School of Public Health and the Institute of Human Development, University of California, Berkeley
School of Nursing and the Center for Health and Community, University of California, San Francisco
Department of Psychiatry, University of Wisconsin, Madison
Department of Psychiatry, School of Medicine and the Western Psychiatric Institute and Clinic, University of Pittsburgh, Pennsylvania, USA
Correspondence: Professor W. Thomas Boyce, School of Public Health, 570 University Hall, University of California, Berkeley, CA 94720-1190, USA
Declaration of interest Funded by the John D. and Catherine T. MacArthur Foundation Research Network on Psychopathology and Development and the National Institute of Mental Health (R01-MH44340).
See editorial, pp.
9394, this issue.
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ABSTRACT |
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Aims To identify measures of autonomic nervous system reactivity that discriminate children with internalising and externalising behavioural symptoms.
Method A cross-sectional study of 122 children aged 6-7 years examined sympathetic and parasympathetic reactivity to standardised field-laboratory stressors as predictors of parent- and teacher-reported mental health symptoms.
Results Measures of autonomic reactivity discriminated between children with internalising behaviour problems, externalising behaviour problems and neither. Internalisers showed high reactivity relative to low-symptom children, principally in the parasympathetic branch, while externalisers showed low reactivity, in both autonomic branches.
Conclusions School-age children with mental health symptoms showed a pattern of autonomic dimorphism in their reactivity to standardised challenges. This observation may be of use in early identification of children with presyndromal psychopathology.
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INTRODUCTION |
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Reactivity within sympathetic or para-sympathetic branches of the autonomic nervous system has been targeted as a measure of stress susceptibility because of its role in mobilising biological resources during fight or flight responses to threatening environmental events (Turner, 1989). Both adults (Cacioppo et al, 1998) and children (Allen & Matthews, 1997) show broad individual differences in autonomic reactivity, which have been associated with a variety of disorders, including internalising and externalising psychopathology (Kagan, 1994; Raine et al, 1997), psychological and physical symptoms (Gannon et al, 1989; Boyce et al, 1995a) and risk-taking behaviour (Liang et al, 1995). Given the possible linkages of autonomic reactivity to psychopathology, the purpose of this study was to examine a new reactivity assessment protocol for children aged 4-8 years and to seek measures of autonomic response that could identify children with early signs of developmental psychopathology.
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METHOD |
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To examine the discriminant validity of the reactivity protocol, children were divided into groups with low or high symptoms using maternal and teacher reports on behaviour. Two composite scores were examined: internalising problems, comprising depression, over-anxious symptoms and separation anxiety, and externalising problems/attention deficits, comprising oppositional defiant and conduct problems, overt hostility, inattention and impulsivity. A designation of low symptoms was given if both mother and teacher rated the child in the lower 80% on both scores; high internalising or high externalising if either rated the child in the upper 20%; and high both if either reporter rated in the top 20% on both.
Design and procedures
In the summer of 1998, visits were conducted in the homes of the 120 study
children, and several components of the MacArthur Assessment Battery (further
details available from the author upon request) were used to examine
constructs salient to children's mental and behavioural health. The MacArthur
Assessment Battery is an integrated assessment measure that addresses
biological, neurological, psychosocial and contextual aspects of development
in middle childhood. During a 15-minute component of the 4-hour assessment,
children's autonomic reactivity to standardised stressors was tested using a
standardised protocol completed in a van stationed outside the family's home.
Children were monitored using thoracic and precordial electrodes, a
circumthoracic band transducer of respiratory activity, a cardiac monitor and
an impedance cardiograph.
Reactivity protocol
Reactivity has been defined as "the deviation of a physiological
response parameter from a comparison or control value that results from an
individual's response to a discrete, environmental stimulus"
(Matthews, 1986). Four
physiological response parameters were employed in the study protocol: heart
rate, mean arterial pressure, respiratory sinus arrhythmia (a measure of
parasympathetic influence on heart rate variability) and pre-ejection period
(an index of sympathetic activation of the heart). Heart rate was ascertained
from interbeat interval data acquired using an electrocardiograph (ECG)
digitised at 500 Hz, edited for artefacts and analysed with the detection
algorithm of Berntson et al
(1990). Mean arterial pressure
(MAP) was measured with the monitor at the point of maximal oscillatory
amplitude (Park & Menard,
1987). Respiratory sinus arrhythmia (RSA), as described in the
work of Porges (1995) and
Cacioppo et al
(1994a), was derived
from spectral analyses of interbeat interval data within the respiratory
cycle-associated, high-frequency (0.15-0.50 Hz) band of the heart rate power
spectrum. The natural logarithm of the variance in high-frequency heart period
was calculated to estimate parasympathetic activity. The pre-ejection period
(PEP), the duration of isovolumetric ventricular contraction, was measured
with impedance cardiography as the 70-100 ms interval between the onset of
electromechanical systole (indicated by the ECG Q-wave) and left ventricular
ejection (indicated by the B point of the thoracic impedance signal). As
described by Cacioppo et al
(1994b), thoracic
impedance (Z0) and its first derivative (dZ/dt)
were measured as resistance to a constant 4 mA, 100 kHz alternating current,
using electrodes placed at the apex and base of the child's thorax. Impedance
data were ensemble averaged in 1-minute intervals, and each waveform was
verified or edited prior to analysis. Autonomic reactivity was thus assessed
as accelerations in heart rate, increases in MAP, diminution in RSA
(reflecting para-sympathetic withdrawal) or shortening of PEP (reflecting a
sympathetic effect on cardiac chronotropism).
The discrete, environmental stimuli used in the reactivity protocol were administered by an unfamiliar female researcher. They included:
The four epochs were selected to represent social, cognitive, physical and emotional challenges for children aged 4-8 years and were presented to each child in the same sequence. Before and after the set of four challenges, children were read a 3-minute calming story to procure resting physiological measures, and between the second and third challenges a 1-minute period of quiet inactivity (the recovery epoch) was imposed to examine short-term recovery in physiological parameters. The total time for completion of the protocol varied between 20 minutes and 30 minutes, including the time required for attachment, application and testing of monitoring equipment.
Reactivity scoring
Although physiological reactivity has most often been represented by change
() scores or standardised residual scores, Boyce et al
(1995b) have suggested
that a more illuminating picture of individual response patterns might be
derived from a multi-dimensional view of a child's reactivity profile. Such a
profile would encompass multiple measures capturing several dimensions of a
child's psycho-biological responses over time, rather than a singular measure
reflecting only the magnitude of such responses. Intensity was
defined as the mean of the response parameter for the four challenging task
epochs. Recovery, defined as the number recall measure minus the
recovery measure, reflected attenuation in response over 1 minute of rest.
Slope was calculated as the coefficient of a single child's
physiological measures regressed on time/epoch and it indicated the tendency
of a given physiological measure to upregulate or downregulate over the course
of the protocol. Variability was indexed as the standard
deviation of the four task values, with diminished variability reflecting
greater reactivity. In this study, these four dimension scores and a
score were calculated for each of the four physiological variables, heart
rate, MAP, RSA and PEP. The only exception was for MAP, which was not measured
during the recovery epoch and thus had no recovery score calculated. In our
previous work with middle-childhood subjects, the
and standardised
residual scores have been almost perfectly correlated.
Statistics
Data analyses were conducted in a sequence of five steps. First, frequency
distributions were examined, and intracorrelations among dimension scores were
computed to determine the degree of independence or redundancy among the
multiple measures. Second, gender effects on reactivity measures were
evaluated using t-tests for male-female differences in means. Third,
because some of the physiological variables were non-normally distributed,
non-parametric KruskalWallis one-way analyses of variance were used to
assess differences in reactivity between the four symptom groups. Because
these analyses offer insufficient insight into the magnitude of the observed
associations, Cohen's , which expresses group differences in terms of
standard deviations, was also calculated as an index of effect size. (Cohen's
is calculated as
=(Meancase
Meancontrol)/s.d.pooled. Thus, a
of 0.10
indicates that the two means differ by a tenth of a standard deviation, a
of 0.50 that the means differ by half of a standard deviation and a
of 2.0 that they differ by two standard deviations.) Where large
differences existed in subgroup sizes, effect size estimates were derived
first from MannWhitney (Wilcoxon) tests and were then converted, for
purposes of comparison, to an approximation of Cohen's
. Fourth,
results of the KruskalWallis analyses were confirmed using a signal
detection model identifying which physiological reactivity variables, and
which cut-off points within those variables' range of values, discriminated
between symptom groups with the greatest possible efficiency. This method
employs a quality receiver operator characteristic (QROC) approach to
maximising the selected variables' sensitivity and specificity in
discriminating between groups (see
Kraemer, 1992). Finally, to
render symptom group differences more visible, radar plots were created to
display comparisons among group-specific reactivity in the intensity,
recovery, slope and variability dimensions.
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RESULTS |
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Reactivity in the four symptom groups
The first analyses of discriminant validity, using KruskalWallis
tests for group differences in autonomic reactivity scores, are summarised in
Table 2. Means and standard
deviations of scores for the four symptom groups are presented along with
effect sizes where group differences were identified. Effect sizes of
approximately 0.20 are considered small, 0.50 moderate and 0.80 large
(Kraemer, 1992). Several
symptom group differences were identified that met criteria for both
statistical significance and moderate to large effect magnitudes. The RSA
intensity score, for example, robustly discriminated high internalising
children from low symptom children. Specifically, internalisers were
significantly more RSA reactive (that is, showed greater parasympathetic
withdrawal under challenge), as reflected in lower RSA intensity scores.
Further, the RSA and PEP scores discriminated high externalising
children from those with low symptoms, with externalisers showing
significantly less reactive scores (that is, higher RSA/PEP
scores
under challenge). A moderate to large and significant effect was also found
for the PEP
score in discriminating children with both internalising
and externalising symptoms from low symptom children. Trends of borderline
significance and moderate effect magnitude were also observed for RSA
variability (higher, indicating less reactivity, among externalising children)
and MAP
scores (lower, indicating less reactivity, among children with
both internalising and externalising symptoms). These results indicated that
autonomic reactivity scores discriminated children with internalising and
externalising symptoms from controls, that RSA and PEP were more effective in
making such discriminations than measures of heart rate and MAP, and that
internalising and externalising children showed contrasting patterns of
autonomic arousal under challenge.
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A second approach to assessing the discriminant validity of autonomic
reactivity scores, using a signal detection model, both confirmed and extended
results from the KruskalWallis analyses (further details available from
the author upon request). For both internalising and externalising symptoms,
an optimally efficient algorithm was developed using reactivity scores to
identify children showing significant behaviour problems. In these analyses,
children with high internalising problems were maximally and significantly
discriminated by three autonomic dimension scores, each reflecting higher
reactivity relative to asymptomatic peers: (a) RSA intensity 6.3; (b) RSA
recovery
0.50; and (c) RSA
score
0.05. Eighty-three per cent
of children meeting all three of these criteria were high internalisers, while
only 15% of those meeting none of the criteria were high internalisers.
Children with high externalising problems, on the other hand, were maximally
and significantly discriminated by two dimensions scores, both reflecting low
reactivity: (a) PEP score
1.25; and (b) RSA slope
0.50. Fifty-three
per cent of children meeting both criteria were high externalisers v.
15% of those meeting neither. Finally, the signal detection algorithm for
children with both internalising and externalising behaviour problems
contained only a single criterion, a PEP variability score of 3.20 or more,
reflecting low sympathetic reactivity. Seventy-one per cent of children
meeting this criterion were in the high both symptom group,
compared with 15% of those not meeting the criterion.
Visual representations of differences in reactivity
Figures 1 and
2 summarise and integrate the
discriminant validity analyses of autonomic reactivity scores.
Figure 1 displays
four-dimensional radar plots in which standardised scores for each reactivity
dimension (intensity, recovery, slope and variability) are plotted for
children with and without internalising and externalising symptoms. Tick marks
on each of the four axes define three points on a standardised scale for that
dimension: -1 (at the origin), 0 and +1. Further, scores have been arranged,
and in some cases reversed, so that increasing distances from the origin
universally indicate higher reactivity. As expected, data points from the
majority, asymptomatic children lie at approximately the mean (a standardised
score of 0) for each reactivity dimension. Internalising children exhibited
exaggerated reactivity in two dimensions, intensity and recovery, but only for
the parasympathetic (RSA) component of autonomic response. In contrast,
externalising children showed diminished reactivity in the two other
dimensions, variability and slope, for both the parasympathetic and
sympathetic (PEP) components. Children with internalising and externalising
disorders were thus distinguishable from each other and from children without
behavioural difficulties by three distinct aspects of their autonomic
reactivity to challenge: magnitude (that is, increased or
decreased reactivity relative to controls), dimension (that is,
effects in the intensity/recovery v. variability/slope dimensions)
and branch (that is, involvement of the para-sympathetic and/or
sympathetic branches of the autonomic nervous system).
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Mapped within two-dimensional autonomic space as conceptualised by Berntson et al (1994) (Fig. 2), the autonomic response biases of the children in this study occupy discrete psychophysiological territories. The axes in Fig. 2 represent the proportional and independent activations of the sympathetic and parasympathetic branches of the autonomic nervous system. Maximal autonomic reactivity, which involves both sympathetic activation and para-sympathetic withdrawal, would be plotted into the far right corner of the autonomic space. Children from the study with internalising symptoms showed heightened reactivity in the form of parasympathetic withdrawal, resulting in a position adjacent to the lower right border of the autonomic map. Conversely, children with externalising symptoms showed diminished reactivity, in the form of both maintenance of parasympathetic tone and relative inactivation of the sympathetic circuitry, resulting in an autonomic position approaching the far left corner. The smaller number of children with both categories of symptomatic behaviour showed unusually low sympathetic activation alone, placing them in a mapped location between the internalisers and externalisers. As supported by the KruskalWallis and signal detection analyses, each of these autonomic profiles was significantly and substantively different from the physiological response patterns of children for whom no behavioural symptoms were reported, who occupy the centre of the autonomic space.
Gender differences
A remaining question was whether identified associations between autonomic
reactivity and early psychopathology were confounded by unevenness in the
gender distribution among the four symptom groups. Two findings suggested that
this was not the case. First almost no gender differences were found in
measures of sympathetic and parasympathetic reactivity, reducing substantially
the likelihood of a confounded association with symptoms. Second, when mean
reactivity scores were computed for the eight subgroups defined by gender and
symptom, asymptomatic boys and girls were virtually identical. Even more
convincingly, gender differences in the internalising and externalising groups
were opposite in direction from those that could have confounded
reactivitysymptom associations. Internalising boys, for example, had
RSA intensity scores reflecting even greater reactivity than internalising
girls, while externalising girls had RSA and PEP scores indicating
even lower reactivity than their externalising male counterparts. These
findings support a conclusion that associations linking autonomic reactivity
to behavioural symptoms were unconfounded by gender.
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DISCUSSION |
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Commonalities with past research
Our findings are commensurate with those of several other research groups.
The seminal work of Ekman and Levenson
(Ekman et al, 1983),
for example, suggested that discrete categories of experienced emotion were
associated with specific patterns of autonomic reactivity in adult subjects.
Other studies in adults have found that a high heart rate following a
traumatic event was predictive of post-traumatic stress disorder
(Shalev et al, 1998)
and that heart rate variability was inversely associated with affective and
anxiety disorders (Rechlin et al,
1994). Parasympathetic dysregulation is predictive of chronic
behaviour problems in toddlers (Porges
et al, 1996) and teenage boys
(Mezzacappa et al,
1996), and resting heart rate in children is inversely associated
with externalising psychopathology and positively associated with anxiety
disorders (Rogeness et al,
1990; Raine,
1996). Other studies have observed increased heart rate reactivity
among pubertal boys at familial risk for alcoholism
(Harden & Pihl, 1995) and
decreased heart rate reactivity and faster habituation to a reward-conditioned
repetitive motor task in children with attention-deficit hyperactivity
disorder (Iaboni et al,
1997). Pine et al
(1998) found inverse
correlations between measures of heart rate variability and externalising
behaviour problems among the younger brothers of convicted delinquents.
Children at risk for criminality, moreover, appear protected by high autonomic
reactivity, suggesting that a predisposition toward an internalising
biological response to stressors may prevent expression of disordered conduct
(Brennan et al,
1997).
Neural substrates of autonomic reactivity
As noted by Pine et al
(1998), abnormalities in brain
monoamine systems, which have been implicated in cardiovascular functions and
psychiatric conditions, could potentially account for associations between
autonomic reactivity and psychopathology. Limbic structures such as the
amygdala can affect autonomic regulation and have been implicated in
psychiatric disorders involving emotion regulatory processes
(Kagan et al, 1988).
Porges' polyvagal theory suggests that the evolution of the
autonomic nervous system, particularly the brain-stem regulatory centres of
the vagus and related cranial nerves, produced a neuropsychological substrate
for affective processes that are the basis for both social relations and
certain psychopathological disorders
(Porges et al, 1999).
Although some evidence exists for the heritability of reactive phenotypes
(Higley et al, 1993;
Scarpa & Raine, 1997), stressful experiences, particularly early in development, also appear capable
of altering individual response characteristics
(Schneider, 1992;
Anisman et al,
1998).
As Kagan (1997) has argued, progress in understanding and classifying psychopathology is likely to depend on the use of multiple and diverse criteria, almost undoubtedly including both behaviour and biology. It appears likely that all current diagnostic categories are heterogeneous with regard to their biological and experiential aetiologies, and that significant gains could be achieved by refining taxonomic distinctions through pursuit of a combined behavioural and biological approach. The significance of the findings reported here lies, at least in part, in observations that many forms of adult psychopathology are meaningfully linked to overt behavioural differences in childhood, and that biological response predispositions may constitute one aetiological bridge between troubled child behaviour and adult disorders. Only the binocularity of a concurrently biological and contextual view of childhood risk may yield a clearer, more coherent path towards understanding and preventing developmental psychopathology.
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Clinical Implications and Limitations |
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LIMITATIONS
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ACKNOWLEDGMENTS |
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Received for publication February 28, 2000. Revision received January 29, 2001. Accepted for publication January 29, 2001.
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