girls), ages 4 to 8 years was recruited for the pilot development of a standardized laboratory protocol assessing psychobiological reactivity to stressful challenges. Both groups of San Francisco Bay Area
children were community convenience samples, recruited from local newspaper, parents’ press, school
bulletin board, and radio or television advertising.
Along with measurements of TM temperature asymmetry scores, parent and/or teacher reports on children’s temperaments and behavior problems were
available for both the San Francisco and Berkeley
samples.
Madison data were drawn from a subsample of
families enrolled in the Wisconsin Study of Families and Work (WSFW), consisting of 570 pregnant
women and 550 husbands or partners of the women
from the Madison and Milwaukee areas (for a detailed description, see Hyde, Klein, Essex, & Clark,
1995). Participants were recruited through obstetrics
clinics, private and university hospital clinics, and a
large health maintenance organization. A WSFW subsample of 192 children (104 girls, 88 boys) had TM
temperature asymmetries measured at the 4.5-year
child assessment.
The Boston sample included 160 participants (84
girls, 76 boys) who were enrolled in a longitudinal
study of children at risk for anxiety disorders (N 33)
and controls (N 127); for a detailed description, see
Kagan (1994). The sample was culled from a larger
cohort of 462 children on the basis of laboratory assessments at ages 14 and 21 months and parent questionnaires regarding children’s symptoms of anxiety
between ages 5 and 7 years. The groups of partici-
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Child Development
pants at high and low risk for anxiety disorders had
been followed, at the time of the current data collection, to an age between 6.5 and 8.5 years.
Study participants were thus drawn from four geographical areas, comprised samples from both longitudinal and cross-sectional studies, and were identified
using a variety of sampling and participant recruitment strategies. At each of the four sites, children
were excluded from current analyses if they were taking any medications, had any single TM temperature
greater than 38C in either ear, or had any within-ear
temperature differences greater than .3C. The sample
sizes noted above indicate the number of study participants from each site following the application of
these exclusion criteria.
Measurement of TM Temperature
All TM temperatures were measured in degrees
centigrade using a self-calibrating infrared Thermoscan® thermometer (Model IR-1, Thermoscan Incorporated, San Diego, CA). At each site, measurements of TM temperatures were conducted without
knowledge of other behavioral or biological variables of relevance to the hypothesized associations.
Laboratory personnel were carefully trained in the
use of the thermometer, and in each group of participants, a posterior displacement of the ear pinna
was performed prior to triggering the instrument to
straighten the external auditory canal and point the
infrared probe directly at the TM. Collection of TM
temperature data followed a fixed procedure in
which four measures were obtained from each participant, alternating between ears and beginning on
the right side. Between the first and second measurements of both ears, the protective plastic cap
was replaced to ensure clarity in the probe’s “view”
of the TM.
Intraoperative comparisons between Thermoscan
infrared aural canal thermometer and a reference
thermocouple adjacent to the TM have demonstrated
correlation coefficients approximating .90 and an accuracy (mean difference between the test thermometer
and the thermocouple) near 0C (Imamura et al., 1998).
Where previously assessed (Chamberlain et al., 1991;
Kenney, 1990; Shenep et al., 1991; Shinozaki, Deane, &
Perkins, 1988; Talo et al., 1991; Weiss, 1991; Weiss,
Pue, & Smith, 1991), temperature differences between
the right and left TMs have been negligible; but past
studies have typically employed ill and febrile participants, reported only mean left–right differences, and
ignored the possible significance of individual variability in temperature asymmetries (Boyce, Higley,
Jemerin, Champoux, & Suomi, 1996).
To meet tolerance standards set for the study, the
two readings within a given ear were required to
match within .3C degrees. The TM temperature for
each ear was computed as the mean of the two readings, and TM temperature asymmetry scores, referred to as T, were computed as the mean left-sided
temperature minus the mean right-sided temperature. Positive T scores thus indicated a warmer left
TM, and negative T scores indicated a warmer
right TM.
Psychometric Measurement
Each of the four sites employed different sets of
temperament and behavior measures, according to
the study protocols from which the participants were
drawn. The only exception was the concordant use of
the Child Behavior Questionnaire (CBQ; Rothbart,
1981) in the San Francisco, Berkeley, and Madison
samples. The four studies thus allowed a concurrent
examination of T-behavior associations using both
duplicate and contrasting psychometric measures.
Constructs and corresponding instruments unique to
each of the four sites are detailed in the study-specific
sections that follow.
Statistical Analyses
For data from each of the four studies, comparisons of TM temperatures between the left and right
sides and between boys and girls were made using
paired and unpaired t tests, respectively; and bivariate associations between TM temperatures, T asymmetry scores, and biobehavioral measures were examined with Pearson correlation coefficients. To detect
possible gender differences in temperature–behavior
associations across study sites, data were separated
by gender-specific subsamples for the correlational
analyses. Because of the exploratory nature of the current research, significance was set at a two-tailed probability level of .05, but borderline significant associations at p .10 were also noted.
GENERAL RESULTS:
MAGNITUDE AND DIRECTION OF TM
TEMPERATURE ASYMMETRIES
Frequency Distributions of T
Figure 1 summarizes the frequency distributions
for TM temperature asymmetries, T, at each of the
four sites. These data revealed that at the sample
level, mean T scores were at or near 0, indicating
approximate parity in left and right TM tempera-
Boyce et al.
723
Study 1: 4.5- to 5.5-Year-Old Kindergarten Children
(San Francisco)
Figure 1 Frequency distributions of temperature laterality
scores, T: San Francisco, CA, N 37; Berkeley, CA, N 79;
Madison, WI, N 192; and Boston, MA, N 160.
tures. Only in Boston, where inhibited children
with anxiety symptoms were intentionally oversampled, were left and right TM temperatures significantly different at a mean T of –.1C, indicating that,
on average, right TM temperatures were slightly
warmer than temperatures on the left, paired t –2.7,
p .01. This right-to-left gradient in temperatures
from the Boston sample was due principally to the
warmer right-sided temperatures found among girls
at that site. Also shown in Figure 1 is the finding that
Ts were normally and broadly distributed at all four
study sites, with difference scores ranging, at the
extremes, from approximately –1C (i.e., right side
warmer than left) to 1C (left side warmer than
right), and standard deviations from the mean on the
order of .3 to .5C.
Two additional observations were derived from inspections of gender differences in TM temperatures
and asymmetries in individual study sites. First, in
cases in which differences were found, boys’ temperatures for both the left and right sides were cooler
than those found for girls: for example in the Madison
sample, left- and right-sided temperatures averaged
36.7C for boys versus 37.0C for girls, t –5.6, p .001. Second, in two of the four sites, boys’ asymmetry scores were smaller than those of girls, a difference that was significant only in the Madison sample, t –2.0, p .05. The inconsistency of these
observations, however, suggested that no reliable
gender differences were present across the study
samples.
Participants and methods. The San Francisco sample
of 37 children was enrolled in the summer of 1994 as
the last of several sequential cohorts of kindergartners in a study of adaptation to primary school
(Boyce, Adams, et al., 1995; Boyce, Chesney, et al.,
1995; Boyce et al., 1993). The ethnic distribution of the
sample was 65% European American, 18% African
American, 12% Asian American, and 5% Hispanic
American. One week prior to kindergarten entry, children were seen in a laboratory visit during which several psychobiological response parameters were assessed, including cardiovascular reactivity (CVR) to
standardized stressors, salivary cortisol, and cellular
and humoral immune functions. Only the CVR data
are presented in this report, because they were the
only measures obtained in response to challenges
during the laboratory visit (see for a discussion of the
laboratory protocol, Boyce, Alkon, Tschann, Chesney,
& Alpert, 1995). Standardized residual scores were
used to index heart rate and mean arterial pressure
(MAP) reactivity to laboratory stressors, with higher
scores reflecting greater heart rate and MAP responses to challenge, relative to resting levels (Boyce,
Alkon, et al., 1995).
At the time of the laboratory evaluation, parents
completed two psychometric questionnaires on aspects
of children’s behavior and temperament, defined as
individual differences in reactivity and self-regulation.
Administered first was the CBQ, a 195-item temperament questionnaire with 12 subscales developed by
Rothbart (1981). Only the seven CBQ subscales deemed
relevant to positive and negative affectivity (activity
level, anger, fear, high-intensity pleasure, inhibitory
control, shyness, and low-intensity pleasure) were
utilized for the present analyses to examine possible
associations of TM temperature asymmetries to behaviors linked to lateralities in prefrontal cortical activity. Mothers were asked to rate their child’s behavior in the past week on a scale of 1 (never) to 7
(always), with an option to indicate “does not apply.”
Second, five-item instruments designed for the
present study were used to index maternal reports on
three other aspects of observable child behavior
thought to be plausibly related to T: children’s
acoustic startle response, food and taste aversions,
and capacities for imaginative involvement (see, e.g.,
Schmidt & Fox, 1998). Startle questions included
items such as “This child is easily startled by loud,
unexpected noises” and “When surprised or startled,
this child may stiffen or fall.” Taste aversion items
included “This child is a ‘picky eater’; he/she will
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Child Development
eat only a very limited variety of foods” and “This
child dislikes foods with ‘strong’ tastes, such as pickles,
lemon, fish, or garlic.” Imaginative involvement
items were statements such as “This child has an
unusually vivid imagination” and “This child loves
to play ‘dress up’ and pretend being someone else.”
Items were scored on a 3-point scale, labeled “not true”
(scored 0), “somewhat or sometimes true” (scored 1),
and “very true or often true” (scored 2). Item scores
were summed to generate three variables designated
startle response, taste aversions, and imagination.
Finally, kindergarten teachers for each of the 37
children in the sample were asked to complete the abbreviated, 30-item version of the Preschool Socioaffective Profile (La Frenière, Dumas, Capuano, Coutu,
& Giuliani, 1993), a well-validated teacher-report instrument with three factors representing internalizing and externalizing behavior problems and social
competence. The questionnaire has been shown to
have high interrater reliability, .72–.89; internal
consistency, Cronbach’s .79–.93; 2-week test–retest
stability, .76–.87, and strong concurrent validity
with direct observations of social participation and
peer sociometry (La Frenière, Dumas, Capuano, &
Dubeau, 1992).
Results. Among boys, TM temperature asymmetry
scores, T, were significantly and strongly associated
with several biobehavioral measures, as shown in Table 2. Significant correlation coefficients are shown in
boldfaced type, whereas significant and hypothesized associations are shown with suprascripts designating their consistency with Hypothesis 1 or Hypothesis 2. Heart rate reactivity and externalizing
behavior problems were inversely related to T, r –.62
and –.60, ps .01, respectively, whereas the activity
and low-intensity pleasure subscales of the CBQ and
maternal reports of imagination were positively associated with T, r .60, p .01; r .53, p .05; and
r .49, p .05, respectively. Each of these is consistent with the pattern of T results predicted by Hypothesis 1. Unexpectedly, maternal ratings of acoustic
startle response were positively related to T, r .51,
p .05. There was also a trend toward a positive association between T and social competence, but
again, only in the male subsample. TM asymmetry
was unrelated to any of the dependent measures in
girls.
Unilateral TM temperatures, however, were related
to behavioral measures in both boys and girls. Left
TM temperature was positively related to social com-
Table 2 Correlations between Biobehavioral Measures and Left Tympanic Membrane (TM) Temperatures, Right TM Temperatures, and Temperature Asymmetry Scores, San Francisco, CA Site
Left TM
Cardiovascular reactivity
Standardized residual heart rate
Standardized residual mean
arterial pressure
Right TM
T
(Left Right)
.11/.08
.16/.07
.03/.09
.10/.13
.16/.11
.11/.11
.05/.53*b
.44/.34
.03/.36
.05/.08
.08/.15
.45/.05
.35/.17
.10/.55*b
.49*/.37
.11/.41
.10/.09
.14/.08
.39/.11
.60**a/.18
.35/.00
.18/.06
.35/.13
.12/.03
.53*a/.25
.10/.18
Maternal reports
Startle responses
Taste aversions
Imagination
.11/.28
.12/.10
.18/.02
.31/.29
.25/.10
.37/.02
.51*/.00
.34/.03
.49*a/.00
Preschool Socio-affective Profile
Internalizing
Externalizing
Social competence
.09/.01
.33/.30
.55*a/.02
.06/.01
.08/.33
.36/.14
.37/.08
.60**a/.08
.46/.37
Child Behavior Questionnaire
Activity level
Anger
Fear
High-intensity pleasure
Inhibitory control
Low-intensity pleasure
Shyness
.62**a/.05
Note: N 37. Values shown are Pearson correlation coefficients, boys/girls. Significant associations
are shown in bold.
a Association consistent with Hypothesis 1.
b Association consistent with Hypothesis 2.
*p .05; ** p .01; p .10 (two-tailed).
Boyce et al.
petence among boys, r .55, p .05 and inversely related to anger expression among girls, r –.53, p .05,
as predicted by Hypothesis 1. Unpredicted, significant inverse associations were found in the girls
between the CBQ anger expression subscale and
right TM temperatures, r –.55, p .05 and, among
boys, between right TM temperatures and fearfulness, r –.49, p .05.
Collectively, the pattern of correlations found in
the Berkeley site suggest two regularities. First, although left and right unilateral TM temperatures
were related to behavioral measures in children of
both gender, temperature asymmetries were associated with behavior only in boys. Second, and consistent with Hypothesis 1, warmer left-sided temperatures were generally linked to competent, affectively
positive behaviors (e.g., greater imaginative capacities, higher levels of activity, low-intensity pleasures,
and stronger social competence), whereas warmer
right-sided temperatures were often related to more
problematic and/or affectively negative behaviors
(e.g., more externalizing behavior problems and
greater cardiovascular reactivity).
Study 2: 4- to 8-Year-Old Children in a Community
Sample (Berkeley)
Participants and methods. Children ranging in age
from 4 to 8 years were recruited from the Berkeley
community for a 1995 to 1998 pilot project involving
the design and implementation of a standardized laboratory protocol for measuring psychobiological reactivity to challenge in middle childhood (Boyce et
al., 2001). Parents responded to fliers and bulletins
distributed in preschools, on Websites, and parenting
newsletters, and participating children reflected the
multiethnic population of the San Francisco Bay Area.
Of the 79 children enrolled, 53% were European
American, 11% were African American, 10% were
Asian American, 6% were Hispanic American, and
20% were biracial or of other ethnicity.
Children in this study underwent a 60-min laboratory paradigm in which psychobiological parameters
were monitored under conditions of interpersonal,
cognitive, physical, and emotional challenge. Tympanic membrane temperatures were assessed twice in
this study’s protocol: once at baseline before the commencement of the standardized challenges, and again
30 min into the laboratory procedure. Because the
first of these measurements most closely replicated
the measurement conditions of the other three studies,
only those TM temperatures were utilized in the reported analyses. While children began the laboratory
portion of the study, mothers completed the CBQ in
725
an adjacent waiting room. As in Study 1, only the
seven subscales relevant to the negative and positive
affectivity dimensions of children’s behavior were
used in the analyses of data.
Results. As shown in Table 3, several significant associations emerged from correlational analyses of
unilateral TM temperatures and behavioral data, although no such associations were identified with T.
As predicted by Hypothesis 1, girls’ left TM temperatures were positively correlated with inhibitory control and inversely associated with anger, rs .36 and
–.33, p .05, respectively, and boys’ right-sided temperatures were inversely related to high intensity
pleasure and positively related to shyness, rs –.30
and .32, ps .05, respectively. Among girls, right TM
temperatures were unexpectedly and inversely associated with anger expression, r –.34, p .05.
This pattern of findings is commensurate with that
of Study 1 and, more generally, with a hypothesized
tendency for warmer left-sided temperatures to be associated with socially competent behavior, such as a
capacity for inhibitory control, and warmer rightsided temperatures to be linked with affectively negative behaviors, such as shyness (Hypothesis 1).
Study 3: 3- to 5-Year-Old Children in a Longitudinal
Cohort (Madison)
Participants and methods. Children and families at
the Madison site were recruited in 1990 and 1991 to
represent as broad a spectrum of ethnicity and social
class as possible, given requirements for participation
Table 3 Correlations between Biobehavioral Measures and Left
Tympanic Membrane (TM) Temperatures, Right TM Temperatures, and Temperature Asymmetry Scores, Berkeley, CA Site
Left TM
Temperament at
3.5 and 4.5 years
Activity level
Anger
Fear
High-intensity
pleasure
Inhibitory control
Low-intensity
pleasure
Shyness
Right TM
T
(Left – Right)
.01/.14
.12/.34*b
.08/.31
.20/.06
.14/.03
.00/.11
.09/.11
.02/.36*a
.10/.00
.30*a/.30
.25/.28
.00/.26
.23/.21
.26 /.07
.11/.28
.09/.09
.32*a/.05
.25/.04
.17/.09
.01/.33*b
.07/.22
Note: N 79. Values shown are Pearson correlation coefficients,
boys/girls. Significant associations are shown in bold.
a Association consistent with Hypothesis 1.
b Association consistent with Hypothesis 2.
* p .05; p .10 (two-tailed).
726
Child Development
and the study’s geographical location. For current
analyses, data were utilized from a subset of the
WSFW sample during the study cohort’s periodic
assessment at 4.5 years of age. Associations were examined between TM temperature asymmetry scores
ascertained at 4.5 years and characteristics of both
earlier and concurrent temperament and behavior. At
the time of data collection for these purposes, 408
families (72%) remained in the geographic area and
were available for home assessments. Children and
their mothers participated in a 2-hr, in-home observational assessment of mother–child interactions and
child temperament. As part of the assessment, TM
temperatures were obtained from children approximately halfway through the evaluation. Using the exclusion criteria described above, a subsample of 192
children was identified for the present analyses.
Within the subsample, the average age was 4.5 years;
92% of enrolled families were European American,
4% were African American, and 4% were of other ethnicities (Asian, Hispanic, or Native American); 72%
were dual-earner families; 95% were married; and
median family income was $64,000 per annum.
As components of the longitudinal study, mothers
had been interviewed in their homes on four occasions, when the children were 4 months, 12 months,
3.5 years, and 4.5 years of age. Fathers had been interviewed by telephone at the same time points, and, at
each assessment interval, mothers and fathers completed mailed questionnaires. When the children
were 3.5 and 4.5 years old, a nonparental adult who
knew the child well (e.g., a child-care provider, preschool teacher, neighbor, or grandparent) was also interviewed and completed a mailed questionnaire
about the child.
Child temperament was measured with the Infant
Behavior Questionnaire (IBQ) during the infancy period and with the CBQ during the preschool period.
Temperament scores at 4 and 12 months were multiplied so that high scores would reflect more stable
temperamental characteristics during the infancy period. Scores at 3.5 and 4.5 years and measures of child
affect and prosocial and problem behaviors, obtained
separately from mothers and other adults, were treated
in the same way. As at the San Francisco and Berkeley
sites, IBQ and CBQ subscales were selected to represent aspects of reactivity and self-regulation most
likely related to TM temperature asymmetries. (The
sets of CBQ subscales used with the San Francisco/
Berkeley and Madison samples were partially nonoverlapping, due to the use of different versions of
the questionnaire at the two geographical sites.) For
measures of child affectivity, mothers and nonparental adult reporters completed the Positive and Nega-
tive Affect Scale (Watson, Clark, & Tellegen, 1988), and
behavior problems were assessed using the Preschool Behavior Questionnaire (PBQ; Behar & Stringfield, 1974), a 30-item questionnaire that yields three
subscales labeled (1) hostile–aggressive, (2) anxious–
fearful, and (3) hyperactive–distractible. The Adaptive Social Behavior Inventory (Hogan, Scott, & Bauer,
1992) is a 30-item, 3-point scale designed to assess
prosocial and adaptive behaviors in preschool-age
children. It yields three subscales, two of which are
nonoverlapping with the PBQ: positive expressivity
and compliance; these two subscales were combined
into a single prosocial measure.
Results. Table 4 shows gender-specific bivariate
correlations among TM temperature scores and reports of children’s temperament and behavior during
the infancy and preschool periods for the Madison
sample. Significant correlations between T and behavioral variables were found for both genders.
Among boys, temperature asymmetries were positively associated with soothability in infancy, r .24,
p .05, and with attentional focus, inhibitory control,
and prosocial behavior at 3.5 and 4.5 years, r .26,
p .05, rs .31 and .30, ps .01, respectively. Inverse
associations with T were found in boys for distress
to novelty in infancy, r –.24, p .05; anger, r –.32,
p .01; negative affect, r –.36, p .001; hostile–
aggressive, r –.27, p .05; and hyperactive–
distractible, r –.36, p .001; at 3.5 and 4.5 years.
Among girls in the Madison sample, a positive association with T was found only for prosocial behavior,
r .20, p .05. Significant inverse associations in
girls were observed between TM asymmetry scores
and anger, r –.23, p .05; shyness, r –.21, p .05;
and anxious–fearful, r –.22, p .05. These associations between T and behavior were universally in
the directions predicted by Hypothesis 1.
Relations between unilateral TM temperatures and
behavioral measures were also identified for both
boys and girls. Left TM temperatures were inversely
associated with shyness and negative affect, rs –.25
and –.24, ps .05, respectively, in boys and with anger, r –.24, p .05; shyness, r –.21, p .05; negative affect, r –.32, p .001; hostile–aggressive, r –.22,
p .05; and anxious–fearful, r –.20, p .05, in girls.
Higher right-sided temperatures were associated
only with less soothability in infant boys, r –.23,
p .05, and greater hyperactivity–distractibility in
preschool-age boys, r .32, p .01. Again, each such
association was consistent in the direction predicted
by Hypothesis 1.
As in Studies 1 and 2, the Madison findings suggest overall that warmer left TMs were related to positive emotion and socially competent behaviors,
Boyce et al.
727
Table 4 Correlations between Biobehavioral Measures and Left Tympanic Membrane (TM) Temperatures, Right TM Temperatures, and Temperature Asymmetry Scores, Madison, WI Site
T
(Left Right)
Left TM
Right TM
Temperament at 4 and 12 months
Distress to novelty
Soothability
.03/.07
.02/.06
.16/.01
.23*a/.03
.24*a/.11
.24*a/.11
Temperament at 3.5 and 4.5 years
Activity level
Anger
Approach
Attentional focus
Fear
Inhibitory control
Shyness
.04/.07
.07/.24*
.03/.10
.08/.09
.05/.11
.06/.20
.25*a/.21*a
.05/.04
.20/.05
.04/.00
.13/.13
.12/.08
.20/.07
.20/.03
.12/.14
.32**/.23*
.08/.12
.26*a/.27
.09/.04
.31**a/.16
.04/.21*a
Affectivity at 3.5 and 4.5 years
Positive affect
Negative affect
.07/.13
.24*a/.32***a
.02/.12
.07/.16
.10/.02
.36***a/.19
.20/.16
.17/.22*a
.07/.20*a
.02/.14
.05/.00
.06/.16
.01/.02
.32**a/.01
.30**a/.20*a
.27*a/.07
.10/.22*a
.36***a/.16
Prosocial and problem behaviors
at 3.5 and 4.5 years
Prosocial behaviors
Hostile–aggressive
Anxious–fearful
Hyperactive–distractible
Note: N 192. Values shown are Pearson correlation coefficients, boys/girls. Significant associations
are shown in bold.
a Association consistent with Hypothesis 1.
b Association consistent with Hypothesis 2.
* p .05; ** p .01; *** p .001; p .10 (two-tailed).
whereas warmer right TMs were more often tied to
problematic, emotionally negative behaviors. The inverse associations of T with shyness and anxious–
fearful behavior, along with its positive relations with
attentional focusing and prosocial behavior, are examples in both genders of this recurring pattern of
findings. Results of Study 3 also suggest that behavioral linkages with TM temperatures and temperature asymmetries may extend backward to developmental periods as early as infancy.
Study 4: 6 to 8-Year-Old Children in a Longitudinal
Cohort (Boston)
Participants and methods. The Boston sample of one
hundred and sixty 6- to 8-year-old children (M 7.3
years) was followed in an ongoing, longitudinal
study of behaviorally inhibited and uninhibited children enrolled in 1988 to 1990 (Kagan, 1994). Children
were all European American and from middle-class
families, characteristic of Cambridge, MA. The temperamental characteristics, especially fearfulness, of a
larger group of children (N 462) had been previously assessed at 14 and 21 months of age. When the
large sample was between 5 and 7 years of age, a parent questionnaire that assessed children’s symptoms
of anxiety was mailed to the homes of this sample and
completed by 73% of the parents. If the scoring of the
parent questionnaire achieved a criterion level of anxious symptoms and behaviors, the child’s teacher was
contacted by telephone and interviewed with regard
to the child’s level of anxious behavior relative to
other children in the same classroom. Two subsamples of children were then selected for which there
were concordant parent and teacher appraisals of
either high or low symptoms of anxiety. A total of 57
children with high anxiety symptom levels and 103
with low symptoms was used as the study sample for
the 1995–1996 measurement of TM temperatures.
TM temperature assessments were done during a
1-hr laboratory assessment completed on all children
in the longitudinal study cohort at approximately 7
years of age. Temperature measurements were carried out using instrumentation and procedures identical to those in Studies 1 through 3. Fearfulness at 14
and 21 months was assessed using a sequence of stimulus episodes: an examiner in a white coat applying
electrodes and a blood pressure cuff; a rotating, noise-
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Child Development
generating wheel; a taste of a lemon juice; puppets; a
clown; and a stranger entering the playroom and sitting a few feet away. Patterns of reactivity and fearfulness were evaluated using both physiologic and behavioral data, including heart rate and blood pressure
responses, facial expressions, crying and vocalization, approach to the examiner and stranger, and motor activity. Anxious symptoms were ascertained
with parent interviews when children were between
5 and 7 years of age, using the Diagnostic Interview
for Children and Adolescents–Parent Version (Herjanic & Reich, 1982).
Results. Table 5 shows Study 4 correlation coefficients for bivariate relations identified between TM
temperature measures and variables describing infant and middle childhood behavior. No statistically
significant associations with T were identified in the
Boston sample. Other associations were found, however, between bilateral TM temperatures and behavioral variables in the female subset of Boston children.
Commensurate with Hypothesis 2, girls’ bilateral TM
temperatures were positively and significantly related to both fearfulness during infancy and anxious
symptoms reported by parents and teachers, rs .23–.37, ps .05–.001.
Examined together, results from the Boston cohort
indicate that the strongest and only significant associations were found in girls, and that negative affectivity (fearfulness and anxious symptoms) was related
to warmer TM temperatures bilaterally, as predicted
by Hypothesis 2.
GENERAL DISCUSSION
Analyses of data from each of the four studies produced findings that, although distinctive in certain
ways from site to site, shared several commonalities.
Employing identical instrumentation for measuring
TM temperatures, the San Francisco, Berkeley, Madi-
Table 5 Correlations between Biobehavioral Measures and
Left Tympanic Membrane (TM) Temperatures, Right TM Temperatures, and Temperature Asymmetry Scores, Boston, MA Site
Left TM
Right TM
Fearfulness at 14 months .05/.37***a .20/.37***a
Fearfulness at 21 months .12/.27**a
.14/.23*a
Anxious symptoms
.15/.28**a
.14/.25*a
T
(Left Right)
.22/.00
.03/.08
.01/.05
Note: N 160. Values shown are Pearson correlation coefficients,
boys/girls. Significant associations are shown in bold.
a Association consistent with Hypothesis 2.
* p .05; ** p .01; *** p .001; p .10 (two-tailed).
son, and Boston studies converged on three principal
observations. First, TM temperatures appeared to be
related in some manner to aspects of temperament
and biobehavioral reactivity. Although the configuration and magnitude of the associations varied, each
site found significant and consistent correlations between TM temperatures and aspects of individual
child behavior. These associations are unlikely to be
attributable to the operation of chance alone. Of the
240 bivariate relations examined in the collective
sample of 468 study children, 43 of these (18%)
showed significant correlations, a number that exceeded by a factor of nearly four the 12 that could
have been expected solely on the basis of chance, at an
probability level of .05. Further, 39 of the 43 statistically significant associations (91%) were in a direction
consistent with the relations between TM temperatures and child behavior predicted by Hypothesis 1 or
Hypothesis 2.
Second, there were substantial commonalities in
the patterns and directions of the observed associations. In all four studies, children with warmer right
TMs, relative to cooler left TMs (i.e., those children in
whom negative T asymmetries were identified)
were characterized as showing more affectively negative and problematic behaviors. In contrast, significant correlations were noted between positive TM
temperature asymmetry scores (i.e., relatively warmer
left TMs) and aspects of positive affectivity or socially
competent behaviors. The latter profile suggests that
children with warmer left TMs display what Rothbart has referred to as “surgency” behavior (Rothbart,
Ahadi, & Hershey, 1994; Rothbart & Derryberry, 1982).
Surgent children are active, risk-taking, socially competent individuals who move easily and actively into
novel settings and display high levels of positive affect (Gunnar, Tout, de Haan, Pierce, & Stansbury, 1997).
The third observation was a set of associations relating unilateral TM temperatures to aspects of temperament and behavior. Consistent with the present
research’s hypotheses, the problematic behavioral
characteristics of more affectively negative children
were correlated with (1) lower left-sided temperatures, (2) higher right-sided temperatures, and/or (3)
higher TM temperatures on both left and right. Also
commensurate with hypothesized relations, the behaviors of surgent, high positive affect children were
associated with either (1) higher left-sided temperatures, or (2) lower right-sided temperatures.
These commonalities across studies were consistent with predictions based on the known neurobiology and correlates of circulatory and cortical asymmetries, and with prior single-study observations of
TM temperature–behavior associations. Electroen-
Boyce et al.
cephalographic studies of emotional dysregulation
for example, have demonstrated (1) asymmetrical activation of the right frontal area in depressed participants (Henriques & Davidson, 1990, 1991), young
children of depressed mothers (Dawson et al., 1997),
and intensely shy children (Davidson, 1995); (2) lateralized activation of the left hemisphere in mania
(Migliorelli et al., 1993); and (3) bilateral activation of
the frontal cortex in depressed, inhibited, and affectively vulnerable children under emotionally evocative conditions (Dawson, Panagiotides, Klinger, &
Hill, 1992). Thus, consistent with the present findings,
negative affectivity has been associated both with enhanced activation of the right frontal region relative
to the left, and with greater bilateral frontal activation
compared with levels found in less vulnerable children. There is also evidence that cerebral blood flow
increases in areas of cortical activation (Rowell,
1986a), reflecting heightened metabolic needs associated with increased regional cortical activity. Because
the TMs are perfused by the arterial system supporting ipsilateral cortical structures and neural circuitry
(Benzinger & Taylor, 1963; Webb, 1973), it is plausible
to propose that TM temperatures may indirectly index cerebral blood flow and thus cortical activation
on the left and right sides of the brain.
These conclusions are strengthened by a small but
growing literature on TM temperature asymmetries
and their correlates in human and nonhuman primate behavior. Hopkins and Fowler (1998), for example, found lateralized changes in TM temperatures
in chimpanzees engaged in cognitive tasks. During
match-to-sample and visual–spatial discrimination
tasks, chimps showed increasing temperatures in the
left TM and concurrent decreases in the right. The authors concluded that asymmetries in cognitive functions were subserved by changes in cerebral blood
flow and reflected in the lateralized alterations in TM
temperatures. In pilot work with small samples of 2year-old rhesus macaques and 8-year-old children,
Boyce and colleagues (1996) found significant differences between left- and right-side TM temperatures,
with the left side slightly warmer on average compared with the right, in both groups. Surprisingly,
temperature asymmetries were associated with some
aspects of behavior in a direction opposite to that
found in the present work; for example, warmer left
TM temperatures were correlated with lower resilience and more behavior problems in the children.
Consistent with the current results, however, greater
exploratory locomotion and lower adrenocorticotropic hormone and cortisol levels were found during
maternal separations in early infancy among monkeys with larger Ts. Discrepancies between the pre-
729
vious and current studies may be accounted for by
differences in sample size, selective factors in subject
recruitment, gender effects, and conditions under
which the measurements were made.
In other human studies, Meiners and Dabbs (1977)
found differential reductions in left- and right-sided
TM temperatures during spatial and verbal tasks,
whereas Swift (1991) reported larger TM temperature
increases during higher cognitive tasks on the side
concordant with known hemispheric specializations
in cognition. Citing evidence that cortical temperatures increase with cognitive performance in rats
(Ahlers, Thomas, & Berkey, 1991), Swift (1991) maintained that elevations in TM temperatures should reflect enhanced ipsilateral cortical activation. More
recently, Mariak, Lewko, Luczaj, Polocki, and White
(1994) acquired direct temperature measurements
from the cerebral surface, TM, forehead, esophagus,
and rectum in patients undergoing open-cranial
neurosurgical procedures. Tympanic membrane temperatures were the most accurate approximations of
cerebral temperatures and were found to be reciprocally related to forehead temperatures. The latter
finding may reconcile the current work, which found
cooler left TMs among inhibited children, with Kagan’s
findings of cooler right foreheads among children
classified as inhibited (Kagan, 1994). Finally, Zajonc,
Murphy, and Inglehart, (1989) presented data suggesting that facial muscle activity during emotional
expression may itself induce affective responses due
to its capacity for restricting venous flow from the
cavernous sinus, thereby cooling arterial blood en
route to specific brain regions. To the degree that facial emotional expression is asymmetrical (Sackheim
et al., 1978), side-to-side differences in facial muscle
activity might alter unilateral blood flow to the cerebrum and TM. Common to each of these studies are
observations that differences in cerebral and TM temperatures, and their lateral asymmetries, may be reliably associated with aspects of behavior, emotion regulation, and cognition.
It is important to acknowledge that the associations reported in the present research were often
modest in magnitude, accounting for small percentages of variance in dependent biobehavioral measures. This suggests that whatever coupling may exist
between a single measure of TM temperature asymmetry and complex behavioral proclivities, the linkages are predictably distant, imprecise, and unlikely
to be monotonic in character. Although the reported
associations were often only moderate in size, they
are largely consistent in direction and configuration,
and the pattern is plausibly concordant with prior
findings regarding brain laterality, cerebral blood
730
Child Development
flow, temperament, and emotion regulation. The relevance of the current research’s results thus resides not
in the magnitude of individual associations, but rather
in the patterned consistencies identified across study
samples and in the possible utility of temperature lateralities as a risk marker for behavioral disorders.
Other researchers have attempted to identify
readily observable phenotypic characteristics of children at risk for developmental psychopathologies.
Kagan and colleagues have suggested that blue iris
pigmentation (Rosenberg & Kagan, 1987) and a narrow facial width (Arcus & Kagan, 1995) may be external markers for a constellation of biobehavioral attributes comprising extreme shyness and exaggerated
psychobiological reactivity. Other investigators have
similarly noted an association between eye color and
social wariness (Rubin & Both, 1989; Samuels &
Block, 1995), and in one study the linkage between
blue eyes and inhibition was found for boys, but not
for girls (Coplan, Coleman, & Rubin, 1998). TM temperature asymmetries might similarly constitute a somatic marker that could be employed to screen for
biobehavioral vulnerabilities. Early identification of
children at risk could arguably assist in boosting the
low recognition and referral rates for children with
psychopathological conditions presenting to primary
care settings (Costello et al., 1988).
The findings presented in this article should be
assessed with the studies’ shortcomings in mind.
First, none of the four study samples were randomly
ascertained, and thus none can claim to be representative of the broader childhood populations from
which each was derived. The heterogeneities in geographic representation and sampling frames, however, render the observed commonalities in the four
studies’ findings more credible and noteworthy. Second, the settings and circumstances in which TM temperatures were measured varied widely from study
to study. This diversity in measurement conditions
may well have contributed to the variations noted
across sites in the magnitude of associations and in
the character of gender effects. Third, TM temperature measures were made using infrared thermometers, the accuracy and reliability of which has been
questioned in past work comparing TM and core
body temperatures, especially for children less than 3
years of age (see, e.g., Petersen-Smith, Barber, Coody,
West, & Yetman, 1994). Almost certainly, a considerable level of imprecision was present in the measurement of TM temperatures in the current four studies,
as reflected in the magnitude of standard deviations
around their sample means. On the other hand, recent
studies have validated the accuracy of TM infrared
thermometry against true core body temperatures,
such as pulmonary artery temperature (Robinson,
Seal, Spady, & Joffres, 1998), and comparisons of
infrared versus direct contact temperature measurements on the TM have further confirmed the accuracy
of infrared TM thermometry (Terndrup, Crofton, Mortelliti, Kelley, & Rajk, 1997). Newer instrumentation,
such as the Oto-Temp® TM thermometer by Exergen,
may offer greater precision and reliability in the measurement of TM temperatures (Imamura et al., 1998),
and is currently in use in the laboratories represented
in this report. Fourth, dependent measures at all four
study sites were limited primarily, although not exclusively, to parental reports of child behavior, a method
with known limitations in the reliable assessment of
child temperament. Finally, statistical analyses of data
from the four studies, each divided by gender, necessitated computation of multiple correlation coefficients,
raising concern over an inflation of Type I errors. Far
more significant correlations were identified than
could be explained by chance, many of these were of
substantial magnitude, and they were found almost
universally in a direction consistent with hypothesized relations. Nonetheless, the interpretive hazards
of multiple statistical tests should be considered in
evaluating the results of the present research.
Like all exploratory work, these studies raised
more questions than were currently answered. Among
such questions are the following: Is TM temperature asymmetry a state or trait variable? To what extent is T stable or reactive over time? At least one
study of chimpanzees suggests that TM laterality is
responsive to environmental demands (Hopkins &
Fowler, 1998). Are TM temperature asymmetries correlated with lateralities in frontal EEG activation, as
we have argued in this article may be the case? Similarly, are asymmetries associated with side-to-side,
activation-related shifts in cerebral blood flow? Both
of the latter questions are answerable with EEG and
neuroimaging technologies currently available. Finally, are temperature asymmetries predictive of developmental or psychiatric outcomes? Early identification of children at risk for childhood and adolescent
psychiatric morbidities is an important first element
in a larger strategy for primary prevention of developmental psychopathology. The findings presented
in this article, although provisional and, to some degree, speculative in nature, suggest that the search for
new phenotypic markers of neurodevelopmental vulnerability may be an important agenda for continuing
research. Targeted, early interventions for children
susceptible to mental disorders may be achievable,
and the use of noninvasive measures of risk status
could play an important role in the identification of
such children.
Boyce et al.
ACKNOWLEDGMENT
This work was supported by the John D. and Catherine T.
MacArthur Foundation Research Network on Psychopathology and Development and by grants from
the National Institute of Mental Health (MH44340)
and the William T. Grant Foundation (90-1306-89).
ADDRESSES AND AFFILIATIONS
Corresponding author: W. Thomas Boyce, Institute
of Human Development and School of Public Health,
University of California, 570 University Hall, Berkeley,
CA 94720-1190; e-mail: [email protected].
Marilyn Essex and Nancy Smider are at the University of Wisconsin, Madison; Abbey Alkon is at the
School of Nursing, University of California, San Francisco; Tyler Pickrell is at the University of Arizona,
Tucson; and Jerome Kagan is at Harvard University,
Cambridge, MA.
REFERENCES
Ahlers, S. T., Thomas, J. R., & Berkey, D. L. (1991). Hippocampal and body temperature changes in rats during
delayed matching-to-sample performance in a cold environment. Physiology and Behavior, 50, 1013–1018.
Arcus, D., & Kagan, J. (1995). Temperament and craniofacial
variation in the first two years. Child Development, 66,
1529–1540.
Behar, L., & Stringfield, S. (1974). A behavior rating scale for
the preschool child. Developmental Psychology, 10, 601–
610.
Benzinger, T. H., & Taylor, G. W. (1963). Temperature—Its
measurement and control in science and industry (Vol. 3).
New York: Reinhold.
Bevan, R., Dodge, J., Nichols, P., Poseno, T., Vijayakumaran,
E., Wellman, T., & Bevan, J. A. (1998). Responsiveness of
human infant cerebral arteries to sympathetic nerve
stimulation and vasoactive agents. Pediatric Research, 44,
730–739.
Boyce, W. T., Adams, S., Tschann, J. M., Cohen, F., Wara, D.,
& Gunnar, M. R. (1995). Adrenocortical and behavioral
predictors of immune responses to starting school. Pediatric Research, 38, 1009–1017.
Boyce, W. T., Alkon, A., Tschann, J. M., Chesney, M. A., &
Alpert, B. S. (1995). Dimensions of psychobiologic reactivity: Cardiovascular responses to laboratory stressors
in preschool children. Annals of Behavioral Medicine, 17,
315–323.
Boyce, W. T., Chesney, M., Alkon-Leonard, A., Tschann, J.,
Adams, S., Chesterman, B., Cohen, F., Kaiser, P., Folkman, S., & Wara, D. (1995). Psychobiologic reactivity to
stress and childhood respiratory illnesses: Results of two
prospective studies. Psychosomatic Medicine, 57, 411–422.
Boyce, W. T., Chesterman, E. A., Martin, N., Folkman, S.,
Cohen, F., & Wara, D. (1993). Immunologic changes oc-
731
curring at kindergarten entry predict respiratory illnesses following the Loma Prieta earthquake. Journal of
Developmental and Behavioral Pediatrics, 14, 296–303.
Boyce, W. T., Higley, J. D., Jemerin, J. J., Champoux, M., &
Suomi, S. J. (1996). Tympanic temperature asymmetry
and stress behavior in rhesus macaques and children.
Archives of Pediatrics and Adolescent Medicine, 150, 518–
523.
Boyce, W. T., Quas, J., Alkon, A., Smider, N., Essex, M., &
Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry,
179, 144–150.
Branston, N. M. (1995). Neurogenic control of the cerebral
circulation. Cerebrovascular & Brain Metabolism Reviews,
7, 338–349.
Chamberlain, J. M., Grandner, J., Rubinoff, J. L., Klein, B. L.,
Waisman, Y., & Huey, M. (1991). Comparison of a tympanic thermometer to rectal and oral thermometers in
a pediatric emergency department. Clinical Pediatrics,
30(Suppl.), 24–29.
Chang, T. (1993). Forehead temperature asymmetries and temperament in four month old infants. Unpublished baccalaureate Honors thesis, Harvard-Radcliffe College, Cambridge, Massachusetts.
Chrousos, G. P., & Gold, P. W. (1992). The concepts of stress
and stress system disorders: Overview of physical and
behavioral homeostasis. Journal of the American Medical
Association, 267, 1244–1252.
Cohen, P., Pine, D. S., Must, A., Kasen, S., & Brook, J. (1998).
Prospective associations between somatic illness and
mental illness from childhood to adulthood. American
Journal of Epidemiology, 147, 232–239.
Coplan, R. J., Coleman, B., & Rubin, K. H. (1998). Shyness
and little boy blue: Iris pigmentation, gender, and social
wariness. Developmental Psychobiology, 32, 37–44.
Costello, E. J., Edelbrock, C. S., Costello, A. J., Dulcan, M. K.,
Burns, B. J., & Brent, D. (1988). Psychopathology in pediatric primary care. Pediatrics, 82, 415–424.
Davidson, R. J. (1988). EEG measures of cerebral asymmetry: Conceptual and methodological issues. International
Journal of Neuroscience, 39, 71–89.
Davidson, R. J. (1995). Cerebral asymmetry, emotion, and
affective style. In R. J. Davidson & K. Hugdahl (Eds.),
Brain asymmetry (pp. 361–387). Cambridge, MA: MIT Press.
Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants’ response to maternal separation.
Journal of Abnormal Psychology, 98, 127–131.
Dawson, G. (1994). Development of emotional expression
and emotion regulation in infancy: Contributions of the
frontal lobe. In G. Dawson & K. W. Fishcher (Eds.), Human behavior and the developing brain. New York: Guilford
Press.
Dawson, G., Frey, K., Panagiotides, H., Osterling, J., &
Hessl, D. (1997). Infants of depressed mothers exhibit
atypical frontal brain activity: A replication and extension of previous findings. Journal of Child Psychology and
Psychiatry, 38, 179–186.
Dawson, G., Hessl, D., & Frey, K. (1994). Social influences
on early developing biological and behavioral systems
732
Child Development
related to risk for affective disorder. Development and
Psychopathology, 6, 759–779.
Dawson, G., Panagiotides, H., Klinger, L. G., & Hill, D.
(1992). The role of frontal lobe functioning in the development of infant self-regulatory behavior. Brain and Cognition, 20, 152–175.
Fox, N. A. (1991). If it’s not left, it’s right: Electroencephalograph asymmetry and the development of emotion.
American Psychologist, 46, 863–872.
Fox, N. A., Rubin, K. H., Calkins, S. D., Marshall, T. R.,
Coplan, R. J., Porges, S. W., Long, J. M., & Stewart, S.
(1995). Frontal activation asymmetry and social competence at four years of age. Child Development, 66, 1770–
1784.
Gomez, B. (1976). Presence of alpha and beta adrenergic
tone in the walls of cerebral blood vessels. In J. CervosNavarro (Ed.), The cerebral vessel wall (pp. 139–142). New
York: Raven Press.
Gould, S. J. (1995). Left snails and right minds. Natural History (April), 10–18.
Gray, J. A. (1982). The neuropsychology of anxiety. New York:
Oxford University Press.
Gray, J. A. (1987). The psychology of fear and stress. New York:
Cambridge University Press.
Gunnar, M. R., Tout, K., de Haan, M., Pierce, S., & Stansbury, K. (1997). Temperament, social competence, and
adrenocortical activity in preschoolers. Developmental
Psychobiology, 31, 65–85.
Hagemann, D., Naumann, E., Becker, G., Maier, S., & Bartussek, D. (1998). Frontal brain asymmetry and affective
style: A conceptual replication. Psychophysiology, 35, 372–
388.
Henriques, J. B., & Davidson, R. J. (1990). Regional brain
electrical asymmetries discriminate between previously
depressed subjects and healthy controls. Journal of Abnormal Psychology, 99, 22–31.
Henriques, J. B., & Davidson, R. J. (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology,
100, 535–545.
Herjanic, B., & Reich, W. (1982). Development of a structured psychiatric interview for children: Agreement between child and parent. Journal of Abnormal Child Psychology, 10, 307–324.
Hogan, A. E., Scott, K. G., & Bauer, C. R. (1992). The Adaptive Social Behavior Inventory: A new assessment of social competence in high-risk 3-year-olds. Journal of Psychoeducational Assessment, 10, 230–239.
Hopkins, W. D., & Fowler, L. A. (1998). Lateralized changes
in tympanic membrane temperature in relation to different cognitive tasks in chimpanzees (Pan troglodytes). Behavioral Neuroscience, 112, 83–88.
Hyde, J. S., Klein, M. H., Essex, M. J., & Clark, R. (1995). Maternity leave and women’s mental health. Psychology of
Women Quarterly, 19, 257–285.
Imamura, M., Matsukawa, T., Ozaki, M., Sessler, D. I., Nishiyama, T., & Kumazawa, T. (1998). The accuracy and precision of four infrared aural canal thermometers during
cardiac surgery. Acta Anaesthesiologica Scandinavica, 42,
1222–1226.
Kagan, J. (1994). Galen’s prophecy. New York: Basic Books.
Kagan, J., Arcus, D., Snidman, N., Peterson, E., Steinberg,
D., & Rimm-Kaufman, S. (1995). Asymmetry of finger
temperature and early behavior. Developmental Psychobiology, 28, 443–451.
Kalin, N. H., Larson, C., Shelton, S. E., & Davidson, R. J.
(1998). Asymmetric frontal brain activity, cortisol, and
behavior associated with fearful temperament in rhesus
monkeys. Behavioral Neuroscience, 112, 286–292.
Kang, D.-H., Davidson, R. J., Coe, C. L., Wheeler, R. E.,
Tomarken, A. J., & Ershler, W. B. (1991). Frontal brain
asymmetry and immune function. Behavioral Neuroscience, 105, 860–869.
Kenney, R. (1990). Evaluation of an infrared tympanic membrane thermometer in pediatric patients. Pediatrics, 85,
854–858.
La Frenière, P. J., Dumas, J. E., Capuano, F., Coutu, D., &
Giuliani, L. (1993, April). The revised preschool socio-affect
profile. Paper presented at the biennial meeting of the Society for Research in Child Development, New Orleans.
La Frenière, P. J., Dumas, J. E., Capuano, F., & Dubeau, D.
(1992). Development and validation of the Preschool Socioaffective Profile. Psycholgical Assessment, 4, 442–450.
Leonard, B. E., & Miller, K. (1995). Stress, the immune system
and psychiatry. New York: Wiley.
Levenson, R. W., Ekman, P., & Friesen, W. V. (1990). Voluntary facial action generates emotion-specific autonomic
nervous system activity. Psychophysiology, 27, 363–384.
Liang, S. W., Jemerin, J. M., Tschann, J., Wara, D., & Boyce,
W. T. (1997). Effects of stressful life events and EEG laterality on immune functions under laboratory challenge. Psychosomatic Medicine, 59, 178–186.
Livshits, G., & Kobyliansky, E. (1991). Fluctuating asymmetry as a possible measure of developmental homeostasis
in humans: A review. Human Biology, 63, 441–466.
Mariak, Z., Lewko, J., Luczaj, J., Polocki, B., & White, M. D.
(1994). The relationship between directly measured human
cerebral and tympanic membrane temperatures during
changes in brain temperatures. European Journal of Applied Physiology and Occupational Physiology, 69, 545–549.
Meiners, M. L., & Dabbs, J. M. (1977). Ear temperature and
brain blood flow: Laterality effects. Bulletin of the Psychonomic Society, 10, 194–196.
Migliorelli, R., Starkstein, S. E., Teson, A., de Quiros, G.,
Vazquez, S., Leiguarda, R., & Robinson, R. G. (1993).
SPECT findings in patients with primary mania. Journal
of Neuropsychiatry and Clinical Neurosciences, 5, 379–383.
Milewski, A., Ferguson, K. L., & Terndrup, T. E. (1991).
Comparison of pulmonary artery, rectal, and tympanic
membrane temperatures in adult intensive care unit patients. Clinical Pediatrics, 30(Suppl.), 13–16.
Min, S. K., & Lee, B. O. (1997). Laterality in somatization.
Psychosomatic Medicine, 59, 236–240.
Mizukami, K., Kobayashi, N., Iwata, H., & Ishii, T. (1989).
Telethermography in measurement of infants’ early attachment. In C. V. Euler, H. Forssberg, & H. Lagercrantz
(Eds.), Neurobiology of early infant behavior (pp. 249–259).
Stockholm: Nobel Institute of Neurophysiology, Karolinska Institute.
Boyce et al.
Petersen-Smith, A., Barber, N., Coody, D. K., West, M. S., &
Yetman, R. J. (1994). Comparison of aural infrared with
traditional rectal temperatures in children from birth to
age three years. Journal of Pediatrics, 125, 83–85.
Pickering, G. (1961). Regulation of body temperature in
health and disease. In B. Lush (Ed.), Concepts of medicine
(pp. 177–196). New York: Pergamon Press.
Randall, W. C., McNally, H., Cowan, J., Caliguiri, L., &
Rohse, W. G. (1957). Functional analysis of the cardioaugmentor and cardioaccelerator pathway in the dog.
American Journal of Physiology, 191, 213–217.
Reis, D. J., & Golanov, E. V. (1997). Autonomic and vasomotor regulation. International Review of Neurobiology, 41,
121–149.
Rimm-Kaufman, S. E., & Kagan, J. (1996). The psychological
significance of changes in skin temperature. Motivation
and Emotion, 20, 63–78.
Robertson, E. J. (1997). Left-right asymmetry. Science, 275,
1280.
Robinson, J. L., Seal, R. F., Spady, D. W., & Joffres, M. R.
(1998). Comparison of esophageal, rectal, axillary, bladder, tympanic, and pulmonary artery temperatures in
children. Journal of Pediatrics, 133, 553–556.
Robinson, R. G., & Coyle, J. T. (1980). The differential effect
of right vs. left hemisphere cerebral infarction on catecholamines and behavior in the rat. Brain Research, 188, 63–78.
Rogers, M. C. (1978). Lateralization of sympathetic control
of the human sinus node. Anesthesiology, 48, 139–141.
Rosenberg, A., & Kagan, J. (1987). Iris pigmentation and behavioral inhibition. Developmental Psychobiology, 20, 377–
392.
Rothbart, M. K. (1981). Measurement of temperament in infancy. Child Development, 52, 569–578.
Rothbart, M. K., Ahadi, S. A., & Hershey, K. L. (1994). Temperament and social behavior in childhood. MerrillPalmer Quarterly, 40, 21–39.
Rothbart, M. K., & Derryberry, D. (1982). Theoretical issues
in temperament. In M. Lewis & L. Taft (Eds.), Developmental disabilities in preschool children: Theory, assessment,
and intervention. New York: Spectrum.
Rowell, L. B. (1986). Cerebral and coronary circulations. In
L. B. Rowell (Ed.), Human circulation regulation during
physical stress. New York: Oxford University Press.
Rubin, K. H., & Both, L. (1989). Iris pigmentation and sociability in childhood: A reexamination. Developmental Psychobiology, 22, 1–9.
Sackheim, H. A., Gur, R. C., & Saucy, M. (1978). Emotions
are expressed more intensely on the left side of the face.
Science, 202, 434–436.
Samuels, C. A., & Block, J. (1995). Eye color and behavioral
inhibition: A further study. Journal of Research in Personality, 29, 139–144.
Schaffer, E. K., Davidson, R. J., & Saron, C. (1983). Frontal
and parietal electroencephalogram asymmetry in depressed and nondepressed subjects. Biological Psychiatry,
18, 753–762.
Schiff, B. B., & MacDonald, B. (1990). Facial asymmetries in
the spontaneous response to positive and negative emotional arousal. Neuropsychologia, 28, 777–785.
733
Schmidt, L. A., & Fox, N. A. (1998). Fear-potentiated startle
responses in temperamentally different human infants.
Developmental Psychobiology, 32, 113–120.
Shenep, J. L., Adair, J. R., Hughes, W. T., Roberson, P. K.,
Flynn, P. M., Brodkey, T. O., Fullen, G. H., Kennedy,
W. T., Oakes, L. L., & Marina, N. M. (1991). Infrared,
thermistor, and glass-mercury thermometry for measurement of body temperature in children with cancer.
Clinical Pediatrics, 30(Suppl.), 36–41.
Shinozaki, T., Deane, R., & Perkins, F. M. (1988). Infrared
tympanic thermometer: Evaluation of a new clinical
thermometer. Critical Care Medicine, 16, 148–150.
Sokolov, E. N. (1963). Higher nervous functions: The orienting reflex. Annal Review of Physiology, 25, 545–580.
Stein, M. T. (1991). Historical perspective on fever and thermometry. Clinical Pediatrics, 30(Suppl.), 5–7.
Svebak, S., Storfjell, O., & Dalen, K. (1982). The effect of a
threatening context upon motivation and task-induced
physiological changes. British Journal of Psychology, 73,
505–512.
Swift, A. B. (1991). Tympanic thermometry: An index of
hemispheric activity. Perceptual and Motor Skills, 73, 275–
293.
Talo, H., Macknin, M. L., & Medendorp, S. V. (1991). Tympanic membrane temperatures compared to rectal and
oral temperatures. Clinical Pediatrics, 30(Suppl.), 30–33.
Terndrup, T. E., Crofton, D. J., Mortelliti, A. J., Kelley, R., &
Rajk, J. (1997). Estimation of contact tympanic membrane temperature with a noncontact infrared thermometer. Annals of Emergency Medicine, 30, 171–175.
Thornhill, R., & Gangestad, S. W. (1994). Human fluctuating
asymmetry and sexual behavior. Psychological Science, 5,
297–302.
Watson, D., Clark, L. A., & Tellegen, A. (1988). Development
and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and
Social Psychology, 54, 1063–1070.
Webb, G. E. (1973). Comparison of esophageal and tympanic temperature monitoring during cardiopulmonary
bypass. Anesthesia, 52, 729–733.
Weiss, M. E. (1991). Tympanic infrared thermometry for fullterm and preterm neonates. Clinical Pediatrics, 30(Suppl.),
42–45.
Weiss, M. E., Pue, A. F., & Smith, J. (1991). Laboratory and
hospital testing of new infrared tympanic thermometers.
Journal of Clinical Engineering, 16, 137–144.
Wittling, W., & Schweiger, E. (1993). Alterations of neuroendocrine brain asymmetry: A neural risk factor affecting
physical health. Neuropsychobiology, 28, 25–29.
Yanowitz, F., Preston, J., & Abildskov, J. (1966). Functional
distribution of right and left stellate innervation of the
ventricles. Circulation Research, 18, 416–428.
Zajonc, R. B., Murphy, S. T., & Inglehart, M. (1989). Feeling
and facial efference: Implications of the vascular theory
of emotion. Psychological Review, 96, 395–416.
Zamrini, E. Y., Meador, K. J., Loring, D. W., Nichols, F. T.,
Lee, G. P., Figueroa, R. E., & Thompson, W. O. (1990).
Unilateral cerebral inactivation produces differential
left/right heart rate responses. Neurology, 40, 1408–1411.