CogniŃie, Creier, Comportament / Cognition, Brain, Behavior Copyright © 2006 Romanian Association for Cognitive Science.
All rights reserved. ISSN: 1224-8398 Volume X, No. 4 (December), 489-515
TEMPERAMENTAL PREDICTORS OF ANXIETY DISORDERS
Ioana łINCAŞ* 1 , Oana BENGA 1 , Nathan A. FOX 2
Department of Psychology, Babeş-Bolyai University, Cluj-Napoca, Romania
Child Development Laboratory, Department of Human Development, University of Maryland, USA
Temperament 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 – Kagan’s model of behavioral inhibition and Rothbart’s multidimensional model of reactivity 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 difficulties related 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 link between temperament and the risk for psychopathology. The question of whether some temperamental characteristics might predispose a person to develop an internalizing or externalizing disorder is relevant not only for theoretical, but also for practical reasons. Since temperament manifests itself early in life, and there are well-established temperament assessment tools, it might constitute a suitable target
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I. łincaş, O. Benga, N.A. Fox Cognition, Brain, Behavior 10 (2006) 489-515
for preventive strategies. However, empirical studies, as well as conceptual analyses are still needed to rigorously delineate the two constructs (temperament and psychopathology) and their relations, as well as to clarify the degree of specificity that certain temperamental characteristics might have for predicting psychopathology, in particular anxiety. As it was shown in Pérez-Edgar and Fox (2005a), multiple sources and levels of analysis are critical for designing the full landscape 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 link between the temperament of behavioral inhibition, and anxiety disorders (e.g., Biederman et al., 2001; Hirshfeld-Becker et al., 2003). However, the different methods for identifying temperament and the diversity of instruments (especially when it comes to assessing psychopathology) make definite conclusions regarding the association between behavioral inhibition and anxiety rather premature. Taking into account these constraints, our review examines the degree to which temperament 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 is to circumscribe the data extant so far, indicating points of convergence and divergence 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 ancient Greece, with Galen’s “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 and Alexander Thomas (Thomas & Chess, 1977). Following their work, a variety of modern temperament models have emerged, integrating behavioral, cognitive and biological 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; Pérez-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 child’s initial behavioral reactions (e.g., failure to approach, reduction of smiling and verbalizations, etc.) to
while Rothbart identifies processes that shape trajectories of temperament over time (and sees temperament as a cluster of continuous. reactivity refers to “the excitability. The second approach. These differences are assumed to be influenced over time by genetic. Kagan’s approach is a person-centered one (regarding behaviorally inhibited and uninhibited children as belonging to different phenotypical categories). 2002). most present-day models (including the two models discussed here) converge in their main assumptions about the characteristics of temperament (Frick. Clarke. Benga. 1998). noticed in children initially placed in extreme categories (Pfeifer et al. 1998) or as intraindividual “shifts” – i. while self-regulation refers to “neural and behavioral processes functioning to modulate this underlying neural activity” (Rothbart & Derryberry. Reznick. The issue of stability and change in temperament is of particular relevance when considering potential precursors of psychopathology. Rather. Rothbart & Derryberry. especially those involving unfamiliar adults or peers (Kagan. Fox Cognition. 1998. p. 1984). or even to display characteristics of the opposite category (Fox. & Rickman. 2000. over time both the triggers of behavioral inhibition and the individual’s abilities change. 1981. 2001). Rubin. Brain. maturational and environmental factors. defines temperament in terms of biologically-based individual differences in reactivity and self-regulation. initiated by Mary K. which may account for
. & Evans.e.. Rothbart. both studies measuring behavioral inhibition (Fox. Henderson. 2001) and those taking into account dimensions from Rothbart’s temperament construct (Pfeifer. Within this model. Henderson. et al. The two approaches are not antithetical to one another. Behavior 10 (2006) 489-515
challenging situations. 40). O. As Pérez-Edgar and Fox (2005a) note. Rubin.. Despite their differences. Snidman. N. or arousability of the behavioral and physiological systems of the organism”. the second one has generated research indicating a moderate to modest developmental stability of temperament (Fox & Henderson.I. 1999). 2000). (2) its corresponding behavioral manifestations are observable early in life. Goldsmith.. Temperament changes can be conceptualized in at least two ways: as developmental changes of behavioral (surface) manifestations within dimensions (see for example Rothbart & Bates. Ahadi.. Schwartz et al. 1997. & Garcia-Coll. łincaş. 2002) seem to indicate a moderate tendency toward change – either to develop more temperate manifestations over time. 2004): (1) temperament is inherited. Rothbart (Rothbart & Bates. and (3) it is relatively stable throughout development.A. Davidson. 1981. An important observation to be made here regards the fact that trait stability does not necessarily imply stability in the phenotypic expression of behavior. from one temperamental category or type to another (Kagan. However. rather than discrete traits). et al. Kagan. responsivity. While the first conceptualization of change is captured by creating measurement instruments targeting different behavioral manifestations at different ages.. or at least it has a constitutional basis.
and the underlying cognitive and biological mechanisms they postulate. Kagan & Snidman. Behavioral inhibition has been traditionally measured through laboratory procedures involving observation of the child in different novel contexts or in interactions with unfamiliar adults or peers. Fox.. Benga. and a tendency to retreat towards the caregiver (Kagan. discussing their general approach to temperament. 2001). 1999. Brain. as well as the contexts in which they are elicited. Thus. In what follows. although postulated as stable in time. 1999). Behavioral inhibition The research program initiated by Kagan and his collaborators conceptualizes behavioral inhibition as a construct with both behavioral and biological aspects (Kagan. In order to examine the temperamental origins of behavioral inhibition. Also. being argued that behaviorally inhibited and behaviorally uninhibited children/adults represent distinct phenotypes. łincaş. behavioral inhibition is regarded as a discrete constellation of traits. tend to change over the course of development. N. a fact that is congruent with the presence of changes in temperament throughout childhood. 1991. One advantage of using this approach regards the dichotomization of the construct (see Bar-Haim et al. we will briefly review the two models mentioned above..
. Schwartz. relations with other variables – such as anxiety – are apparently much easier to detect using this approach versus the continuous one (Kagan. O. detectable early in life. Behavior 10 (2006) 489-515
the external observable changes. That is.A. selected at 4 months of age infants who were highly reactive and displayed high negative affect to novel auditory and visual stimuli. Behavioral inhibition is operationally defined as reluctance to approach novel situations or unfamiliar persons. as such. behavioral manifestations of inhibited temperament. it is important to note that consistency in personality seems to increase as time passes. 2000). and related to greater arousal in the limbic-sympathetic axes. Rubin. A significant percentage of these infants displayed signs of behavioral inhibition at one year of age in both samples. Through longitudinal research. 1997. 2003. Fox. the way they define temperament at the behavioral level.492
I. Fox Cognition. 1996). 1999). Henderson. Biederman et al. it was possible to establish the fact that. 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. Snidman. they should be treated as separate groups in research studies. Kagan & Snidman. while at four months an inhibited infant encountering novelty will most likely react with distress (mostly irritability) and motor activity. & Kagan. 2003. & Marshall. apparently stabilizing only in middle age (Roberts & DelVecchio. 1999) and Fox (Calkins. 1998. the assessment methods they use. and. both Kagan (Kagan & Snidman. in two independent studies. Also. this constant tendency being stable. 2003).
5 years of age was also associated with high levels of cortisol concurrently measured. & Gold. & Buss. 1997) or higher cortisol increases in response to stressful events (Nachmias. and greater postural change in diastolic blood pressure (Kagan. Reznick. Kagan. Behavior 10 (2006) 489-515
Calkins and Schmidt (2001) reported that 25% of the infants selected for these reactivity patterns remained inhibited through age four. reflected in the elevated secretion of the stress hormone cortisol. lower heart variability. and larger decreases in HP (heart rate acceleration) in response to unfamiliarity negatively correlated with behavioral inhibition in toddlerhood up to 7. Salivary cortisol levels – high baseline cortisol levels (Kagan.. 1991. amygdala in particular – is assumed to remain stable. decreased vocalizations. 1999)..A. Cardiac and neuroendocrine response systems. Kagan. and increased proximity to caregivers (see also Garcia-Coll. like De Haan. Benga.. Kagan et al. despite changes in the surface features of inhibited behavior. Although not sustaining the correlation between HP and behavioral inhibition at 4. 1988. Brain. Biederman et al. Schulkin. long latencies to approach. (1987) found elevated cortisol levels in 5. selected samples as data pools for such association studies (Fox et al. For example. 1999) – have been related to behavioral inhibition. inhibited behavior at 5. 1996. Reznick.5 years (Kagan et al. Parritz. such as motor quieting. Gibbons. Reznick. this pattern of physiological responses being stable over time. Gunnar. Behavioral inhibition has also been related to the activation of the hypothalamic-pituitary-adrenal hormone system. corresponding to higher heart rate. N.5 years. O. its underlying biology – the hyperexcitability of the limbic system.I. & Snidman. these results supporting the need for larger sample size. 2005). other studies. Fox. the extensive connectivity of this neural structure with different response systems pointing to its role in the modulation of physiological. However. 1987.5-year-olds who had been classified as behaviorally inhibited at 21 months of age. & Reznick. or inclusion of extreme. as well as certain aspects of cortical processing have been assumed to reflect the increased amygdala activation. 1984). Calkins and Fox (1992) found no relationship between behavioral inhibition and baseline levels of HP in an unselected sample of 2-year-olds. & Johnson.
. Schmidt. However. Snidman. acceleration of heart rate in response to mild stress / unfamiliarity. Kagan hypothesized the presence of individual differences in amygdala reactivity to novelty. 1990). motor and emotional reactivity (Kagan & Snidman. 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. 1984. Fox Cognition. Lower heart period (HP). As a neural substrate for behavioral inhibition. łincaş.5 years predicted which of the children would remain inhibited at age 7. Behaviorally inhibited children displayed characteristic behaviors when confronted with novelty.. 1989). & Gibbons. Mangelsdorf. Marshall and Stevenson-Hinde (1998) found that HP at 4. Schmidt et al. active avoidance.
Henderson. 1992. 1989. McManis.494
I. & Marshall. The majority of this work has focused on hemispheric asymmetries in EEG activation over the frontal region of the brain. (1996) supports this conclusion. & Woodward.. 1989) found that negative emotional temperament was negatively correlated with baseline cortisol levels in 13-monthold infants. Larson. Yet another parameter related to behavioral inhibition is the pattern of hemispheric activation in the prefrontal region. Also. Henderson. There are developmental data supporting the relations between frontal EEG asymmetry and this affective bias. Tout. adrenocortical activity may not necessarily map onto fear-related constructs. as measured via the electroencephalogram (EEG). compared to children who were also highly inhibited but who were securely attached. & Rubin. łincaş. Pérez-Edgar & Fox. has been considered the best predictor of temperamental outcome in infants across the first four years of life (Henderson et al. 2001. Fox. Fox Cognition. as reflected in the pattern of frontal EEG asymmetry. 2001. Snidman. Fox. 2002). Henderson & Marshall. Mangelsdorf. Benga. its functional significance being conceptualized in terms of motivational systems of approach and withdrawal (Davidson. O. Behaviorally inhibited children showed across studies a pattern of stable right frontal EEG asymmetry – higher right frontal activation. & Marshall. the right frontal region is thought to promote withdrawal-directed responses to perceived aversive stimuli. angry and aggressive behavior. The cortisol increase for inhibitedinsecure infants was also greater than that for the uninhibited infants. Dissociations between HPA activity and negative emotional responses have led to the assumption that novelty or discrepancy may be more important than the expression of negative affect in the activation of the HPA system (Fox. although negative emotional temperament was positively associated with elevations in cortisol during maternal separation at 9 and 13 months. found more equivocal associations: an increased cortisol response to starting preschool. Studies with infants have also found negative relations between negative emotionality and cortisol levels. Brain. Hart. 1991. associated with more assertive. Behaviorally inhibited children also had higher right frontal alpha desynchronization during the anticipation of a future
. The combination of behavioral reactivity and negative affect bias. as reflected in decreased alpha power in electrodes over the right frontal region – while uninhibited children showed higher left frontal EEG activation (Davidson & Fox. & Hertsgaard. 2001). 2005a). whether securely or insecurely attached. Kagan. Gunnar and colleagues (Gunnar. 1992. Henderson. 1994). but may be related to the maintenance or failure of coping strategies (Pérez-Edgar & Fox.A. Behavior 10 (2006) 489-515
Gunnar. The study of Nachmias et al. 2005a). and Stansbury (1998). & Jones. approach-directed emotional responses. their data showing that infants who were highly inhibited and insecurely attached had greater cortisol responses to the Strange Situation and the challenging coping episode. Fox. 2001). 1994. While the left frontal region is thought to promote appetitive. Bell. Mothers in secure dyads may support their inhibited children’s strategies for coping with unfamiliar and/or stressful situation (Fox. N. 2001. Fox.. Fox et al.
2003) showed that amygdala reactivity when viewing familiar versus novel faces was higher in adults from Kagan’s original sample who had been categorized as behaviorally inhibited in infancy. Marshall. Benga. Schwartz and collaborators (Schwartz. or might reflect bottom-up differences in early processes that may affect later processing and evaluation of sensory information. Brain. łincaş. Within an “oddball” auditory paradigm1. fMRI).to 12-year-olds) were found to have smaller mismatch negativity (MMN) amplitudes and longer latencies (Bar-Haim. Such individual differences in sensory processing could be either a consequence of top-down influences by higher affective centers such as the amygdala. 1999) or related to performance in an affective version of the Posner task (Pérez-Edgar & Fox. Fox. Wright. Schorr. Schmidt et al. This latter element (which includes attention. and selfsoothing) is thought to modulate reactivity throughout development. of superior temporal precision. 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. N. 2005b). & Gordon-Salant.. Using fMRI.I. ERP. Fox Cognition. EEG. 2003)2.A. In summary. socially withdrawn children (8. Kagan. The scarce neuroimaging evidence on brain functioning in behaviorally inhibited individuals seems to support the major assumption of Kagan’s theory.
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. thus giving an insight into the nature and timing of neural events. The dynamic balance between reactivity and regulation must always be approached within the context of the developmental trajectory of the child (Pérez-Edgar & Fox. approach/withdrawal. & Rauch. 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. 2005b). More recently. This study provides intriguing evidence of continuity in the physiological reactivity systems that might underlie behavioral inhibition (Pérez-Edgar & Fox. 2005b). behavioral inhibition. differences between behaviorally inhibited and uninhibited children have been revealed using ERP (event-related potential) techniques. All of these have generated results that seem to validate the existence of differentiating characteristics between behaviorally inhibited and behaviorally uninhibited individuals at both the behavioral and biological levels. 2 The MMN is an index of the function of a change-detection mechanism present in the primary auditory cortex. Behavior 10 (2006) 489-515
negative social event (giving an embarrassing speech. O.
1981. presumably including the brain stem. and (2) Effortful control executive attention system.5 months).5-10 /13..496
I. low intensity pleasure and perceptual sensitivity).. Rothbart & Ahadi. The model (Rothbart. Putnam. 2001. the ability to inhibit a dominant response in favor of a sub-dominant (but presumably more contextually-adaptive) one (see Rothbart & Posner. 1982). The progressive development of the second system allows for an increased regulation and modulation of the reactive tendencies over development. Behavior 10 (2006) 489-515
though the assumption is that below the surface changes.A. Gartstein & Rothbart. the instruments developed by Rothbart and her collaborators (see Rothbart.. 1994. but continues to develop throughout adolescence. However. related to Gray’s (1975) Behavioral Inhibition System (BIS). manifested especially through effortful control. Rothbart et al. but differences between them will start to emerge once they are observed in interactions with unfamiliar adults or peers. that is. In keeping with the idea of emotion driving self-regulation. while preserving the core underlying temperamental dimensions. linked to Neuroticism and to Gray’s Behavioral Inhibition System). 2000). As a consequence. Rothbart et al. (2000) found
. 2003. (3) Effortful Control (includes sub-dimensions of inhibitory control. a behaviorally inhibited and a behaviorally uninhibited child might both look quite similar if placed in a socially-familiar environment. O. and is conceptually linked to Eysenck’s Extraversion and Gray’s Behavioral Activation System – see Gray. which organize into three main higher-order factors: (1) Extraversion / Surgency (which includes primarily sub-dimensions like positive emotionality and approach. Benga. Hershey. there are several temperamental dimensions. & Rothbart. targeting children 3 to 7 years of age. 1994) postulates the existence of two temperament-related regulatory or control systems: (1) Behavioral inhibition system. Rothbart et al. hippocampus and amygdala. the anterior cingulate gyrus. an active control system. 2006. Brain. & Fisher. a passive control system. thought to develop late in the first year (6. 2001). Rothbart et al. Fox Cognition. łincaş. Ahadi. 2001). attentional focusing. and is related to the dorsolateral prefrontal cortex. The defining characteristic of this temperament model is the explicit inclusion – as a temperamental dimension in itself – of self-regulation. Gartstein. 1989. One wellknown instrument assessing these dimensions of temperament is the Children’s Behavior Questionnaire (CBQ. orbital frontal cortex. the temperamental traits remain stable. the surface individual and developmental variability points to the need of taking into account contextual appropriateness in measuring a certain temperamental trait (Rothbart & Deryberry. medial septal area. which emerges at the end of the first year. 2001 for a more detailed discussions of effortful / attentional control). Rothbart. supplementary motor area and portions of the basal ganglia (Rothbart & Posner. 1981. At every age. Rothbart & Ahadi. (2) Negative Affectivity (includes negative affectivity. N. at the biological level. For example. shyness and avoidance. 2000) maintain the underlying assumption of a developmental change in the surface features of temperament.
O. Both Kagan’s and Rothbart’s models have generated large amounts of research that have helped consolidate and develop the two constructs and their corresponding measurement methods. 2002.I. 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-reported attentional control (Derryberry & Reed. 2005. & Fox.A. & Kovacs.. Systematic research is still needed.. Pérez-Edgar & Fox. It seems thus possible that the mechanisms used to cope with self-regulation of emotion in early development are then transferred to issues of control of cognition during later infancy and childhood (Rothbart & Posner.g. łincaş. Pérez-Edgar.g. 2005a): poor self-regulation is thus considered a critical variable in the development and maintenance of anxiety. Compared to the categorical approach of behavioral inhibition. Cohn. By the end of the first year of life. and to point to relations between temperament and emotional functioning. Behavior 10 (2006) 489-515
evidence that this second self-regulatory system is related to attentional control or executive attention. acting as a buffer in the face of negative reactivity. suggesting an inhibitory control on the amygdala by mid-frontal regions. The primary form of regulation consists in distress control via attention focusing. Brain. 1991) assuring the regulation of behavior via executive attention. N. and not a temperamental dimension per se (Fox et al. the fruitfulness of this approach is reflected in the growing understanding of the fact that early reactivity. the anterior attention system emerges (Posner & Rothbart. Fox Cognition. though present from the first months of life. even when acknowledged as a mediator of the relationship between temperament and anxiety. 1998). 2006). 1994). However. Rothbart’s continuous model of the dynamic relationship between reactivity and selfregulation has been considered less straightforward for the delineation of individual temperamental differences (Pérez-Edgar & Fox. even more if we acknowledge that a child’s inability to regulate negative affect can be differentially expressed across three realms: behavior (e. Even adults who report themselves as having good ability to focus and shift attention seem to experience less negative affect (Derryberry & Rothbart. cognition (e. does not dictate outcome (Calkins & Fox.. low self-worth) and psychophysiology (e. anxious withdrawal). The hypothesis of a connection between temperament and emotionality in general has probably been one of the factors that further stimulated interest in the link between temperament and emotional psychopathology. This research has also managed to shed some light into the underlying biology of temperament.. Fox. we must notice the emphasis placed on attentional control. 2001). Of particular interest for the present paper. as a function of intrinsic (developmental) as well as extrinsic (environmental) constraints. And since developmentally temperament represents probably the first manifestation of
. in order to fully understand all interactions that underlie psychopathological outcomes of temperamental tendencies. 2005a). Benga. elevated cortisol levels) (Schmidt.g. 1988).
Pfister.A. N. Other studies. some anxiety symptoms – covering generalized/overanxious anxiety disorder and social anxiety – seem to be part of the same syndrome as depression. while separation anxiety disorder seems to be linked to future panic disorder (Masi. 2001. 2001). Fox Cognition. overt manifestations and comorbidity. obsessions and compulsions seem to be subsumed to a distinct dimension of anxiety. Benga. Lahey et al.358 children and adolescents (4 to 17 years of age). and long-term tendencies of an anxiety response to environmental events (trait anxiety). Dierker. Anxiety disorders are considered among the most common forms of child psychopathology. Wittchen. as well as its developmental patterns. 1997) (for children/adolescents 8 to 19 years of age) indicate six clusters of symptoms. whereas separation anxiety.or parent reports. we will particularly address this topic. social phobia. 2001. or at most subclinical levels of acute or immediate (state anxiety). Stolar. panic-agoraphobia. generalized anxiety and fears of physical injury – though high intercorrelations between factors could be
. 1998). & Wittchen. 1994) and ICD-10 (World Health Organization. & Merikangas. trait anxiety and anxiety disorders. Kessler. it has been suggested that childhood anxiety disorders are not transient phenomena for many children. the third category comprises pathological anxiety. (2004) suggest some differences from DSM-IV regarding anxiety disorders: in particular. persisting throughout adolescence and adulthood. and generalized anxiety disorder in particular. Longitudinal studies support such distinction. While the first two cover normative. like the Spence Children’s Anxiety Scale (Spence. & Millepiedi. Brain. łincaş. & Lieb 2000). O. the next natural step was to investigate the function that it might play in the emergence of psychopathology in children. based on self. Since research joining temperament and anxiety in childhood has focused predominantly on clinical anxiety. around 8-12% of children meeting diagnostic criteria for some form of anxiety disorder that perturbs the normal functioning of the child (see Spence. specific phobia. In a recent study based on a representative sample of 1. obsessive-compulsive disorder. Li. being primary conditions that frequently precede depression (Avenevoli.498
I. Höfler. Keller. relating to separation anxiety. Furthermore. CHILDHOOD ANXIETY Research often distinguishes between state anxiety. We will now turn to discussing one such form of psychopathology – namely childhood anxiety – by analyzing aspects related to its epidemiology. anxiety disorders. Behavior 10 (2006) 489-515
individuality. Kessler. Taxonomic criteria for childhood psychopathology based on DSMIV (American Psychiatric Association. although developmental differences have to be considered. Mucci. 1992) suggest that at least some of the adult syndromes can also be identified at early ages.
2005a).61. & Verduin. Other studies have indicated high comorbidity between depression . It is this “route” that we now turn to. by discussing the degree to which extant evidence supports temperament as a risk factor for anxiety disorders. Serra. 2005. However. and Ingram (2001). 2003. respectively between anxiety and ADHD – 34. O. 2001). thus. łincaş. Behavior 10 (2006) 489-515
explained by a higher order factor of anxiety in general. Second. 2000. Pérez-Edgar & Fox. for example.5 years. TEMPERAMENT AND THE RISK FOR ANXIETY DISORDERS As already mentioned. Even if the early presence of childhood psychopathology may have a predictive value for the subsequent onset. Comorbidity modifies prognosis in a significant way and may suggest specific therapeutic interventions according to each case. overanxious / generalized anxiety disorder or avoidant disorder/social phobia) (Kendall. McDonald. Brady. 1992). research has started investigating temperament as a possible “ingredient” in the emergence of psychopathology in children (see reviews by Clark. as Frick (2004) and Lahey (2004) have pointed out. severity and persistence of other disorders. that childhood anxiety disorders still need to be explored. N. Fox Cognition. confirm this structure of anxiety symptoms. Benga.A. In this case. & Kendall. Rapee. Brain. 79% of them presenting symptoms for more than one anxiety disorders (separation anxiety disorder. & Franco. some of the instruments used to measure temperament contain items that overlap with clinical criteria used to diagnose psychopathology.5 to 6. In clinical samples. Another promising route regards the behavioral. First. establishing the exact nature of the relation between these two constructs – as well as its plausible underlying mechanisms – is complicated for at least three reasons. Goldsmith & Lemery. there are multiple additional risk or protective factors (like.I. environmental and biologic markers of risk and in particular the exploration of early temperamental traits as a predisposing factor for later psychopathology. moreover when we consider the preschool age. Spence.. the links with future pathology are not yet very clear. Mattos.3% (Souza. 2001). using Spence Preschool Anxiety Scale on children 2. however with less clear-cut delimitations of anxiety subtypes. it has also been noticed a high comorbidity in anxious children. It seems. Hirshfeld-Becker et al. parenting characteristics) coming into play on the pathway leading from a certain temperamental profile to the presence or absence of psychopathological symptoms – and this is more acute if we consider the behavioral inhibition framework. any relations between temperament and symptomatology obtained through
many studies highlight that not (only) amygdala hyperactivation. 2004). 2002. Vasey.. Lengua. startle response. plead for functional differences between children with anxiety and their healthy counterparts. For example. West. Pérez-Edgar & Fox.
. volumetric data (Milham et al. other authors see psychopathology simply as an extreme manifestation of a certain temperamental pattern (Lahey. In this sense. 2003. Vasey & Dadds. N. Keightley et al. salivary cortisol). 1998). and sustain that amygdala hyperactivation coupled with a deficitary control over it by frontal
3 However. heart rate and heart rate variability. Behavior 10 (2006) 489-515
such measures will be artificially inflated3. can develop on the foundation of temperamental risk factors. & Hazen. theoretical complications are added by the fact that different authors see the relation between temperament and anxiety in different ways: some conceptualize temperament as reflecting individual variability within the normal/typical range. Brain. De Bellis et al. Lonigan. All these data. Third. & Phillips.500
I. 2001). Fox Cognition. 2005) showed reduced left amygdala in pediatric anxiety. Sander et al. 2005) in adults. abnormally large right amygdala volumes have been reported not only in adults. Lonigan.A. 2002. 2005a. Essex. like: overly sensitive danger detection systems. but also in children and adolescents with generalized anxiety disorders (see Schore. Benga. avoidant coping style. the magnitude of amygdala signal correlating with the severity of everyday anxiety symptoms. attentional bias to threat. The rationale for bridging the two constructs is mainly the presence of common characteristics shared by anxiety and temperament – in particular behavioral inhibition (Anthony. On the other hand. psychophysiologic patterns (EEG asymmetry. with psychopathology being a distinctive entity that. under certain circumstances. O. & Smider. & Sandler. 2001). but perturbations of the neural networks involved in anxiety from the healthy state might be critical in understanding the neurobiology of anxiety disorders. pupil dilatation. although still insufficient. and probably in children as well. some of these instruments do seem to retain their predictive value even after elimination of the overlapping items (see Lemery.. but a deficitary attentional topdown control is associated with anxious symptomatology (Hamann & Canli. (2000) found in a MRI study significantly larger right and total amygdala volumes in children with generalized anxiety disorders (age 8-16) compared to normal children. 2001) also revealed an exaggerated amygdala response to fearful faces in children with anxiety disorders (8-16 years of age) compared to healthy children. coming back to Rothbart’s model.. Hooe. łincaş. Functional neuroimaging studies (Thomas et al. in terms of common neurobiological grounds. and an overreactive amygdala. 2004. suggesting that not the absolute volumetric variations. Phillips. 2004..
Curent age: 13 years.5 years)
BI (lab observation) BI stability Child psychopathology (DSM-based interview) BI (lab observation) Child psychopathology (DSM-based interview)
Schwartz et al (1999)
Kagan cohort (children followed since 4 months and rated for BI first at 14 months and 21months) Kagan cohort. High-risk sample: higher rates of overanxious
Biederman et al. No significant differences for other anxiety disorders. Temperamental predictors of anxiety disorders In what follows.. Behavior 10 (2006) 489-515
structures. Biederman et al. O.
The BI children had significantly higher rates for anxiety disorders – including multiple anxiety disorders and phobic disorders (mostly social). Summaries of studies linking temperament to psychopathology in children or adolescents. We preferred to leave out discussion of studies targeting the temperament-externalizing disorders link.
Hirshfeld et al.
Table 1. would be characteristic for anxiety disorders – as well as for certain temperamental precursors. Fox Cognition. Although especially in young children the distinction between internalizing and externalizing disorders cannot be drawn in a very clear-cut manner. most studies seem to indicate quite separate temperamental predictors for these two broad psychopathological categories (e. łincaş. adolescents and young adults. Child psychopathology (DSM-based interview)
Clinical (referred) sample: 4-7 years. Longitudinal sample: 7-8
. N..I.g. The samples involve children. (1992)
Longitudinal (21 months – 7. 2001). Gender: more pronounced difference for girls. Brain. we attempt to draw a few tentative conclusions related to the temperament–anxiety link and its specificity.A. Benga. Higher rates of multiple anxiety disorders in both samples compared to controls. 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 of temperament.
Significantly higher rates of social anxiety in BI than BUI adolescents. These studies are summarized in table 1. or longitudinally). (1990)
BI (lab observation).
Clinical (referred) sample. Age: 2-6 years
Significantly higher rates of social anxiety disorder in BI than in BUI children. PD+MD. BI stability (assessed over a three-year interval) Child psychopathology (K-SADS-E) – parent report. No interaction effects.
Biederman et al. at threeyear follow-up. No interaction effects. 21 years in children rated as Age: 3-21 years BI at 3. MD. version of Thomas & Chess’ scale) Attachment security (SSP – preschool version) Child anxiety disorders (ADIS-CPIV. DSM-IV-based interview. łincaş. DSM-based interview). AG.
Hayward et al (1998)
Longitudinal / Retrospective
Higher social avoidance and fearfulness in the 9th grade was significantly
years from Kagan’s cohort (selected at 21 months for extreme BI). Benga. (2001)
BI (lab observation). Parental diagnosis (PD.
BI children had higher rates of anxiety disorders and higher rates of newly-onset anxiety than BUI children. control – SCID: DSM-based interview). Longitudinal sample: higher rates of phobias (mainly social).502
I. BI (Reznick Retrospective SelfReport of High-school students 9-12th grade.
Caspi et al (1996)
Longitudinal / Prospective (3-21 years)
BI (assessment of behavior during a testing session. Independent effects of BI and parental diagnosis. Current age: 411 years. Fox Cognition.A. Stable BI children had higher rates of all anxiety disorders assessed (mostly multiple and avoidant anxiety disorder). N. (2005)
BI (lab observation + Non-clinical parent questionnaire – sample. The clinical sample from Biederman et al (1990).
ShamirEssakov et al. parent).
Non-clinical Higher rate of depression at sample. No differences for anxiety (only current disorders were assessed).
Biederman et al (1993)
Longitudinal / Prospective
BI (lab observation). at 3 years) Psychopathology (assessed at 21 years. Maternal trait anxiety (STAI-Y). O. Behavior 10 (2006) 489-515
Parental diagnosis (PD. control). MD.
BI and attachment status were both independently related to child anxiety (N too low to distinguish among different anxiety disorders). STSC – a modified Age: 3-5 years. Controls. Child psychopathology (K-SADS-E).
Anxiety (SCAS). Age: 11-15 years
associated to the risk for developing newly-onset social phobia. van Brakel et al (2006) Concurrent BI (three levels of BI: high. anxiety seems to mediate the link between BI and depression. Anxiety and Major depression (RCADS – adaptation of SCAS).
Muris & Meesters (2002)
Non-clinical sample.A. No interaction effects. Attachment (SSP) Stress reactivity (cortisol level). Anxiety (SCARED) Worry (PSWQ-C) Depression (DQC). O. BI (BIS. Age: 12-18 years.a 1-item global assessment). but similar patterns of results.
The three factors were significant independent predictors of child anxiety. low) BI (BIS.
Non-clinical sample. Depression (CDI). Fox Cognition. a 4-item self-report questionnaire + a 1item global assessment). Child. BI and attachment were significant independent predictors of anxiety disorders. BI (BII . Age: 12-15 years
Significant links between BI and both anxiety and depression. a 4-item self-report questionnaire + a 1item global assessment). a 4-item selfreport questionnaire). (1996)
Non-clinical Attachment status had a sample moderating role in Age: 18 months predicting stress reactivity from BI. Significant but small interaction between BI and Attachement. medium. low)
Non-clinical sample. mediu m.I. mediu m. yearly assessment (9th-12th grade). Attachment (questionnaire – AQC).and parentreport Non-clinical sample. Instead. mediu m.
Nachmias et al. Parenting style (measured using a Swedish questionnaire). Child anxiety (SCARED). Attachment (questionnaire – AQ-C).
Muris et al. BI (lab observation + TBAQ). low)
BI (BIS. Discrepancy between parent and child reports.
. No specific relation to social phobia. łincaş. low) BI (three levels of BI: high. Age: 11-15 years
Muris et al (1999)
BI (three levels of BI: high. Significant relation to certain anxiety disorders. There was a significant effect of BI on social anxiety and separation anxiety disorder. Brain. N. Behavior 10 (2006) 489-515
Inhibition) Child psychopathology (social phobia & depression). Significantly more insecurely attached children were BI. (2001)
BI (three levels of BI: high. self-rated. Benga. No evidence of a direct link between BI and depression. Significant linear association of BI to psychopathological symptoms in general.
Abbreviations for Temperament / Psychopathology categories: BI=behavioral inhibition / behaviorally inhibited. N.A. Maternal depression and child fear/shyness predicted internalizing behavior across the 12year span. 5 assessment episodes)
Emotio nal reactivi ty and regulati on
Girls’ internalizing behavior increased over time. 1984).504
I. CBCL – parent) All the variables from Lengua et al (1998). Brain.
Leve et al (2005)
Longitudinal (5-17 years. MD=major depression.
Our analysis is guided by the intention to determine de degree of predictive specificity of the temperamental characteristics included in studies related to internalizing disorders. K-SADS-E = Schedule for Affective Disorders and Schizophrenia for School-Age Children – Epidemiologic Version. Parenting (Child Report of Parenting Behavior Inventory) Temperament (CBQ) Parental environment (discipline. marital adjustment. Attachment: SSP = Strange Situation Procedure. SCARED = The Screen for Child Anxiety Related Emotional Disorders. for anxiety
Positive emotionality was found to be a moderator (protective factor) between parental rejection and depression. PD=panic disorder.
Lengua et al (2000)
Emotio nal reactivi ty and regulati on
Non-clinical sample Age: 9-12 years. Abbreviations for measurement scales: Temperament: STSC = Short Temperament Scale for Childrenl. PSWQ-C = Penn State Worry Questionnaire for Children. AQ-C = Attachment Questionnaire for Children.
Negative emotionality was significantly related to depression. Positive emotionality (DOTS-R) Self-regulation (CBQ. Fox Cognition. DQC = Depression Questionnaire for Children. CDI = Child Depression Inventory. DOTS-R = Dimensions of Temperament Survey – Revised. maternal depressive symptoms. Behavior 10 (2006) 489-515
Lengua et al (1998)
Emotio nal reactivi ty and regulati on
Negative emotionality (Buss & Plomin. Externalizing behavior decreased for both genders. AG=agoraphobia. Goldsmith & Rothbart. 1991) Depression (CDI – child. SCAS = Spence Childhood Anxiety Scale. BUI=behaviorally uninhibited. Psychopathology: CBCL = Child Behavior Checklist. łincaş. O. RCADS = Revised Children’s Anxiety and Depression Scale. STAI = State-Trait Anxiety Inventory (for parents). family income) Internalizing & externalizing disorders (CBCL)
Non-clinical sample Age: 9-12 years. We are mainly interested in establishing whether these characteristics are predictive for a certain type of anxiety disorder. Benga.
parent and teacher ratings of child anxiety symptoms were obtained. & Taylor. O. A consistent proportion of research using the construct of behavioral inhibition seems to have identified a specific link to social anxiety (social phobia. and subsequently re-evaluated when they were 4. Others have identified similar relations on different samples... 1998. behavioral inhibition classification in infancy was significantly related to the later development of anxious symptoms. In a further study. 1990. They found that a significant number of the adolescents categorized in infancy as being highly reactive were having symptoms of social anxiety. using questionnaires instead of the classical observational procedure (Hayward. a significant predictor of social anxiety.5 and 7. Schwartz et al. Here.5 years old. For example. 1999). There was also a relation with parental diagnosis of panic disorder. Biederman et al. 2005a). However. Hirshfeld et al.. The link between behavioral inhibition and anxiety is probably readily obvious due to the many characteristics that the two constructs seem to share (Pérez-Edgar & Fox. Killen. there is also evidence pointing to a more general relation. Behavior 10 (2006) 489-515
disorders in general. 2002).. assessed either through traditional laboratory observational procedures (e. despite this supporting data.. As indicated in table 1. or whether they are even more nonspecific indicators – of a risk for internalizing disorders in general. In another study. most studies of interest to the present topic have focused on the concept of behavioral inhibition (as initially defined by Kagan).. Brain.
. 2001. Benga. which indicated that behavioral inhibition was. (1999) interviewed adolescents from this longitudinal sample. Fewer studies have been conducted using Rothbart’s model and the respective assessment instruments. These children were assessed for behavioral inhibition at 14 and 21 months. Kagan and Snidman (1999) described the longitudinal study which followed a cohort of children starting when they were 4 months old... but the two factors were independent of each other. there seems to be at least some support (using two types of assessment methods) for predicting a higher probability of present or future social anxiety in behaviorally inhibited children. Most studies linking behavioral inhibition to social anxiety have included participants from Kagan et al’s (1984) original sample (Biederman et al. N.I. Merckelbach. Biederman and colleagues (Biederman et al.g. During this last assessment. in the absence of significant manifestations of any other anxiety disorder. on its own. Wessel. Results indicated that although behavioral inhibition stability was modest. Schwartz et al. Thus.g.. Muris & Meesters. Fox Cognition.A. Muris. łincaş. & van de Ven. avoidant disorder) (see also Ollendick & Hirshfeld-Becker. Kraemer. 2001) or through questionnaires administered to the parent and/or child (e. Biederman et al. 1999). 1992. (2001) included externalizing symptoms in their assessment of psychopathology to further test the predictive specificity of behavioral inhibition. the only significant relation found was that of behavioral inhibition with social anxiety disorder. 2002 for a recent review on the topic).
the relation between behavioral inhibition and depression was mediated by anxiety. anger seemed to be a significant predictor for externalizing disorders.to 14-year-old children. A group of studies using the behavioral inhibition construct but relying exclusively on questionnaire measures seem to indicate a similarly general role for behavioral inhibition in predicting concurrent anxiety symptoms. & Bohlin. behavioral inhibition seems to be a quite consistent predictor of anxiety. However. Berlin. & Bogie. N. and Rapee (2005) in 3 to 5-year-old children (although here more detailed conclusions were impeded by the very low number of children in each specific anxiety disorder category). depression). However. 1999). Muris et al. The strongest link was between anxiety symptoms (in general. (1999) investigated the relation between behavioral inhibition (child self-rated) and psychopathology (anxiety. Benga. O. despite the variability in assessment methods. Their results indicated higher levels of psychopathology in children who rated themselves as high in behavioral inhibition. while fear significantly predicted
. or even behavioral inhibition and other internalizing disorders (e.g. Although probably caution is necessary when interpreting the results of some studies (e. Bögels. Brain. we can conclude that the data does generally support the existence of a fairly specific link between behavioral inhibition and anxiety. Merckelbach. The results showed that the lower-order emotional traits discriminated between externalizing and internalizing disorders. To summarize. A similar relation between behavioral inhibition and anxiety symptoms in general was found by van Brakel. even though negative affect predicted psychopathology in general. More specifically. Fox Cognition. and Thomassen (2006) in children aged between 11 and 15 years.. while others indicating a more general relation between behavioral inhibition and anxiety. Schmidt..A. Behavior 10 (2006) 489-515
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 years before. 2003) measured emotionality using scales essentially similar to Rothbart’s Negative Emotionality and Surgency/Extraversion from the CBQ. depression) in 12. not just social anxiety) and behavioral inhibition. łincaş. Less clear conclusions can be formulated with respect to Rothbart’s model. Gadet. Also. A subsequent study (Muris.. the behavioral inhibition measures used in these 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). because there are almost no studies investigating relations between the various temperament dimensions and anxiety. The only relevant study we could identify (Rydell.. in a large sample of adolescents (12-18 years). respectively.506
I.g. girls exhibited higher levels of these disorders than did boys. Ungerer. worry. 2001) identified relations between behavioral inhibition and anxiety and behavioral inhibition and depression. Muris. those assessing behavioral inhibition with short questionnaires – Muris et al. Similar results were found by Shamir-Essakov. with some studies supporting a very specific link to social anxiety.
but taking into account the results of Muris et al. & Silva. has fast heart rate. and who displays these symptoms over a period of time might be considered to meet criteria for a DSM anxiety disorder. Caspi and colleagues (Caspi. this study focused on internalizing (and externalizing) disorders in general. N. Thus. Probably more studies would be needed to clarify the relation of behavioral inhibition to depression. As can be noted in table 1. O. However. Wolchik.I. Most of the existing data seems to support a link between behavioral inhibition and anxiety. Similar results were found by Leve. 2000) indicated that positive (not negative) emotionality played a moderating role between parental rejection and depression. However. Lengua and collaborators. Fox Cognition. (2001). They discussed several longitudinal studies indicating a bias for the relation between emotional reactivity (neuroticism) and internalizing disorders. A medical/psychiatric approach views illness or disorder as reflected in number and constellation of symptoms. Muris and Ollendick (2005) recently reviewed evidence for their 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 as emotional reactivity) and low effortful control. The medical/psychiatric model is more of a static approach to temperament while the Rothbart approach provides entry into a dynamic picture of the developing child. Kim. Sandler. one could reasonably state that the presence of only depression at 21 years does not exclude the previous occurrence of anxiety. However.A. Thus. but the results converge with a limited number of studies showing links to internalizing disorders other than anxiety (namely. when discussing possible reasons for this
. using a composite measure of temperament derived from different scales showed a link between negative affectivity and depression (Lengua et al. and the fact that Caspi et al. Behavior 10 (2006) 489-515
internalizing disorders. 1998). 1996) found a relation between behavioral inhibition assessed at 3 years and symptoms of depression at 21 years. In the case of Rothbart’s model. a child who fears novelty. withdraws from social situations. but no significant link to anxiety. subsequent analyses including parenting style as a factor (Lengua. One possible reason for the paucity of research linking temperament and psychopathology with Rothbart’s model is the inherent contradiction between a process based model (Rothbart) and a typological or categorical position (psychiatric diagnosis). and Pears (2005) using the CBQ. Moffitt.. depression). (1996) only included an assessment of current (not lifetime) psychopathology. Newman. Benga. łincaş. Brain. and this link seems to be specific at least as far as the larger group of anxiety disorders are concerned. The fact that these “symptoms” or behaviors may change as a function of development. & West. or that specific moderators of these behaviors such as parenting or executive functions may change the trajectory of development is often not of critical importance in this view. the paucity of studies and the multidimensional nature of the construct itself make clear predictions more difficult.
Fox Cognition. 1992. the most probable conclusion would be that behavioral inhibition and certain dimensions related to reactivity and selfregulation might constitute relevant predictors for anxiety (and they might be less relevant for other internalizing disorders like depression). and what differentiated between them was the lower-order trait indicating the dominant emotion (e.. Thus. Such studies were able to show that reactive emotionality was predictive of both internalizing and externalizing symptoms. or very general assessments of psychopathology (or both). 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. fear versus anger). but it points to the necessity for caution when interpreting the data.anxiety link. parental psychopathology (Rosenbaum et al. they pointed to the fact that these studies measured temperament with questionnaires covering lower-order traits (for example. łincaş. while at least some conclusions and hypotheses can be formulated for the behavioral inhibition .. Schwartz et al. 2000). 2003 used Ellis & Rothbart’s 2001 Early Adolescent Temperament Questionnaire).508
I. Rydell et al. 2004). On the other hand.. Most of the above studies that pointed toward less specificity have either used very general questionnaire measurements of behavioral inhibition. These factors include mostly aspects related to parental environment. referred samples. Muris et al. 1998.g. this does not necessarily favor the narrow specificity interpretation. 1999). 1996). parenting style (van Brakel et al. instead focusing exclusively on anxiety and the predictive value of temperament. 2006) or general family environment (Hirshfeld-Becker et al. N. This information. 2001. and used more complex measurement instruments both for behavioral inhibition and anxiety (Biederman et al.g.. Brain. as an aside it can be mentioned that in most studies reviewed here (with the exception of Nachmias et al..... 1996. Another important point of caution relates to the fact that beyond the temperament -anxiety relation there are several factors that come into play during development and that can act as moderators or as additional risk/protective factors. Benga.. or had samples with symptoms that did not reach clinical intensity of symptoms (e. 1999). the studies that linked behavioral inhibition to social anxiety had selected. However. 2002). while it is likely that these predictors might not extend to internalizing disorders in general. Of course. Lengua et al. However.. O. like attachment security (Nachmias et al. The relations between these factors are extremely complex and most of them seem to be related both to temperamental and psychopathological outcomes. along with their individual effects. future research using Rothbart’s model would probably have to take on a more exploratory approach. their predictive value might in fact be narrower – that is. Behavior 10 (2006) 489-515
bias. Muris & Meesters.. Regarding the specificity issue. as well as the research already discussed (and the one still lacking) indicates that the relation
. related to specific anxiety diagnoses. The present paper did not explicitly take into account these factors.A.
N. A. M. (2002). C. (1996). A 3-year follow-up of children with and without behavioral inhibition. Meminnger. Dierker. & Gordon-Salant.. Schorr. F.
.. 14. Friedman. V. 67. Biological Psychiatry. Snidman. Anthony J. J. Marshall. Biederman. S.. and behavioral inhibition at twenty-four months. S. R.
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