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Cogniie, Creier, Comportament / Cognition, Brain, Behavior
Copyright 2006 Romanian Association for Cognitive Science. All rights reserved.
ISSN: 1224-8398Volume X, No. 4 (December), 489-515
TEMPERAMENTAL PREDICTORS OF ANXIETY
DISORDERS
Ioana INCA* 1, Oana BENGA1, Nathan A. FOX2
1Department of Psychology, Babe-Bolyai University, Cluj-Napoca, Romania
2Child Development Laboratory, Department of Human Development,
University of Maryland, USA
ABSTRACTTemperament is a fundamental factor in psychological adjustment throughout
development. The present paper explores the relation between temperament and
the emergence of anxiety disorders in children and young adults. The paper
focuses on two of the most prominent models in current temperament research
Kagans model ofbehavioral inhibition and Rothbarts multidimensional model
ofreactivity and self-regulation, and discusses the main differences and points
of convergence between them, with respect to assessment and
behavioral/biological manifestations. Controversial issues and difficultiesrelated to childhood anxiety disorders (diagnosis, forms of manifestation,
comorbidity) are also analyzed. The major aim of this paper is to determine the
degree of empirical support for temperament as a risk factor in the development
of anxiety disorders, and the specificity of this support. Although
straightforward conclusions are difficult to draw, due to the unbalanced
representation of the two models in the literature (most of the research was
conducted on behavioral inhibition) and the diversity of measurement methods
and samples used, we consider that existing results are encouraging; they point
to temperament as a promising area of investigation in the search for anxiety
risk factors.
KEYWORDS:temperament, behavioral inhibition, childhood anxiety,
development, risk factors
In recent years, there has been an increasing interest in the potential linkbetween temperament and the risk for psychopathology. The question of whethersome temperamental characteristics might predispose a person to develop an
internalizing or externalizing disorder is relevant not only for theoretical, but alsofor practical reasons. Since temperament manifests itself early in life, and there are
well-established temperament assessment tools, it might constitute a suitable target
*Corresponding author:
E-mail: [email protected]
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for preventive strategies. However, empirical studies, as well as conceptual
analyses are still needed to rigorously delineate the two constructs (temperamentand psychopathology) and their relations, as well as to clarify the degree of
specificity that certain temperamental characteristics might have for predictingpsychopathology, in particular anxiety. As it was shown in Prez-Edgar and Fox
(2005a), multiple sources and levels of analysis are critical for designing the fulllandscape of such a converging approach.
In this paper we focus on the connection between temperament and
anxiety. A number of studies seem to have found evidence for quite a specific linkbetween the temperament of behavioral inhibition, and anxiety disorders (e.g.,
Biederman et al., 2001; Hirshfeld-Becker et al., 2003). However, the differentmethods for identifying temperament and the diversity of instruments (especially
when it comes to assessing psychopathology) make definite conclusions regardingthe association between behavioral inhibition and anxiety rather premature. Taking
into account these constraints, our review examines the degree to whichtemperament can be considered a relevant factor for the development of childhood
and adult anxiety disorders. Although we acknowledge that potential moderators
(e.g., parental environment) can play their part in shaping this relation, our goal isto circumscribe the data extant so far, indicating points of convergence anddivergence between studies, and potential gaps in need of further research.
TEMPERAMENT ACROSS DEFINITIONS AND MODELS
Systematic interest in temperament is presumed to have its roots in ancientGreece, with Galens humoral theory as probably the first attempt to link
relatively consistent patterns of human behavior and emotion to biology. However,modern characterizations of temperament have emerged much later after the
middle of the 20th
century with the pioneering work of Stella Chess andAlexander Thomas (Thomas & Chess, 1977). Following their work, a variety of
modern temperament models have emerged, integrating behavioral, cognitive andbiological factors. Some of these models investigate discrete temperamental types
(e.g., behavioral inhibition, Kagan, 1998), while others adopt a multidimensional
approach (Fox, Henderson, & Marshall, 2001; Goldsmith et al., 1987; Rothbart &Ahadi, 1994).
The present paper will focus on two such models that reflect the
approaches dominating the field at this point (see Benga, 2002; Fox, Henderson,Marshall, Nichols, & Ghera, 2005; Kagan, 1998; Prez-Edgar & Fox, 2005a;
Rothbart & Bates, 1998, for more extensive reviews that include other models).
The first approach was initiated by Jerome Kagan and his collaborators (Kagan,2003; Kagan & Snidman, 1991, 1999), and focuses on the concept of behavioral
inhibition to the unfamiliar, assessed by observing the childs initial behavioralreactions (e.g., failure to approach, reduction of smiling and verbalizations, etc.) to
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challenging situations, especially those involving unfamiliar adults or peers
(Kagan, 1997; Kagan, Reznick, Clarke, Snidman, & Garcia-Coll, 1984).The second approach, initiated by Mary K. Rothbart (Rothbart & Bates,
1998; Rothbart & Derryberry, 1981; Rothbart, Ahadi, & Evans, 2000), definestemperament in terms of biologically-based individual differences in reactivity and
self-regulation. These differences are assumed to be influenced over time bygenetic, maturational and environmental factors. Within this model, reactivity
refers to the excitability, responsivity, or arousability of the behavioral and
physiological systems of the organism, while self-regulation refers to neural andbehavioral processes functioning to modulate this underlying neural activity
(Rothbart & Derryberry, 1981, p. 40).The two approaches are not antithetical to one another. Rather, Kagans
approach is a person-centered one (regarding behaviorally inhibited anduninhibited children as belonging to different phenotypical categories), while
Rothbart identifies processes that shape trajectories of temperament over time (andsees temperament as a cluster of continuous, rather than discrete traits).
Despite their differences, most present-day models (including the two
models discussed here) converge in their main assumptions about thecharacteristics of temperament (Frick, 2004): (1) temperament is inherited, or atleast it has a constitutional basis; (2) its corresponding behavioral manifestations
are observable early in life; and (3) it is relatively stable throughout development.The issue of stability and change in temperament is of particular relevance
when considering potential precursors of psychopathology. Temperament changes
can be conceptualized in at least two ways: as developmental changes ofbehavioral (surface) manifestations within dimensions (see for example Rothbart &
Bates, 1998) or as intraindividual shifts i.e., from one temperamental categoryor type to another (Kagan, 1998).
While the first conceptualization of change is captured by creatingmeasurement instruments targeting different behavioral manifestations at different
ages, the second one has generated research indicating a moderate to modestdevelopmental stability of temperament (Fox & Henderson, 2000; Schwartz et al.,
1999). However, both studies measuring behavioral inhibition (Fox, Henderson,
Rubin, et al., 2001) and those taking into account dimensions from Rothbartstemperament construct (Pfeifer, Goldsmith, Davidson, & Rickman, 2002) seem to
indicate a moderate tendency toward change either to develop more temperate
manifestations over time, noticed in children initially placed in extreme categories(Pfeifer et al., 2002), or even to display characteristics of the opposite category
(Fox, Henderson, Rubin, et al., 2001).
An important observation to be made here regards the fact that traitstability does not necessarily imply stability in the phenotypic expression of
behavior. As Prez-Edgar and Fox (2005a) note, over time both the triggers ofbehavioral inhibition and the individuals abilities change, which may account for
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the external observable changes. Also, it is important to note that consistency in
personality seems to increase as time passes, apparently stabilizing only in middleage (Roberts & DelVecchio, 2000), a fact that is congruent with the presence of
changes in temperament throughout childhood.In what follows, we will briefly review the two models mentioned above,
discussing their general approach to temperament, the way they definetemperament at the behavioral level, the assessment methods they use, and the
underlying cognitive and biological mechanisms they postulate.
Behavioral inhibition
The research program initiated by Kagan and his collaborators
conceptualizes behavioral inhibition as a construct with both behavioral andbiological aspects (Kagan, 1998; Kagan & Snidman, 1991, 1999; Schwartz,
Snidman, & Kagan, 1999). Behavioral inhibition is operationally defined asreluctance to approach novel situations or unfamiliar persons, this constant
tendency being stable, detectable early in life, and related to greater arousal in the
limbic-sympathetic axes.One advantage of using this approach regards the dichotomization of the
construct (see Bar-Haim et al., 2003; Biederman et al., 2001). That is, behavioral
inhibition is regarded as a discrete constellation of traits, being argued thatbehaviorally inhibited and behaviorally uninhibited children/adults represent
distinct phenotypes, and, as such, they should be treated as separate groups in
research studies. Also, relations with other variables such as anxiety areapparently much easier to detect using this approach versus the continuous one
(Kagan, 2003; Kagan & Snidman, 1999).Behavioral inhibition has been traditionally measured through laboratory
procedures involving observation of the child in different novel contexts or ininteractions with unfamiliar adults or peers. Through longitudinal research, it was
possible to establish the fact that, although postulated as stable in time, behavioralmanifestations of inhibited temperament, as well as the contexts in which they are
elicited, tend to change over the course of development. Thus, while at four months
an inhibited infant encountering novelty will most likely react with distress (mostlyirritability) and motor activity, a four-year-old or a seven-year-old child will most
likely react to unfamiliar adults or peers with a decrease in smiling and
spontaneous verbal comments, and a tendency to retreat towards the caregiver(Kagan, 1997, 2003). In order to examine the temperamental origins of behavioral
inhibition, both Kagan (Kagan & Snidman, 1999) and Fox (Calkins, Fox, &
Marshall, 1996), in two independent studies, selected at 4 months of age infantswho were highly reactive and displayed high negative affect to novel auditory and
visual stimuli. A significant percentage of these infants displayed signs ofbehavioral inhibition at one year of age in both samples. Fox, Henderson, Rubin,
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Calkins and Schmidt (2001) reported that 25% of the infants selected for these
reactivity patterns remained inhibited through age four. Behaviorally inhibitedchildren displayed characteristic behaviors when confronted with novelty, such as
motor quieting, long latencies to approach, active avoidance, decreasedvocalizations, and increased proximity to caregivers (see also Garcia-Coll, Kagan,
& Reznick, 1984).However, despite changes in the surface features of inhibited behavior, its
underlying biology the hyperexcitability of the limbic system, amygdala in
particular is assumed to remain stable. As a neural substrate for behavioralinhibition, Kagan hypothesized the presence of individual differences in amygdala
reactivity to novelty, the extensive connectivity of this neural structure withdifferent response systems pointing to its role in the modulation of physiological,
motor and emotional reactivity (Kagan & Snidman, 1991, 1999). Cardiac andneuroendocrine response systems, as well as certain aspects of cortical processing
have been assumed to reflect the increased amygdala activation, this pattern ofphysiological responses being stable over time.
Behaviorally inhibited children in the original cohort studied by Kagan
were shown to have high arousal states with heightened physiological reactivity higher resting heart rate, lower heart variability, acceleration of heart rate inresponse to mild stress / unfamiliarity, and greater postural change in diastolic
blood pressure (Kagan, Reznick, & Gibbons, 1989). Lower heart period (HP),corresponding to higher heart rate, and larger decreases in HP (heart rate
acceleration) in response to unfamiliarity negatively correlated with behavioral
inhibition in toddlerhood up to 7.5 years (Kagan et al., 1984; Kagan, Reznick,Snidman, Gibbons, & Johnson, 1988; Biederman et al., 1990). Although not
sustaining the correlation between HP and behavioral inhibition at 4.5 years,Marshall and Stevenson-Hinde (1998) found that HP at 4.5 years predicted which
of the children would remain inhibited at age 7. Calkins and Fox (1992) found norelationship between behavioral inhibition and baseline levels of HP in an
unselected sample of 2-year-olds, these results supporting the need for largersample size, or inclusion of extreme, selected samples as data pools for such
association studies (Fox et al., 2005).
Behavioral inhibition has also been related to the activation of thehypothalamic-pituitary-adrenal hormone system, reflected in the elevated secretion
of the stress hormone cortisol. Salivary cortisol levels high baseline cortisol
levels (Kagan, Reznick, & Snidman, 1987; Schmidt et al., 1997) or higher cortisolincreases in response to stressful events (Nachmias, Gunnar, Mangelsdorf, Parritz,
& Buss, 1996; Schmidt, Fox, Schulkin, & Gold, 1999) have been related to
behavioral inhibition. For example, Kagan et al. (1987) found elevated cortisollevels in 5.5-year-olds who had been classified as behaviorally inhibited at 21
months of age; inhibited behavior at 5.5 years of age was also associated with highlevels of cortisol concurrently measured. However, other studies, like De Haan,
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Gunnar, Tout, Hart, and Stansbury (1998), found more equivocal associations: an
increased cortisol response to starting preschool, associated with more assertive,angry and aggressive behavior. Studies with infants have also found negative
relations between negative emotionality and cortisol levels. Gunnar and colleagues(Gunnar, Mangelsdorf, Larson, & Hertsgaard, 1989) found that negative emotional
temperament was negatively correlated with baseline cortisol levels in 13-month-old infants, although negative emotional temperament was positively associated
with elevations in cortisol during maternal separation at 9 and 13 months.
Dissociations between HPA activity and negative emotional responses have led tothe assumption that novelty or discrepancy may be more important than the
expression of negative affect in the activation of the HPA system (Fox, Henderson& Marshall, 2001). Also, adrenocortical activity may not necessarily map onto
fear-related constructs, but may be related to the maintenance or failure of copingstrategies (Prez-Edgar & Fox, 2005a). The study of Nachmias et al. (1996)
supports this conclusion, their data showing that infants who were highly inhibitedand insecurely attached had greater cortisol responses to the Strange Situation and
the challenging coping episode, compared to children who were also highly
inhibited but who were securely attached. The cortisol increase for inhibited-insecure infants was also greater than that for the uninhibited infants, whethersecurely or insecurely attached. Mothers in secure dyads may support their
inhibited childrens strategies for coping with unfamiliar and/or stressful situation(Fox, Henderson, & Marshall, 2001; Prez-Edgar & Fox, 2005a).
Yet another parameter related to behavioral inhibition is the pattern of
hemispheric activation in the prefrontal region, as measured via theelectroencephalogram (EEG). The majority of this work has focused on
hemispheric asymmetries in EEG activation over the frontal region of the brain, itsfunctional significance being conceptualized in terms of motivational systems of
approach and withdrawal (Davidson, 1992; Fox, 1991, 1994). While the left frontalregion is thought to promote appetitive, approach-directed emotional responses, the
right frontal region is thought to promote withdrawal-directed responses toperceived aversive stimuli. There are developmental data supporting the relations
between frontal EEG asymmetry and this affective bias. Behaviorally inhibited
children showed across studies a pattern of stable right frontal EEG asymmetry higher right frontal activation, as reflected in decreased alpha power in electrodes
over the right frontal region while uninhibited children showed higher left frontal
EEG activation (Davidson & Fox, 1989; Fox, Bell, & Jones, 1992; Fox et al., 1994;Fox, Henderson, & Marshall, 2001; Henderson, Fox, & Rubin, 2001; McManis,
Kagan, Snidman, & Woodward, 2002). The combination of behavioral reactivity
and negative affect bias, as reflected in the pattern of frontal EEG asymmetry, hasbeen considered the best predictor of temperamental outcome in infants across the
first four years of life (Henderson et al., 2001). Behaviorally inhibited children alsohad higher right frontal alpha desynchronization during the anticipation of a future
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negative social event (giving an embarrassing speech; Schmidt et al., 1999) or
related to performance in an affective version of the Posner task (Prez-Edgar &Fox, 2005b).
More recently, differences between behaviorally inhibited and uninhibitedchildren have been revealed using ERP (event-related potential) techniques, of
superior temporal precision, thus giving an insight into the nature and timing ofneural events. Within an oddball auditory paradigm
1, socially withdrawn
children (8- to 12-year-olds) were found to have smaller mismatch negativity
(MMN) amplitudes and longer latencies (Bar-Haim, Marshall, Fox, Schorr, &Gordon-Salant, 2003)
2. Such individual differences in sensory processing could be
either a consequence of top-down influences by higher affective centers such as theamygdala, or might reflect bottom-up differences in early processes that may affect
later processing and evaluation of sensory information.The scarce neuroimaging evidence on brain functioning in behaviorally
inhibited individuals seems to support the major assumption of Kagans theory.Using fMRI, Schwartz and collaborators (Schwartz, Wright, Shin, Kagan, &
Rauch, 2003) showed that amygdala reactivity when viewing familiar versus novel
faces was higher in adults from Kagans original sample who had been categorizedas behaviorally inhibited in infancy. This study provides intriguing evidence ofcontinuity in the physiological reactivity systems that might underlie behavioral
inhibition (Prez-Edgar & Fox, 2005b).In summary, research investigating behavioral inhibition has attempted to
outline the characteristics of this temperamental type by combining observational
procedures with (neuro)physiological and neuroimaging methods (HP, EEG, ERP,fMRI). All of these have generated results that seem to validate the existence of
differentiating characteristics between behaviorally inhibited and behaviorallyuninhibited individuals at both the behavioral and biological levels.
The multidimensional model of temperament
Within the model put forward by Mary Rothbart, temperament is the result
of the balance between emotional reactivity and self-regulation. This latter element
(which includes attention, approach/withdrawal, behavioral inhibition, and self-soothing) is thought to modulate reactivity throughout development. The dynamic
balance between reactivity and regulation must always be approached within the
context of the developmental trajectory of the child (Prez-Edgar & Fox, 2005b),
1 The auditory oddball paradigm consists in the presentation of a train of standard(frequent) and deviant (infrequent) tones. Participants are usually only required to passively
attend to the tones.2
The MMN is an index of the function of a change-detection mechanism present in the
primary auditory cortex.
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though the assumption is that below the surface changes, at the biological level, the
temperamental traits remain stable. However, the surface individual anddevelopmental variability points to the need of taking into account contextual
appropriateness in measuring a certain temperamental trait (Rothbart & Deryberry,1981; Rothbart & Ahadi, 1994; Rothbart et al., 2000). For example, a behaviorally
inhibited and a behaviorally uninhibited child might both look quite similar ifplaced in a socially-familiar environment, but differences between them will start
to emerge once they are observed in interactions with unfamiliar adults or peers.
As a consequence, the instruments developed by Rothbart and hercollaborators (see Rothbart, 1981; Gartstein & Rothbart, 2003; Putnam, Gartstein,
& Rothbart, 2006; Rothbart, Ahadi, Hershey, & Fisher, 2001; Rothbart et al., 2000)maintain the underlying assumption of a developmental change in the surface
features of temperament, while preserving the core underlying temperamentaldimensions. At every age, there are several temperamental dimensions, which
organize into three main higher-order factors: (1) Extraversion / Surgency (whichincludes primarily sub-dimensions like positive emotionality and approach, and is
conceptually linked to Eysencks Extraversion and Grays Behavioral Activation
System see Gray, 1982); (2) Negative Affectivity (includes negative affectivity,shyness and avoidance; linked to Neuroticism and to Grays Behavioral InhibitionSystem); (3) Effortful Control (includes sub-dimensions of inhibitory control,
attentional focusing, low intensity pleasure and perceptual sensitivity). One well-known instrument assessing these dimensions of temperament is the Childrens
Behavior Questionnaire (CBQ; Rothbart et al., 2001), targeting children 3 to 7
years of age.The defining characteristic of this temperament model is the explicit
inclusion as a temperamental dimension in itself of self-regulation, manifestedespecially through effortful control, that is, the ability to inhibit a dominant
response in favor of a sub-dominant (but presumably more contextually-adaptive)one (see Rothbart & Posner, 2001 for a more detailed discussions of effortful /
attentional control). The model (Rothbart, 1989; Rothbart & Ahadi, 1994)postulates the existence of two temperament-related regulatory or control systems:
(1) Behavioral inhibition system, a passive control system, thought to develop late
in the first year (6.5-10 /13.5 months), related to Grays (1975) BehavioralInhibition System (BIS), presumably including the brain stem, orbital frontal
cortex, medial septal area, hippocampus and amygdala; and (2) Effortful control -
executive attention system, an active control system, which emerges at the end ofthe first year, but continues to develop throughout adolescence, and is related to the
dorsolateral prefrontal cortex, the anterior cingulate gyrus, supplementary motor
area and portions of the basal ganglia (Rothbart & Posner, 2001).The progressive development of the second system allows for an increased
regulation and modulation of the reactive tendencies over development. In keepingwith the idea of emotion driving self-regulation, Rothbart et al. (2000) found
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evidence that this second self-regulatory system is related to attentional control or
executive attention. By the end of the first year of life, the anterior attention systememerges (Posner & Rothbart, 1991) assuring the regulation of behavior via
executive attention. The primary form of regulation consists in distress control viaattention focusing, suggesting an inhibitory control on the amygdala by mid-frontal
regions. Even adults who report themselves as having good ability to focus andshift attention seem to experience less negative affect (Derryberry & Rothbart,
1988); and adults who performed well on a spatial-conflict task of executive
attention tended to report lower levels of anxiety and higher levels of self-reportedattentional control (Derryberry & Reed, 1994). It seems thus possible that the
mechanisms used to cope with self-regulation of emotion in early development arethen transferred to issues of control of cognition during later infancy and childhood
(Rothbart & Posner, 2001).Compared to the categorical approach of behavioral inhibition, Rothbarts
continuous model of the dynamic relationship between reactivity and self-regulation has been considered less straightforward for the delineation of
individual temperamental differences (Prez-Edgar & Fox, 2005a), even more if
we acknowledge that a childs inability to regulate negative affect can bedifferentially expressed across three realms: behavior (e.g., anxious withdrawal),cognition (e.g., low self-worth) and psychophysiology (e.g., elevated cortisol
levels) (Schmidt, & Fox, 1998), as a function of intrinsic (developmental) as wellas extrinsic (environmental) constraints. However, the fruitfulness of this approach
is reflected in the growing understanding of the fact that early reactivity, though
present from the first months of life, does not dictate outcome (Calkins & Fox,2002; Prez-Edgar, Fox, Cohn, & Kovacs, 2006). Of particular interest for the
present paper, we must notice the emphasis placed on attentional control, evenwhen acknowledged as a mediator of the relationship between temperament and
anxiety, and not a temperamental dimension per se (Fox et al., 2005; Prez-Edgar& Fox, 2005a): poor self-regulation is thus considered a critical variable in the
development and maintenance of anxiety, acting as a buffer in the face of negativereactivity. Systematic research is still needed, in order to fully understand all
interactions that underlie psychopathological outcomes of temperamental
tendencies.Both Kagans and Rothbarts models have generated large amounts of
research that have helped consolidate and develop the two constructs and their
corresponding measurement methods. This research has also managed to shedsome light into the underlying biology of temperament, and to point to relations
between temperament and emotional functioning.
The hypothesis of a connection between temperament and emotionality ingeneral has probably been one of the factors that further stimulated interest in the
link between temperament and emotional psychopathology. And sincedevelopmentally temperament represents probably the first manifestation of
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individuality, the next natural step was to investigate the function that it might play
in the emergence of psychopathology in children.We will now turn to discussing one such form of psychopathology
namely childhood anxiety by analyzing aspects related to its epidemiology, overtmanifestations and comorbidity, as well as its developmental patterns.
CHILDHOOD ANXIETY
Research often distinguishes between state anxiety, trait anxiety andanxiety disorders. While the first two cover normative, or at most subclinical levels
of acute or immediate (state anxiety), and long-term tendencies of an anxietyresponse to environmental events (trait anxiety), the third category comprises
pathological anxiety. Since research joining temperament and anxiety in childhoodhas focused predominantly on clinical anxiety, we will particularly address this
topic.Anxiety disorders are considered among the most common forms of child
psychopathology; around 8-12% of children meeting diagnostic criteria for some
form of anxiety disorder that perturbs the normal functioning of the child (seeSpence, 1998). Furthermore, it has been suggested that childhood anxiety disordersare not transient phenomena for many children, persisting throughout adolescence
and adulthood. Taxonomic criteria for childhood psychopathology based on DSM-IV (American Psychiatric Association, 1994) and ICD-10 (World Health
Organization, 1992) suggest that at least some of the adult syndromes can also be
identified at early ages, although developmental differences have to be considered.In a recent study based on a representative sample of 1,358 children and
adolescents (4 to 17 years of age), Lahey et al. (2004) suggest some differencesfrom DSM-IV regarding anxiety disorders: in particular, some anxiety symptoms
covering generalized/overanxious anxiety disorder and social anxiety seem to bepart of the same syndrome as depression, whereas separation anxiety, specific
phobia, obsessions and compulsions seem to be subsumed to a distinct dimensionof anxiety.
Longitudinal studies support such distinction, anxiety disorders, and
generalized anxiety disorder in particular, being primary conditions that frequentlyprecede depression (Avenevoli, Stolar, Li, Dierker, & Merikangas, 2001; Kessler,
Keller, & Wittchen, 2001; Wittchen, Kessler, Pfister, Hfler, & Lieb 2000), while
separation anxiety disorder seems to be linked to future panic disorder (Masi,Mucci, & Millepiedi, 2001).
Other studies, based on self- or parent reports, like the Spence Childrens
Anxiety Scale (Spence, 1997) (for children/adolescents 8 to 19 years of age)indicate six clusters of symptoms, relating to separation anxiety, social phobia,
obsessive-compulsive disorder, panic-agoraphobia, generalized anxiety and fearsof physical injury though high intercorrelations between factors could be
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explained by a higher order factor of anxiety in general. Spence, Rapee,
McDonald, and Ingram (2001), using Spence Preschool Anxiety Scale on children2.5 to 6.5 years, confirm this structure of anxiety symptoms, however with less
clear-cut delimitations of anxiety subtypes.In clinical samples, it has also been noticed a high comorbidity in anxious
children, 79% of them presenting symptoms for more than one anxiety disorders(separation anxiety disorder, overanxious / generalized anxiety disorder or avoidant
disorder/social phobia) (Kendall, Brady, & Verduin, 2001). Other studies have
indicated high comorbidity between depression - 61.9% (Brady, & Kendall, 1992),respectively between anxiety and ADHD 34.3% (Souza, Serra, Mattos, &
Franco, 2001). Comorbidity modifies prognosis in a significant way and maysuggest specific therapeutic interventions according to each case.
It seems, thus, that childhood anxiety disorders still need to be explored,moreover when we consider the preschool age. Even if the early presence of
childhood psychopathology may have a predictive value for the subsequent onset,severity and persistence of other disorders, the links with future pathology are not
yet very clear.
Another promising route regards the behavioral, environmental andbiologic markers of risk and in particular the exploration of early temperamentaltraits as a predisposing factor for later psychopathology. It is this route that we
now turn to, by discussing the degree to which extant evidence supportstemperament as a risk factor for anxiety disorders.
TEMPERAMENT AND THE RISK FOR ANXIETY DISORDERS
As already mentioned, research has started investigating temperament as apossible ingredient in the emergence of psychopathology in children (see
reviews by Clark, 2005; Goldsmith & Lemery, 2000; Hirshfeld-Becker et al., 2003;Prez-Edgar & Fox, 2005a). However, establishing the exact nature of the relation
between these two constructs as well as its plausible underlying mechanisms iscomplicated for at least three reasons. First, there are multiple additional risk or
protective factors (like, for example, parenting characteristics) coming into play on
the pathway leading from a certain temperamental profile to the presence orabsence of psychopathological symptoms and this is more acute if we consider
the behavioral inhibition framework. Second, as Frick (2004) and Lahey (2004)
have pointed out, some of the instruments used to measure temperament containitems that overlap with clinical criteria used to diagnose psychopathology. In this
case, any relations between temperament and symptomatology obtained through
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such measures will be artificially inflated3. Third, theoretical complications are
added by the fact that different authors see the relation between temperament andanxiety in different ways: some conceptualize temperament as reflecting individual
variability within the normal/typical range, with psychopathology being adistinctive entity that, under certain circumstances, can develop on the foundation
of temperamental risk factors; other authors see psychopathology simply as anextreme manifestation of a certain temperamental pattern (Lahey, 2004).
The rationale for bridging the two constructs is mainly the presence of
common characteristics shared by anxiety and temperament in particularbehavioral inhibition (Anthony, Lonigan, Hooe, & Phillips, 2002; Lonigan, Vasey,
Phillips, & Hazen, 2004; Prez-Edgar & Fox, 2005a; Vasey & Dadds, 2001), like:overly sensitive danger detection systems, attentional bias to threat, avoidant
coping style, psychophysiologic patterns (EEG asymmetry, startle response, heartrate and heart rate variability, pupil dilatation, salivary cortisol), and an over-
reactive amygdala.For example, in terms of common neurobiological grounds, abnormally
large right amygdala volumes have been reported not only in adults, but also in
children and adolescents with generalized anxiety disorders (see Schore, 2001); DeBellis et al. (2000) found in a MRI study significantly larger right and totalamygdala volumes in children with generalized anxiety disorders (age 8-16)
compared to normal children. Functional neuroimaging studies (Thomas et al.,2001) also revealed an exaggerated amygdala response to fearful faces in children
with anxiety disorders (8-16 years of age) compared to healthy children, the
magnitude of amygdala signal correlating with the severity of everyday anxietysymptoms.
On the other hand, coming back to Rothbarts model, volumetric data(Milham et al., 2005) showed reduced left amygdala in pediatric anxiety,
suggesting that not the absolute volumetric variations, but perturbations of theneural networks involved in anxiety from the healthy state might be critical in
understanding the neurobiology of anxiety disorders. In this sense, many studieshighlight that not (only) amygdala hyperactivation, but a deficitary attentional top-
down control is associated with anxious symptomatology (Hamann & Canli, 2004;
Keightley et al., 2003; Sander et al., 2005) in adults, and probably in children aswell.
All these data, although still insufficient, plead for functional differences
between children with anxiety and their healthy counterparts, and sustain thatamygdala hyperactivation coupled with a deficitary control over it by frontal
3 However, some of these instruments do seem to retain their predictive value even after
elimination of the overlapping items (see Lemery, Essex, & Smider, 2002; Lengua, West,
& Sandler, 1998).
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structures, would be characteristic for anxiety disorders as well as for certain
temperamental precursors.
Temperamental predictors of anxiety disorders
In what follows, we attempt to draw a few tentative conclusions related tothe temperamentanxiety link and its specificity. The studies reviewed for this
purpose include at least one measure of temperament and one diagnosis measure
for internalizing disorders (measured either concurrently with the assessment oftemperament, or longitudinally). The samples involve children, adolescents and
young adults. These studies are summarized in table 1. We preferred to leave outdiscussion of studies targeting the temperament-externalizing disorders link.
Although especially in young children the distinction between internalizing andexternalizing disorders cannot be drawn in a very clear-cut manner, most studies
seem to indicate quite separate temperamental predictors for these two broadpsychopathological categories (e.g., Biederman et al., 2001).
Table 1. Summaries of studies linking temperament to psychopathology in children or
adolescents.
S
tudy
T
ype
T
emperament
C
onstruct
V
ariables
(
measurement)
S
ample
c
haracteristics
M
ainfindings
Hirshfeld etal. (1992)
Longitudinal(21 months
7.5 years)
BI BI (labobservation)
BI stability
Childpsychopathology(DSM-based
interview)
Kagan cohort(children
followed since
4 months and
rated for BIfirst at 14
months and
21months)
The BI children hadsignificantly higher rates
for anxiety disorders
including multiple anxiety
disorders and phobicdisorders (mostly social).
Schwartz et
al (1999)
Longitudinal BI BI (lab
observation)
Childpsychopathology
(DSM-based
interview)
Kagan cohort.
Curent age: 13
years.
Significantly higher rates of
social anxiety in BI than
BUI adolescents.Gender: more pronounced
difference for girls.
No significant differencesfor other anxiety disorders.
Biedermanet al. (1990) Concurrent/Longitudinal BI BI (labobservation).
Childpsychopathology(DSM-based
interview)
Clinical(referred)
sample: 4-7
years.Longitudinal
sample: 7-8
Higher rates of multipleanxiety disorders in both
samples compared to
controls.High-risk sample: higher
rates of overanxious
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Parental diagnosis(PD, AG, MD,
control).
years fromKagans cohort
(selected at 21
months forextreme BI).
Controls.
disorder.Longitudinal sample:
higher rates of phobias
(mainly social).
Biederman
et al (1993)
Longitudinal
/ Prospective
BI BI (lab
observation).
BI stability(assessed over athree-year interval)
Child
psychopathology(K-SADS-E)
parent report.
The clinical
sample from
Biederman et al
(1990), at three-year follow-up.
Current age: 4-
11 years.
BI children had higher rates
of anxiety disorders and
higher rates of newly-onset
anxiety than BUI children.Stable BI children had
higher rates of all anxiety
disorders assessed (mostlymultiple and avoidant
anxiety disorder).
Biederman
et al. (2001)
Concurrent BI BI (lab
observation).
Child
psychopathology(K-SADS-E).
Parental diagnosis(PD, PD+MD, MD,control SCID:
DSM-based
interview).
Clinical
(referred)
sample.Age: 2-6 years
Significantly higher rates of
social anxiety disorder in
BI than in BUI children.Independent effects of BI
and parental diagnosis. No
interaction effects.
Caspi et al
(1996)
Longitudinal
/ Prospective
(3-21 years)
BI BI (assessment of
behavior during a
testing session; at 3years)
Psychopathology(assessed at 21years; DSM-based
interview).
Non-clinical
sample.
Age: 3-21 years
Higher rate of depression at
21 years in children rated as
BI at 3.No differences for anxiety
(only currentdisorders
were assessed).
Shamir-Essakov et
al. (2005)
Concurrent BI BI (lab observation +parent questionnaire
STSC a modified
version of Thomas &Chess scale)
Attachment security(SSP preschool
version)
Child anxietydisorders (ADIS-CP-
IV; DSM-IV-based
interview, parent).
Maternal traitanxiety (STAI-Y).
Non-clinicalsample.
Age: 3-5 years.
BI and attachment statuswere both independently
related to child anxiety (N
too low to distinguishamong different anxiety
disorders). No interactioneffects.
Hayward et
al (1998)
Longitudinal /
Retrospective
BI BI (Reznick
Retrospective Self-
Report of
High-school
students
9-12th grade.
Higher social avoidance
and fearfulness in the 9th
grade was significantly
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Inhibition)Child
psychopathology
(social phobia &depression); yearly
assessment (9th-12
th
grade), self-rated.
associated to the risk fordeveloping newly-onset
social phobia.
van Brakel
et al (2006)
Concurrent BI (three
levels of
BI: high,medium,
low)
BI (BIS; a 4-item self-
report questionnaire).
Attachment(questionnaire AQ-
C).
Parenting style(measured using a
Swedishquestionnaire).
Child anxiety(SCARED).
Non-clinical
sample.
Age: 11-15years
The three factors were
significant independent
predictors of child anxiety.Significant but small
interaction between BI and
Attachement.
Muris et al.
(2001)
Concurrent BI
(threelevels
of BI:
high,
medium, low)
BI (BIS; a 4-item
self-reportquestionnaire + a 1-
item global
assessment).
Anxiety (SCAS).Depression (CDI).
Non-clinical
sample.Age: 12-18
years.
Significant links between
BI and both anxiety anddepression.
No evidence of a direct link
between BI and depression.
Instead, anxiety seems tomediate the link between
BI and depression.
Muris &Meesters
(2002)
Concurrent BI(three
levelsof BI:
high,
medium, low)
BI (BII - a 1-itemglobal assessment).
Attachment(questionnaire
AQ-C).Anxiety and Major
depression(RCADS
adaptation ofSCAS).
Child- and parent-
report
Non-clinicalsample.
Age: 11-15years
Discrepancy betweenparent and child reports, but
similar patterns of results.Significantly more
insecurely attached children
were BI.There was a s ignificant
effect of BI on social
anxiety and separationanxiety disorder. BI and
attachment were significant
independent predictors of
anxiety disorders. Nointeraction effects.
Muris et al
(1999)
Concurrent BI
(threelevels
of BI:high,
mediu
m, low)
BI (BIS; a 4-item
self-reportquestionnaire + a 1-
item globalassessment).
Anxiety
(SCARED)Worry (PSWQ-C)
Depression (DQC).
Non-clinical
sample.Age: 12-15
years
Significant linear
association of BI topsychopathological
symptoms in general.No specific relation to
social phobia. Significant
relation to certain anxietydisorders.
Nachmiaset al. (1996)
Concurrent BI BI (lab observation+ TBAQ).Attachment (SSP)
Stress reactivity(cortisol level).
Non-clinicalsample
Age: 18 months
Attachment status had amoderating role in
predicting stress reactivityfrom BI.
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Lengua et al(1998)
Concurrent Emotional
reactivi
ty andregulati
on
Negativeemotionality (Buss
& Plomin, 1984).
Positiveemotionality
(DOTS-R)
Self-regulation(CBQ; Goldsmith
& Rothbart, 1991)Depression (CDI child; CBCL
parent)
Non-clinicalsample
Age: 9-12
years.
Negative emotionality wassignificantly related to
depression.
Lengua et al(2000)
Concurrent Emotional
reactivity and
regulation
All the variablesfrom Lengua et al
(1998).Parenting (Child
Report of ParentingBehaviorInventory)
Non-clinicalsample
Age: 9-12years.
Positive emotionality wasfound to be a moderator
(protective factor) betweenparental rejection and
depression.
Leve et al
(2005)
Longitudinal
(5-17 years;5 assessment
episodes)
Emotio
nalreactivi
ty and
regulation
Temperament(CBQ)Parental
environment(discipline,maternal depressive
symptoms, marital
adjustment, familyincome)
Internalizing &
externalizingdisorders (CBCL)
Non-clinical
sample
Girls internalizing
behavior increased overtime. Externalizing
behavior decreased for
both genders.Maternal depression and
child fear/shyness
predicted internalizingbehavior across the 12-
year span.
Abbreviations for Temperament / Psychopathology categories: BI=behavioral inhibition /behaviorally inhibited; BUI=behaviorally uninhibited; PD=panic disorder; AG=agoraphobia;
MD=major depression.
Abbreviations for measurement scales:Temperament: STSC = Short Temperament Scale for Childrenl; DOTS-R = Dimensions ofTemperament Survey Revised;
Psychopathology: CBCL = Child Behavior Checklist; SCARED = The Screen for Child Anxiety
Related Emotional Disorders; SCAS = Spence Childhood Anxiety Scale; RCADS = RevisedChildrens Anxiety and Depression Scale; K-SADS-E = Schedule for Affective Disorders and
Schizophrenia for School-Age Children Epidemiologic Version; PSWQ-C = Penn State WorryQuestionnaire for Children; CDI = Child Depression Inventory; DQC = Depression Questionnaire for
Children; STAI = State-Trait Anxiety Inventory (for parents).
Attachment: SSP = Strange Situation Procedure; AQ-C = Attachment Questionnaire for Children.
Our analysis is guided by the intention to determine de degree of predictivespecificity of the temperamental characteristics included in studies related to
internalizing disorders. We are mainly interested in establishing whether these
characteristics are predictive for a certain type of anxiety disorder, for anxiety
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disorders in general, or whether they are even more nonspecific indicators of a
risk for internalizing disorders in general.As indicated in table 1, most studies of interest to the present topic have
focused on the concept of behavioral inhibition (as initially defined by Kagan),assessed either through traditional laboratory observational procedures (e.g.,
Biederman et al., 2001) or through questionnaires administered to the parent and/orchild (e.g., Muris, Merckelbach, Wessel, & van de Ven, 1999). The link between
behavioral inhibition and anxiety is probably readily obvious due to the many
characteristics that the two constructs seem to share (Prez-Edgar & Fox, 2005a).Fewer studies have been conducted using Rothbarts model and the respective
assessment instruments.A consistent proportion of research using the construct of behavioral
inhibition seems to have identified a specific link to social anxiety (social phobia,avoidant disorder) (see also Ollendick & Hirshfeld-Becker, 2002 for a recent
review on the topic). Kagan and Snidman (1999) described the longitudinal studywhich followed a cohort of children starting when they were 4 months old. These
children were assessed for behavioral inhibition at 14 and 21 months, and
subsequently re-evaluated when they were 4.5 and 7.5 years old. During this lastassessment, parent and teacher ratings of child anxiety symptoms were obtained.Results indicated that although behavioral inhibition stability was modest,
behavioral inhibition classification in infancy was significantly related to the laterdevelopment of anxious symptoms. In a further study, Schwartz et al., (1999)
interviewed adolescents from this longitudinal sample. They found that a
significant number of the adolescents categorized in infancy as being highlyreactive were having symptoms of social anxiety, in the absence of significant
manifestations of any other anxiety disorder. In another study, Biederman et al.,(2001) included externalizing symptoms in their assessment of psychopathology to
further test the predictive specificity of behavioral inhibition. Here, the onlysignificant relation found was that of behavioral inhibition with social anxiety
disorder. There was also a relation with parental diagnosis of panic disorder, butthe two factors were independent of each other, which indicated that behavioral
inhibition was, on its own, a significant predictor of social anxiety.
Most studies linking behavioral inhibition to social anxiety have includedparticipants from Kagan et als (1984) original sample (Biederman et al., 1990,
2001;Hirshfeld et al., 1992; Schwartz et al., 1999). Others have identified similar
relations on different samples, using questionnaires instead of the classicalobservational procedure (Hayward, Killen, Kraemer, & Taylor, 1998; Muris &
Meesters, 2002). Thus, there seems to be at least some support (using two types of
assessment methods) for predicting a higher probability of present or future socialanxiety in behaviorally inhibited children.
However, despite this supporting data, there is also evidence pointing to amore general relation. For example, Biederman and colleagues (Biederman et al.,
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1993) identified a higher risk for anxiety disorders in general in the case of stable
behaviorally inhibited children from a group of 4-11 year-olds rated three yearsbefore. Similar results were found by Shamir-Essakov, Ungerer, and Rapee (2005)
in 3 to 5-year-old children (although here more detailed conclusions were impededby the very low number of children in each specific anxiety disorder category).
A group of studies using the behavioral inhibition construct but relyingexclusively on questionnaire measures seem to indicate a similarly general role for
behavioral inhibition in predicting concurrent anxiety symptoms. Muris et al.,
(1999) investigated the relation between behavioral inhibition (child self-rated) andpsychopathology (anxiety, worry, depression) in 12- to 14-year-old children. Their
results indicated higher levels of psychopathology in children who ratedthemselves as high in behavioral inhibition. The strongest link was between
anxiety symptoms (in general, not just social anxiety) and behavioral inhibition.Also, girls exhibited higher levels of these disorders than did boys. A subsequent
study (Muris, Merckelbach, Schmidt, Gadet, & Bogie, 2001) identified relationsbetween behavioral inhibition and anxiety and behavioral inhibition and
depression, respectively, in a large sample of adolescents (12-18 years). However,
the relation between behavioral inhibition and depression was mediated by anxiety.A similar relation between behavioral inhibition and anxiety symptoms in generalwas found by van Brakel, Muris, Bgels, and Thomassen (2006) in children aged
between 11 and 15 years. However, the behavioral inhibition measures used inthese three studies might be criticized on the account that they were quite simple
and general (the authors combined a four-item scale inspired by Gest (1997) and a
one-item global instrument for the assessment of behavioral inhibition).To summarize, despite the variability in assessment methods, behavioral
inhibition seems to be a quite consistent predictor of anxiety, with some studiessupporting a very specific link to social anxiety, while others indicating a more
general relation between behavioral inhibition and anxiety, or even behavioralinhibition and other internalizing disorders (e.g., depression). Although probably
caution is necessary when interpreting the results of some studies (e.g., thoseassessing behavioral inhibition with short questionnaires Muris et al., 1999), we
can conclude that the data does generally support the existence of a fairly specific
link between behavioral inhibition and anxiety.Less clear conclusions can be formulated with respect to Rothbarts model,
because there are almost no studies investigating relations between the various
temperament dimensions and anxiety. The only relevant study we could identify(Rydell, Berlin, & Bohlin, 2003) measured emotionality using scales essentially
similar to Rothbarts Negative Emotionality and Surgency/Extraversion from the
CBQ. The results showed that the lower-order emotional traits discriminatedbetween externalizing and internalizing disorders. More specifically, even though
negative affect predicted psychopathology in general, anger seemed to be asignificant predictor for externalizing disorders, while fearsignificantly predicted
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internalizing disorders. Similar results were found by Leve, Kim, and Pears (2005)
using the CBQ. As can be noted in table 1, this study focused on internalizing (andexternalizing) disorders in general, but the results converge with a limited number
of studies showing links to internalizing disorders other than anxiety (namely,depression). Thus, Caspi and colleagues (Caspi, Moffitt, Newman, & Silva, 1996)
found a relation between behavioral inhibition assessed at 3 years and symptoms ofdepression at 21 years, but no significant link to anxiety. Lengua and collaborators,
using a composite measure of temperament derived from different scales showed a
link between negative affectivity and depression (Lengua et al., 1998). However,subsequent analyses including parenting style as a factor (Lengua, Wolchik,
Sandler, & West, 2000) indicated that positive (not negative) emotionality played amoderating role between parental rejection and depression.
One possible reason for the paucity of research linking temperament andpsychopathology with Rothbarts model is the inherent contradiction between a
process based model (Rothbart) and a typological or categorical position(psychiatric diagnosis). A medical/psychiatric approach views illness or disorder as
reflected in number and constellation of symptoms. Thus, a child who fears
novelty, withdraws from social situations, has fast heart rate, and who displaysthese symptoms over a period of time might be considered to meet criteria for aDSM anxiety disorder. The fact that these symptoms or behaviors may change as
a function of development, or that specific moderators of these behaviors such asparenting or executive functions may change the trajectory of development is often
not of critical importance in this view. The medical/psychiatric model is more of a
static approach to temperament while the Rothbart approach provides entry into adynamic picture of the developing child.
Most of the existing data seems to support a link between behavioralinhibition and anxiety, and this link seems to be specific at least as far as the larger
group of anxiety disorders are concerned. Probably more studies would be neededto clarify the relation of behavioral inhibition to depression, but taking into account
the results of Muris et al. (2001), and the fact that Caspi et al. (1996) only includedan assessment of current (not lifetime) psychopathology, one could reasonably
state that the presence of only depression at 21 years does not exclude the previous
occurrence of anxiety.In the case of Rothbarts model, the paucity of studies and the
multidimensional nature of the construct itself make clear predictions more
difficult. However, Muris and Ollendick (2005) recently reviewed evidence fortheir assertion that the probability of child psychopathology (both internalizing and
externalizing disorders) might be higher in children whose temperament is
characterized by the combination of high neuroticism (understood here asemotional reactivity) and low effortful control. They discussed several longitudinal
studies indicating a bias for the relation between emotional reactivity (neuroticism)and internalizing disorders. However, when discussing possible reasons for this
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bias, they pointed to the fact that these studies measured temperament with
questionnaires covering lower-order traits (for example, Rydell et al., 2003 usedEllis & Rothbarts 2001 Early Adolescent Temperament Questionnaire). Such
studies were able to show that reactive emotionality was predictive of bothinternalizing and externalizing symptoms, and what differentiated between them
was the lower-order trait indicating the dominant emotion (e.g., fear versus anger).Thus, while at least some conclusions and hypotheses can be formulated
for the behavioral inhibition - anxiety link, future research using Rothbarts model
would probably have to take on a more exploratory approach.Regarding the specificity issue, the most probable conclusion would be
that behavioral inhibition and certain dimensions related to reactivity and self-regulation might constitute relevant predictors for anxiety (and they might be less
relevant for other internalizing disorders like depression). However, while it islikely that these predictors might not extend to internalizing disorders in general,
their predictive value might in fact be narrower that is, related to specific anxietydiagnoses. Most of the above studies that pointed toward less specificity have
either used very general questionnaire measurements of behavioral inhibition, or
very general assessments of psychopathology (or both), or had samples withsymptoms that did not reach clinical intensity of symptoms (e.g., Lengua et al.,1998; Muris et al., 1999). On the other hand, the studies that linked behavioral
inhibition to social anxiety had selected, referred samples, and used more complexmeasurement instruments both for behavioral inhibition and anxiety (Biederman et
al., 2001; Schwartz et al., 1999). Of course, this does not necessarily favor the
narrow specificity interpretation, but it points to the necessity for caution wheninterpreting the data.
Another important point of caution relates to the fact that beyond thetemperament -anxiety relation there are several factors that come into play during
development and that can act as moderators or as additional risk/protective factors.These factors include mostly aspects related to parental environment, like
attachment security (Nachmias et al., 1996; Muris & Meesters, 2002), parentalpsychopathology (Rosenbaum et al., 1992, 2000), parenting style (van Brakel et
al., 2006) or general family environment (Hirshfeld-Becker et al., 2004). The
relations between these factors are extremely complex and most of them seem tobe related both to temperamental and psychopathological outcomes.
The present paper did not explicitly take into account these factors, instead
focusing exclusively on anxiety and the predictive value of temperament.However, as an aside it can be mentioned that in most studies reviewed here (with
the exception of Nachmias et al., 1996), along with their individual effects,
parenting factors and temperament were found to have additive (not interactive)effects on anxiety, which indicates that in most cases temperament on its own
significantly predicts current or future anxiety. This information, as well as theresearch already discussed (and the one still lacking) indicates that the relation
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between temperament and anxiety is indeed a topic worthy of further investigation,
and one which has high chances of generating effective prevention strategies in thefuture.
ACKNOWLEDGEMENTS
This paper was supported by CEEX-M1 Grant no. 124 (AnxNeuroCog) and CEEX Grant
no. 131-ET from the Romanian Ministry of Education and Research.
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