77research

7/29/2019 77research

1/27

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]


2/27

I. inca, O. Benga, N.A. Fox

Cognition, Brain, Behavior 10 (2006) 489-515

490

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


3/27



491

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


4/27



492

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,


5/27



493

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,


6/27



494

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


7/27



495

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.


8/27



496

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


9/27



497

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


10/27



498

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


11/27



499

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


12/27



500

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).


13/27



501

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


14/27



502

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


15/27



503

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.


16/27



504

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


17/27



505

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.,


18/27



506

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


19/27



507

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


20/27



508

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


21/27



509

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.

REFERENCESAmerican Psychiatric Association (1994). Diagnostic and Statistical Manual of Mental

Disorders (4th edition). Washington: American Psychiatric Association.

Anthony J. L., Lonigan, C. L., Hooe, E. S., & Phillips, B. M. (2002). An affect-based,

hierarchical model of temperament and its relations with internalizingsymptomatoloy.Journal of Clinical Child & Adolescent Psychology, 31, 480-490.

Avenevoli, S., Stolar, M., Li, J., Dierker, L., & Merikangas, K. R. (2001). Comorbidity of

depression in children and adolescents: models and evidence from a prospective

high-risk family study. Biological Psychiatry, 49, 1071-1081.

Bar-Haim, Y., Marshall, P. J., Fox, N. A., Schorr, E., & Gordon-Salant, S. (2003).

Mismatch negativity in socially withdrawn children. Biological Psychiatry, 54, 17-

24.

Benga, O. (2002). Temperamentul i bazele timpurii ale personalitii. In A. Opre (Ed.),

Noi tendine n psihologia personalitii. Vol I: Modele teoretice (pp. 91-154). Cluj-

Napoca: Editura ASCR.

Biederman, J., Hirshfeld-Becker, D. D., Rosenbaum, J. F., Hrot, C., Friedman, D.,

Snidman, N., Kagan, J., & Faraone, S. V. (2001). Further evidence of association

between behavioral inhibition and social anxiety in children. American Journal of

Psychiatry, 158, 1673-1679.Biederman, J., Rosenbaum, Bolduc-Murphy, E. A., Faraone, S. V., Chaloff, J., Hirshfeld,

D. R., & Kagan, J. (1993). A 3-year follow-up of children with and without

behavioral inhibition. Journal of the American Academy of Child and Adolescent

Psychiatry, 32, 814-821.

Biederman, J., Rosenbaum, J. F., Hirshfeld, D. R, Faraone, S. V., Bolduc, E. A., Gersten,

M., Meminnger, S.R., Kagan, J., Snidman, N., & Reznick, J. S. (1990). Psychiatric

correlated of behavioral inhibition in young children of parents with and without

psychiatric disorders.Archives of General Psychiatry, 47, 21-26.

Brady, E. U., & Kendall, P. C. (1992). Comorbidity of anxiety and depression in children

and adolescents. Psychological Bulletin, 111, 244-255.

Calkins, S. D., & Fox, N. (2002). Self-regulatory processes in early personality

development: A multilevel approach to the study of childhood social withdrawal andaggression.Development and Psychopathology, 14, 477-498.

Calkins, S. D., & Fox, N. A. (1992). The relations among infant temperament, security of

attachment, and behavioral inhibition at twenty-four months. Child Development, 63,

1456-1472.

Calkins, S. D., Fox, N. A., & Marshall, T. R. (1996). Behavioral and physiological

antecedents of inhibition in infancy. Child Development, 67, 523540.


22/27



510

Caspi, A., Moffitt, T. E., Newman, D. L., & Silva, P. A. (1996). Behavioral observations at

age 3 years predict adult psychiatric disorders : Longitudinal evidence from a birth

cohort.Archives of General Psychiatry, 53, 1033-1039.

Clark, L. A. (2005). Temperament as a unifying basis for personality and psychopathology.

Journal of Abnormal Psychology, 114, 505-521.

Davidson, R. J. (1992). Emotion and affective style: Hemispheric substrates. Psychological

Science, 3, 39-43.

Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants response to

maternal separation.Journal of Abnormal Psychology, 98, 127-131.

De Bellis, M. D., Casey, B. J., Dahla, R. E., Birmahera, B., Williamson, D. E., Thomas, K.

M., Axelson, D. A., Frustaci, K., Boring, A. M., Hall, J., & Ryan, N. D. (2000). A

pilot study of amygdala volumes in pediatric generalized anxiety disorder.

Biological Psychiatry, 48, 51-57.

De Haan, M., Gunnar, M. R., Tout, K., Hart, J., & Stansbury, K. (1998). Familiar and novel

contexts yield different associations between cortisol and behavior among 2-year-old

children.Developmental Psychobiology, 33, 93-101.

Derryberry, D., & Reed, M. A. (1994). Temperament and attention: Orienting toward and

away from positive and negative signals. Journal of Personality and Social

Psychology, 66, 1128-1129.

Derryberry, D., & Rothbart, M. K. (1988). Arousal, affect, and attention as components of

temperament.Journal of Personality and Social Psychology, 55, 958-966.

Ellis, L. K., & Rothbart, M. K. (2001). Revision of the Early Adolescent Temperament

Questionnaire. Poster presented at the 2001 Biennial Meeting of the Society for

Research in Child Development, Minneapolis, Minnesota

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. (1994). Dynamic cerebral processes underlying emotion regulation. In N. A.

Fox (Ed.), The development of emotion regulation: Biological and behavioral

considerations (pp. 152-166). Monographs of the Society for Research in Child

Development, 59 (2-3, Serial No. 240).

Fox, N. A., & Henderson, H. A. (2000). Does infancy matter? Predicting social behavior

from infant temperament.Infant Behavior & Development, 22, 445-455.

Fox, N. A., Bell, M. A., & Jones, N. A. (1992). Individual differences in response to stress

and cerebral asymmetry.Developmental Neuropsychology, 8, 161-184.

Fox, N. A., Calkins, S. D., & Bell, M. A. (1994). Neural plasticity and development in the

first two years of life: Evidence from cognitive and socioemotional domains of

research.Developmental Psychopathology, 6, 677696.

Fox, N. A., Henderson, H. A., & Marshall, P. J. (2001). The biology of temperament: An

integrative approach. In C. A. Nelson & M. Luciana (Eds.), The handbook of

developmental cognitive neuroscience (pp. 631-645). Cambridge, MA: MIT Press.

Fox, N. A., Henderson, H. A., Rubin, K. H., Calkins, S. D., & Schmidt, L. A. (2001).

Continuity and discontinuity of behavioral inhibition and exuberance:

Psychophysiological and behavioral influences across the first four years of life.Child Development, 72, 1-21.


23/27



511

Fox, N., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005).

Behavioral inhibition: Linking biology and behavior within a developmental

framework.Annual Review of Psychology, 56, 235-262.

Frick, P. J. (2004). Integrating research on temperament and childhood psychopathology:

Its pitfalls and promise.Journal of Clinical Child and Adolescent Psychology, 33, 2-

7.

Garcia-Coll, C., Kagan, J., & Reznick, J. S. (1984). Behavioral inhibition in young

children. Child Development, 55, 1005-1019.

Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the Revised

Infant Behavior Questionnaire.Infant Behavior and Development, 26, 64-86.

Gest, S. D. (1997). Behavioral inhibition: Stability and associations with adaptation from

childhood to early adulthood. Journal of Personality and Social Psychology, 72,

467-475.

Goldsmith, H. H., & Lemery, K. S. (2000). Linking temperamental fearfulness and anxiety

symptoms: A behavior genetic perspective.Biological Psychiatry, 48, 1199-1209.

Goldsmith, H. H., Buss, A. H., Plomin, R., Rothbart, M. K., Thomas, A., Chess, S., Hinde,

R. A., & McCall, R. B. (1987). Roundtable: What is temperament? Four approaches.Child Development, 58, 505-529.

Gray, J. A. (1975).Elements of a two process theory of learning. London: Academic Press.

Gray, J. A. (1982). The neuropsychology of anxiety. New York: Oxford University Press.

Gunnar, M. R., Mangelsdorf, S., Larson, M., & Hertsgaard, L. (1989). Attachment,

temperament, and adrenocortical activity in infancy: A study of psychoendocrine

regulation.Developmental Psychology, 25, 355-363.

Hamann, S., & Canli, T. (2004). Individual differences in emotion processing. Current

Opinion in Neurobiology, 14, 233-238.

Hayward, C., Killen, J., Kraemer, K., & Taylor, C. (1998). Linking self-reported childhood

behavioral inhibition to adolescent social phobia. Journal of the American Academy

of Child and Adolescent Psychiatry, 37, 1308-1316.

Henderson, H. A., Fox, N. A., & Rubin, K. H. (2001). Temperamental contributions to

social behavior: The moderating roles of frontal EEG asymmetry and gender.Journal of the American Academy of Child and Adolescent Psychiatry, 40, 68-74.

Hirshfeld, D. R., Rosenbaum J. F., Biederman J., Bolduc E. A., Faraone S. V., Snidman N.,

Reznick, J. S., & Kagan, J. (1992). Stable behavioral inhibition and its association

with anxiety disorder. Journal of the American Academy of Child and Adolescent


Hirshfeld-Becker, D. R., Biederman, Calltharp, S., Rosenbaum, E. D., Faraone, S. V., &

Rosenbaum, J. F. (2003). Behavioral inhibition and disinhibition as hypothesized

precursors to psychopathology: Implications for pediatric bipolar disorder.


Hirshfeld-Becker, D. R., Biederman, J., Faraone, S. V., Segool, N., Buchwald, J., &

Rosenbaum, J. F. (2004). Lack of association between behavioral inhibition and

psychosocial adversity factors in children at risk for anxiety disorders. American

Journal of Psychiatry, 161, 547-555.Kagan, J. (1997). Temperament and the reactions to unfamiliarity. Child Development, 68,

139-143.


24/27



512

Kagan, J. (1998). Biology and the child. In W. Damon (Editor-in-chief) & N. Eisenberg

(Ed.),Hanbook of child psychology (Fifth edition). Volume three: Social, emotional

and personality development (pp. 177-235). New York: John Wiley & Sons, Inc.

Kagan, J. (2003). Biology, context, and developmental inquiry. Annual Review of

Psychology, 54, 1-23.

Kagan, J., & Snidman, N. (1991). Infant predictors of inhibited and uninhibited profiles.

Psychological Science, 2, 40-44.

Kagan, J., & Snidman, N. (1999). Early childhood predictors of adult anxiety disorders.


Kagan, J., Reznick, J. S., & Gibbons, J. (1989). Inhibited and uninhibited types of children.Child Development, 60, 838-845.

Kagan, J., Reznick, J. S., & Snidman, N. (1987). The physiology an psychology of

behavioral inhibition in children. Child Development, 58, 1459-1473.

Kagan, J., Reznick, J. S., Clarke, C., Snidman, N., & Garcia-Coll, C. (1984). Behavioral

inhibition to the unfamiliar. Child Development, 55, 2212-2226.

Kagan, J., Reznick, J. S., Snidman, N., Gibbons, J., & Johnson, M. O. (1988). Childhood

derivatives of inhibition and lack of inhibition to the unfamiliar. Child Development,

59, 1580-1589.

Keightley, M. L., Winocur, G., Graham, S. J., Mayberg, H. S., Hevenor, S. J., & Grady, C.

L. (2003) An fMRI study investigating cognitive modulation of brain regions

associated with emotional processing of visual stimuli. Neuropsychologia, 41, 585-

596.

Kendall, P. C., Brady, E. U., & Verduin, T. L. (2001). Comorbidity in childhood anxiety

disorders and treatment outcome. Journal of the American Academy of Child and

Adolescent Psychiatry, 40, 787-794.

Kessler, R. C., Keller, M. B., & Wittchen, H. U. (2001). The epidemiology of generalized

anxiety disorder. Psychiatric Clinics of North America, 24, 19-39.

Lahey, B. (2004). Commentary: Role of temperament in developmental models of

psychopathology.Journal of Clinical Child & Adolescent Psychology, 33, 88-93.

Lahey, B. B., Applegate, B., Waldman, I. D., Loft, J. D., Hankin, B. L., & Rick, J. (2004).

The structure of child and adolescent psychopathology: Generating new hypotheses.


Lemery, K. S., Essex, M. J., & Smider, N. A. (2002). Revealing the relationship between

temperament and behavior problems by eliminating measurement confounding:

Expert ratings and factor analysis. Child Development, 73 867-882.

Lengua, L. J., West, S. G., & Sandler, I. N. (1998). Temperament as predictor of

symptomatology in children: Addressing contamination of measures. Child

Development, 69, 164-181.

Lengua, L. J., Wolchik, S. A., Sandler, I. N., & West, S. G. (2000). The additive and

interactive effects of parenting and temperament in predicting adjustment problems

in children of divorce.Journal of Clinical Child Psychology, 29, 232-244.

Leve, L. D., Kim, H. K., & Pears, K. C. (2005). Childhood temperament and family

environment as predictors of internalizing and externalizing trajectories from ages 5to 17.Journal of Abnormal Child Psychology, 33, 505-520.


25/27



513

Lonigan, C. J, Vasey, M. W., Phillips, B. M., & Hazen, R. A. (2004). Temperament,

anxiety, and the processing of threat-relevant stimuli. Journal of Clinical Child &

Adolescent Psychology, 33, 8-20.

Marshall, P. J., & Stevenson-Hinde, J. (1998). Behavioral inhibition, heart period, and

respiratory sinus arrhythmia in young children. Developmental Psychobiology, 33,

283-292.

Masi G., Mucci, M, & Millepiedi S. (2001). Separation anxiety disorder in children and

adolescents: Epidemiology, diagnosis and management. CNS Drugs, 15, 93-104.

McManis, M. H., Kagan, J., Snidman, N. C., & Woodward, S. A. (2002). EEG asymmetry,

power, and temperament in children.Developmental Psychobiology, 41, 169-177.

Milham, M. P., Nugent, A. C., Drevets, W. C., Dickstein, D. P., Leibenluft, E., Ernst, M.,

Charney, D., & Pine, D. S. (2005). Selective reduction in amygdala volume in

pediatric anxiety disorders: A voxel-based morphometry investigation. Biological


Muris, P., & Meesters, C. (2002). Attachment, behavioral inhibition, and anxiety disorders

symptoms in normal adolescents. Journal of Psychopathology and Behavioral

Assessment, 24 97-106.

Muris, P., & Ollendick, T. H. (2005). The role of temperament in the etiology of child

psychopathology. Clinical Child and Family Psychology Review, 8 271-289.

Muris, P., Merckelbach, H., Schmidt, H., Gadet, B., & Bogie, N. (2001). Anxiety and

depression as correlates of self-reported behavioural inhibition in normal

adolescents.Behaviour Research and Therapy, 39, 1051-1061.

Muris, P., Merckelbach, H., Wessel, I., & van de Ven, M. (1999). Psychopathological

correlates of self-reported behavioural inhibition in normal children. Behaviour

Research and Therapy, 37, 575-584.

Nachmias, M., Gunnar, M., Mangelsdorf, S., Parritz, R. H., & Buss, K. (1996). Behavioral

inhibition and stress reactivity: The moderating role of attachment security. Child


Ollendick, T. H., & Hirshfeld-Becker, D. R. (2002). The developmental psychopathology

of social anxiety disorder.Biological Psychiatry, 51, 44-58.

Prez-Edgar, K., & Fox, N. A. (2005a). Temperament and anxiety disorders. Child and

Adolescent Psychiatric Clinics of North America, 14 681-706.

Prez-Edgar, K., & Fox, N. A. (2005b). A behavioral and electrophysiological study of

childrens selective attention to neutral and affective conditions. Journal of

Cognition and Development, 6, 89-118.

Prez-Edgar, K., Fox, N. A., Cohn, J. F., & Kovacs, M. (2006). Behavioral and

electrophysiological markers of selective attention in children of parents with a

history of depression.Biological Psychiatry, 60, 1131-1138.

Pfeifer, M., Goldsmith, H. H., Davidson, R. J., & Rickman, M. (2002). Continuity and

change in inhibited and uninhibited children. Child Development, 73, 1474-1485.

Posner, M. I., & Rothbart, M. K. (1991). Attentional mechanisms and conscious

experience. In M. Rugg & A. D. Milner (Eds.), The neuropsychology of

consciousness (pp. 91-112). London: Academic Press.Putnam, S. P., Gartstein, M. A., & Rothbart, M. K. (2006). Measurement of fine-grained

aspects of toddler temperament: The Early Childhood Behavior Questionnaire.

Infant Behavior and Development, 29 386-401.


26/27



514

Roberts, B. W., & DelVecchio, W. F. (2000). The rank-order consistency of personality

from childhood to old age: A quantitative review of longitudinal studies.

Psychological Bulletin, 126, 3-25.

Rosenbaum, J. F., Biederman, J., Bolduc, E. A., Hirshfeld, D. R., Faraone, S. V., & Kagan,

J. (1992). Comorbidity of parental anxiety disorders as risk for childhood-onset

anxiety in inhibited children. The American Journal of Psychiatry, 149, 475-481.

Rosenbaum, J. F., Biederman, J., Hirshfeld-Becker, D. R., Kagan, J., Snidman, N.,

Friedman, D., Nineberg, A., GAllery, D. J., & Faraone, S. V. (2000). A controlled

study of behavioral inhibition in children of parents with panic disorder and

depression. The American Journal of Psychiatry, 157, 2002-2010.

Rothbart, M. K. (1981). Measurement of temperament in infancy. Child Development, 52,

569-578.

Rothbart, M. K. (1989). Temperament in childhood: A framework. In G. Kohnstamm, J.

Bates, & M. K. Rothbart (Eds.), Temperament in childhood(pp. 59-73). Chichester,

UK: Wiley.

Rothbart, M. K., & Ahadi, S. A. (1994). Temperament and the development of personality.


Rothbart, M. K., & Bates, J. E. (1998). Temperament. In W. Damon (Editor-in-chief) & N.

Eisenberg (Ed.),Hanbook of child psychology (Fifth edition). Volume three: Social,

emotional and personality development (pp. 105-176). New York: John Wiley &

Sons, Inc.

Rothbart, M. K., & Derryberry, D. (1981). Development of individual differences in

temperament. In M. E. Lamb, & A. L. Brown (Eds.), Advances in developmental

psychology (pp. 37-86). Hillsdale, NJ: Erlbaum.

Rothbart, M. K., & Posner, M. I. (2001). Mechanism and variation in the development of

attentional networks. In C. A. Nelson, & M. Luciana (Eds.), Handbook of

developmental cognitive neuroscience (pp. 353-363). Cambridge, MA: The MIT

Press.

Rothbart, M. K., Ahadi, S. A., & Evans, D. E. (2000). Temperament and personality:

Origins and outcomes.Journal of Personality and Social Psychology, 78, 122-135.

Rothbart, M. K., Ahadi, S. A., Hershey, K. L., & Fisher, P. (2001). Investigations of

temperament at three to seven years: The Childrens Behavior Questionnaire. Child


Rydell, A.-M., Berlin, L., & Bohlin, G. (2003). Emotionality, emotion regulation, and

adaptation among 5- to 8-year-old children.Emotion, 3, 30-47.

Sander, D., Grandjean, D., Pourtois, G., Schwartz, S., Seghier, M. L., Scherer, K. L., &

Vuilleumier, P. (2005). Emotion and attention interactions in social cognition: Brain

regions involved in processing anger prosody.NeuroImage, 28, 848-858.

Schmidt, L. A., & Fox, N. A. (1998). Fear-potentiated startle responses in temperamentally

different human infants.Developmental Psychobiology, 32, 113-120.

Schmidt, L. A., Fox, N. A., Rubin, K. H., Sternberg, E. M., Gold, P. W., Smith, C. C.,

Schulkin, J. (1997). Behavioral and neuroendocrine responses in shy children.

Developmental Psychobiology, 30, 127-140.Schmidt, L. A., Fox, N. A., Schulkin, J., & Gold, P. W. (1999). Behavioral and

psychophysiological correlates of self-presentation in temperamentally shy children.

Developmental Psychopathology, 35, 119-135.


27/27



515

Schore, A. N. (2001). The effects of early relational trauma on right brain development,

affect regulation, and infant mental health. Infant Mental Health Journal, 22, 201-

269.

Schwartz, C. E., Wright, C. I., Shin, L. M., Kagan, J., & Rauch, S. L. (2003). Inhibited and

uninhibited infants grow up: Adult amygdalar response to novelty. Science, 300,

1952-1953.

Schwartz, C., Snidman, N., & Kagan, J. (1999). Adolescent social anxiety as an outcome of

inhibited temperament in childhood. Journal of the American Academy of Child and

Adolescent Psychiatry, 381008-1015.

Shamir-Essakow, G., Ungerer, J. A., & Rapee, R. M. (2005). Attachment, behavioral

inhibition, and anxiety in preschool children. Journal of Abnormal Child

Psychology, 33, 131-143.

Souza, I., Serra, M. A., Mattos, P., Franco, V. A. (2001). Comorbidity among children and

adolescents with attention-deficit disorder: Preliminary results. Arquivos de Neuro-

Psiquiatria, 59, 401-406.

Spence, S. (1998). A measure of anxiety symptoms among children. Behaviour Research

and Therapy, 36, 545-566.

Spence, S. H. (1997). Structure of anxiety symptoms among children: A confirmatory

factor-analytic study.Journal of Abnormal Psychology, 106, 280-297.

Spence, S. H., Rapee, R., McDonald, C., & Ingram, M. (2001). The structure of anxiety

symptoms among preschoolers.Behaviour Research and Therapy, 39, 12931316.

Thomas, A., & Chess, S. (1977). Temperament and development. New York:

Bruner/Mazel.

Thomas, K. M., Drevets, W. C., Whalen, P. J., Eccard, C. H., Dahl, R. E., Ryan, N. D.,

Casey, B. J. (2001). Amygdala response to facial expressions in children and adults.


van Brakel, A. M. L., Muris, P., Bgels, S. M., & Thomassen, C. (2006). A multifactorial

model for the etiology of anxiety in non-clinical adolescents: Main and interactive

effects of behavioral inhibition, attachment and parental rearing. Journal of Clinical

Family Studies, 15, 569-579.

Vasey, M. W., & Dadds, M. R. (2001). An introduction to the developmental

psychopathology of anxiety. In M. W. Vasey, & M. R. Dadds (Eds.), The

developmental psychopathology of anxiety (pp. 326). New York: Oxford University

Press.

Wittchen, H.-U., Kessler, R. C., Pfister, H., Hfler, M., & Lieb, R. (2000). Why do people

with anxiety disorders become depressed? A prospective-longitudinal community

study.Acta Psychiatrica Scandinavica, 102, 14-23.

World Health Organization (1992). The International Statistical Classification of Diseases

and Health Related Problems. Geneva: World Health Organization.

77research

Documents