Annual Research Review: Developmental pathways linking early behavioral inhibition to later anxiety.

Behavioral Inhibition is a temperament identified in the first years of life that enhances the risk for development of anxiety during late childhood and adolescence. Amongst children characterized with this temperament, only around 40 percent go on to develop anxiety disorders, meaning that more than half of these children do not. Over the past 20 years, research has documented within-child and socio-contextual factors that support differing developmental pathways. This review provides a historical perspective on the research documenting the origins of this temperament, its biological correlates, and the factors that enhance or mitigate risk for development of anxiety. We review as well, research findings from two longitudinal cohorts that have identified moderators of behavioral inhibition in understanding pathways to anxiety. Research on these moderators has led us to develop the Detection and Dual Control (DDC) framework to understand differing developmental trajectories among behaviorally inhibited children. In this review, we use this framework to explain why and how specific cognitive and socio-contextual factors influence differential pathways to anxiety versus resilience.

Children's shyness and physiological arousal to a peer's social stress.

Previous work has shown that children's shyness is related to personal anxiety during social stress, but we know little about how shyness is related to anxiety during a peer's social stress. Children (Mage  = 10.22 years, SD = 0.81, N = 62) were paired with an unfamiliar peer and engaged in a speech task while electrocardiography was recorded. We modeled changes in children's heart rate, a physiological correlate of anxiety, while they observed their peer prepare and deliver a speech. Results revealed that the observing child's shyness related to increases in their heart rate during their peer's preparation period, but modulation of this arousal was sensitive to the presenting peer's anxious behavior while delivering their speech. Specifically, if the presenting child displayed high levels of anxious behavior, the observing child's shyness was related to further increases in heart rate, but if the presenting child displayed low levels of anxious behavior, the observing child's shyness was related to decreases in heart rate from the preparation period. Shy children may experience physiological arousal to a peer's social stress but can regulate this arousal based on social cues from the peer, which may be due to heightened social threat detection and/or empathic anxiety.

Bidirectional and interactive effects of child temperament and parenting in early childhood on the trajectory of social anxiety in adolescence.

INTRODUCTION: Research suggests that certain parenting behaviors are best suited to promote optimal child development, depending on a child's distinctive temperamental presentation. This multimethod, longitudinal study examines the interactive effect of parenting and temperament in early childhood on the developmental trajectory of social anxiety in adolescence. METHODS: Longitudinal growth modeling was used to examine the developmental trajectory of child social anxiety from age 9-15 and the interactive effect of parenting and child temperament at 36 months on the developmental trajectory of child social anxiety from age 9-15. RESULTS: The slope of social anxiety from age 9-15 suggested a decrease in social anxiety throughout early adolescence. Furthermore, 36-month behavioral inhibition (BI) predicted the trajectory of child social anxiety from age 9-15 when parents displayed low and high levels of dismissive and supportive parenting (at 36 months). CONCLUSIONS: Results support an interactive effect of infant temperament and parenting in early childhood (at 36 months) on the developmental trajectory of child social anxiety from age 9-15. Specifically, results suggest that engaging highly inhibited children with high supportive and low dismissive parenting may help reduce social anxiety over time in adolescence. Furthermore, parenting needs may differ for children high or low in BI to impact the developmental trajectory of social anxiety in adolescence, such that children who are high BI seem to benefit from low dismissive and high supportive parenting, and children who are low in BI seem to benefit more from high dismissive parenting.

Trajectories of socially anxious behavior from age 5 to 13: Temperamental and sociocognitive pathways.

The authors examined temperamental and sociocognitive predictors of socially anxious behavior from preschool to early adolescence. Children (N = 227; 59% male; 69% White) completed a speech task at ages 5, 7, 10, and 13 and socially anxious behaviors were coded. Behavioral inhibition (BI) was assessed at ages 2/3 and Theory of Mind (ToM) was assessed at age 4. Data collection occurred between 2003 and 2016. Three trajectories of socially anxious behavior were identified: high stable, average increasing, and low stable. Higher BI was related to the high stable trajectory, whereas lower ToM was related to the increasing trajectory of socially anxious behavior. There are heterogenous pathways of socially anxious behavior, which may be uniquely influenced by early temperamental and sociocognitive factors.

Infant temperament prospectively predicts general psychopathology in childhood.

Recent models of psychopathology suggest the presence of a general factor capturing the shared variance among all symptoms along with specific psychopathology factors (e.g., internalizing and externalizing). However, few studies have examined predictors that may serve as transdiagnostic risk factors for general psychopathology from early development. In the current study we examine, for the first time, whether observed and parent-reported infant temperament dimensions prospectively predict general psychopathology as well as specific psychopathology dimensions (e.g., internalizing and externalizing) across childhood. In a longitudinal cohort (N = 291), temperament dimensions were assessed at 4 months of age. Psychopathology symptoms were assessed at 7, 9, and 12 years of age. A bifactor model was used to estimate general, internalizing, and externalizing psychopathology factors. Across behavioral observations and parent-reports, higher motor activity in infancy significantly predicted greater general psychopathology in mid to late childhood. Moreover, low positive affect was predictive of the internalizing-specific factor. Other temperament dimensions were not related with any of the psychopathology factors after accounting for the general psychopathology factor. The results of this study suggest that infant motor activity may act as an early indicator of transdiagnostic risk. Our findings inform the etiology of general psychopathology and have implications for the early identification for children at risk for psychopathology.

Mind wandering and executive dysfunction predict children's performance in the metronome response task.

Mind wandering is a ubiquitous experience during adulthood and has received significant scholarly attention in recent years. Relatively few studies, however, have examined the phenomenon in children. Building on recent work, the current study examined the frequency and validity of children's reports of mind wandering while completing a minimalistic task previously unused in past child research-the Metronome Response Task (MRT) [Journal of Experimental Psychology: Human Perception and Performance (2013), Vol. 39, pp. 1-5]. Furthermore, the current study examined how parent reports of executive dysfunction in daily life relate to children's reports of mind wandering and behavioral performance in the MRT. A total of 81 children aged 7-9 years completed the MRT, the demands of which simply involved pressing a key on a computer keyboard in concert with the unwavering tones of a metronome. Sporadic experience-sampling probes gauged whether children were on-task or mind wandering. Parents also reported on their children's day-to-day difficulties with executive functioning across several domains. A series of multilevel models revealed that children reported being on-task more frequently then mind wandering and that children were more variable and less synchronous in their keypresses preceding reports of mind wandering than preceding reports of being on task. In addition, parent-reported difficulties with behavioral regulation predicted higher rates of mind wandering, whereas both behavioral dysregulation and metacognitive difficulties predicted lower MRT performance. These findings suggest that children are able to reliably report on their experiences of mind wandering in boredom-inducing contexts and advance our understanding of the factors underlying children's experience of mind wandering under real-world conditions.

Inhibitory control and set shifting describe different pathways from behavioral inhibition to socially anxious behavior.

Individuals with a behaviorally inhibited (BI) temperament are more likely to develop social anxiety. However, the mechanisms by which socially anxious behavior emerges from BI are unclear. Variation in different forms of top-down control, specifically executive functions (EF), may play distinct roles and characterize differential pathways to social anxiety. Here 291 children were assessed for BI in toddlerhood (ages 2 and 3), parent-reported inhibitory control and set shifting during middle childhood (age 7), and multidimensional assessment of socially anxious behavior completed during late childhood and early adolescence (ages 9 and 12). Structural equation modeling revealed that early variation in BI predicted the development of socially anxious behavior through either higher levels of parent-reported inhibitory control or lower levels of parent-reported set shifting. These data reinforce the notion that top-down control does not uniformly influence relations between temperament and socially anxious behavior. These data suggest novel approaches to thinking about the role of EFs and social anxiety outcomes as children approach adolescence.

Are you as important as me? Self-other discrimination within trait-adjective processing.

Healthy adults typically display enhanced processing for self- (relative to other-) relevant and positive (relative to negative) information. However, it is unclear whether these two biases interact to form a self-positivity bias, whereby self-positive information receives prioritized processing. It is also unclear how a blocked versus mixed referent design impacts reference and valence processing. We addressed these questions using behavioral and electrophysiological indices across two studies using a Self-Referential Encoding Task, followed by surprise recall and recognition tasks. Early (P1) and late (LPP) event-related potentials were time-locked to a series of trait adjectives, encoded relative to oneself or a fictional character, with referent presented in a blocked (Exp. 1) or mixed (Exp. 2) trial design. Regardless of study design, participants recalled and recognized more self- than other-relevant adjectives, and recognized more positive than negative adjectives. Additionally, participants demonstrated larger LPP amplitudes for self-relevant and positive adjectives. The LPP self-relevance effect emerged earlier and persisted longer in the blocked (400-800 ms) versus mixed design (600-800 ms). The LPP valence effect was not apparent in the blocked design, but appeared late in the mixed design (600-1200 ms). Critically, the interaction between self-relevance and valence appeared only behaviorally in the mixed design, suggesting that overall self-relevance and valence independently impact neural socio-cognitive processing.

Attention bias to reward predicts behavioral problems and moderates early risk to externalizing and attention problems.

The current study had three goals. First, we replicated recent evidence that suggests a concurrent relation between attention bias to reward and externalizing and attention problems at age 7. Second, we extended these findings by examining the relations between attention and behavioral measures of early exuberance (3 years), early effortful control (4 years), and concurrent effortful control (7 years), as well as later behavioral problems (9 years). Third, we evaluated the role of attention to reward in the longitudinal pathways between early exuberance and early effortful control to predict externalizing and attention problems. Results revealed that attention bias to reward was associated concurrently and longitudinally with behavioral problems. Moreover, greater reward bias was concurrently associated with lower levels of parent-reported effortful control. Finally, attention bias to reward moderated the longitudinal relations between early risk factors for behavioral problems (gender, exuberance, and effortful control) and later externalizing and attention problems, such that these early risk factors were most predictive of behavioral problems for males with a large attention bias to reward. These findings suggest that attention bias to reward may act as a moderator of early risk, aiding the identification of children at the highest risk for later behavioral problems.

Relations between catechol-O-methyltransferase Val158Met genotype and inhibitory control development in childhood.

The Val158Met rs4680 single-nucleotide polymorphism (SNP) at the catechol-O-methyltransferase (COMT) gene, primarily involved in dopamine breakdown within prefrontal cortex, has shown relations with inhibitory control (IC) in both adults and children. However, little is known about how COMT genotype relates to developmental trajectories of IC throughout childhood. Here, our study explored the effects of the COMT genotype (Val/Val, Val/Met, and Met/Met) on IC trajectories between the ages of 5 and 10 years. Children (n = 222) completed a Go/Nogo task at ages 5, 7, and 10; IC was characterized using signal detection theory to examine IC performance (d') and response strategy (RS) (criterion). COMT genotype was not related to initial levels of IC performance and RS at age 5 or change in RS from ages 5 to 10. In contrast, COMT genotype was related to change in IC performance between 5 and 10 years. While Val/Val children did not differ from Val/Met children in development of IC performance, children with the Met/Met genotype exhibited more rapid development of IC performance when compared with Val/Met peers. These results suggest that COMT genotype modulates the development of IC performance in middle childhood.

Adolescent cognitive control, theta oscillations, and social observation.

Theta oscillations (4-8 Hz) provide an organizing principle of cognitive control, allowing goal-directed behavior. In adults, theta power over medial-frontal cortex (MFC) underlies conflict/error monitoring, whereas theta connectivity between MFC and lateral-frontal regions reflects cognitive control recruitment. However, prior work has not separated theta responses that occur before and immediately after a motor response, nor explained how medial-lateral connectivity drives different kinds of control behaviors. Theta's role during adolescence, a developmental window characterized by a motivation-control mismatch also remains unclear. As social observation is known to influence motivation, this might be a particularly important context for studying adolescent theta dynamics. Here, adolescents performed a flanker task alone or under social observation. Focusing first on the nonsocial context, we parsed cognitive control into dissociable subprocesses, illustrating how theta indexes distinct components of cognitive control working together dynamically to produce goal-directed behavior. We separated theta power immediately before/after motor responses, identifying behavioral links to conflict monitoring and error monitoring, respectively. MFC connectivity was separated before/after responses and behaviorally-linked to reactive and proactive control, respectively. Finally, distinct forms of post-error control were dissociated, based on connectivity with rostral/caudal frontal cortex. Social observation was found to exclusively upregulate theta measures indexing post-response error monitoring and proactive control, as opposed to conflict monitoring and reactive control. Linking adolescent cognitive control to theta oscillations provides a bridge between non-invasive recordings in humans and mechanistic studies of neural oscillations in animal models; links to social observation provide insight into the motivation-control interactions that occur during adolescence.

Development of inhibitory control during childhood and its relations to early temperament and later social anxiety: unique insights provided by latent growth modeling and signal detection theory.

BACKGROUND: Children with the temperament of behavioral inhibition (BI) face increased risk for social anxiety. However, not all children with BI develop anxiety symptoms. Inhibitory control (IC) has been suggested as a moderator of the pathway between BI and social anxiety. This study uses longitudinal data to characterize development of IC and tests the hypothesis that IC moderates associations between early BI and later social anxiety symptoms. METHODS: Children completed a Go/Nogo task at ages 5, 7, and 10 years as part of a longitudinal study of BI (measured at 2-3 years) and social anxiety symptoms (measured at 12 years). To assess IC development, response strategy (criterion) and inhibitory performance (d') were characterized using signal detection theory. Latent growth models were used to characterize the development of IC and examine relations among BI, IC parameters, and social anxiety symptoms. RESULTS: IC response strategy did not change between 5 and 10 years of age, whereas IC performance improved over time. BI scores in toddlerhood predicted neither initial levels (intercept) nor changes (slope) in IC response strategy or IC performance. However, between ages 5 and 10, rate of change in IC performance, but not response strategy, moderated relations between BI and later parent-reported social anxiety symptoms. Specifically, greater age-related improvements in IC performance predicted higher levels of social anxiety in high BI children. CONCLUSIONS: IC development in childhood occurs independent of BI levels. However, rapid increases in IC performance moderate risk for social anxiety symptoms in children with BI. Implications for theory and practice are discussed.

Developmental Relations Among Behavioral Inhibition, Anxiety, and Attention Biases to Threat and Positive Information.

This study examined relations between behavioral inhibition (BI) assessed in toddlerhood (n = 268) and attention biases (AB) to threat and positive faces and maternal-reported anxiety assessed when children were 5- and 7-year-old. Results revealed that BI predicted anxiety at age 7 in children with AB toward threat, away from positive, or with no bias, at age 7; BI did not predict anxiety for children displaying AB away from threat or toward positive. Five-year AB did not moderate the link between BI and 7-year anxiety. No direct association between AB and BI or anxiety was detected; moreover, children did not show stable AB across development. These findings extend our understanding of the developmental links among BI, AB, and anxiety.

Early-Childhood Social Reticence Predicts Brain Function in Preadolescent Youths During Distinct Forms of Peer Evaluation.

Social reticence is expressed as shy, anxiously avoidant behavior in early childhood. With development, overt signs of social reticence may diminish but could still manifest themselves in neural responses to peers. We obtained measures of social reticence across 2 to 7 years of age. At age 11, preadolescents previously characterized as high (n = 30) or low (n = 23) in social reticence completed a novel functional-MRI-based peer-interaction task that quantifies neural responses to the anticipation and receipt of distinct forms of social evaluation. High (but not low) social reticence in early childhood predicted greater activity in dorsal anterior cingulate cortex and left and right insula, brain regions implicated in processing salience and distress, when participants anticipated unpredictable compared with predictable feedback. High social reticence was also associated with negative functional connectivity between insula and ventromedial prefrontal cortex, a region commonly implicated in affect regulation. Finally, among participants with high social reticence, negative evaluation was associated with increased amygdala activity, but only during feedback from unpredictable peers.

Error-monitoring in response to social stimuli in individuals with higher-functioning Autism Spectrum Disorder.

Error-monitoring, or the ability to recognize one's mistakes and implement behavioral changes to prevent further mistakes, may be impaired in individuals with Autism Spectrum Disorder (ASD). Children and adolescents (ages 9-19) with ASD (n = 42) and typical development (n = 42) completed two face processing tasks that required discrimination of either the gender or affect of standardized face stimuli. Post-error slowing and the difference in Error-Related Negativity amplitude between correct and incorrect responses (ERNdiff ) were used to index error-monitoring ability. Overall, ERNdiff increased with age. On the Gender Task, individuals with ASD had a smaller ERNdiff than individuals with typical development; however, on the Affect Task, there were no significant diagnostic group differences on ERNdiff . Individuals with ASD may have ERN amplitudes similar to those observed in individuals with typical development in more social contexts compared to less social contexts due to greater consequences for errors, more effortful processing, and/or reduced processing efficiency in these contexts. Across all participants, more post-error slowing on the Affect Task was associated with better social cognitive skills.

Early Behavioral Inhibition and Emotion Regulation: Pathways Toward Social Competence in Middle Childhood.

This study examined emotion regulation (ER) as a mediator in the relation between early behavioral inhibition (BI) and later social competence (N = 257), and whether this mediation varied depending on BI levels. Maternal report and observational measures were used to assess BI (ages 2 and 3). Children's ER strategies (age 5) and social competence with an unfamiliar peer (age 7) were measured using observational measures. Results showed that BI predicted less engaged ER strategies during a disappointment task, and engaged ER predicted higher social competence. Engaged ER mediated the effect of BI on social competence, but only for highly inhibited children. Findings elucidate developmental trajectories of risk and resilience, and suggest targeting regulatory strategies in early prevention efforts with highly inhibited children.

Infant attachment security and early childhood behavioral inhibition interact to predict adolescent social anxiety symptoms.

Insecure attachment and behavioral inhibition (BI) increase risk for internalizing problems, but few longitudinal studies have examined their interaction in predicting adolescent anxiety. This study included 165 adolescents (ages 14-17 years) selected based on their reactivity to novelty at 4 months. Infant attachment was assessed with the Strange Situation. Multimethod BI assessments were conducted across childhood. Adolescents and their parents independently reported on anxiety. The interaction of attachment and BI significantly predicted adolescent anxiety symptoms, such that BI and anxiety were only associated among adolescents with histories of insecure attachment. Exploratory analyses revealed that this effect was driven by insecure-resistant attachment and that the association between BI and social anxiety was significant only for insecure males. Clinical implications are discussed.

Emergent patterns of risk for psychopathology: The influence of infant avoidance and maternal caregiving on trajectories of social reticence.

The current study investigated the influential role of infant avoidance on links between maternal caregiving behavior and trajectories at risk for psychopathology. A sample of 153 children, selected for temperamental reactivity to novelty, was followed from infancy through early childhood. At 9 months, infant avoidance of fear-eliciting stimuli in the laboratory and maternal sensitivity at home were assessed. At 36 months, maternal gentle discipline was assessed at home. Children were repeatedly observed in the lab with an unfamiliar peer across early childhood. A latent class growth analysis yielded three longitudinal risk trajectories of social reticence behavior: a high-stable trajectory, a high-decreasing trajectory, and a low-increasing trajectory. For infants displaying greater avoidance, 9-month maternal sensitivity and 36-month maternal gentle discipline were both positively associated with membership in the high-stable social reticence trajectory, compared to the high-decreasing social reticence trajectory. For infants displaying lower avoidance, maternal sensitivity was positively associated with membership in the high-decreasing social reticence trajectory, compared to the low-increasing trajectory. Maternal sensitivity was positively associated with the high-stable social reticence trajectory when maternal gentle discipline was lower. These results illustrate the complex interplay of infant and maternal behavior in early childhood trajectories at risk for emerging psychopathology.

Cognitive control moderates early childhood temperament in predicting social behavior in 7-year-old children: an ERP study.

Behavioral inhibition (BI) is a temperament associated with heightened vigilance and fear of novelty in early childhood, and social reticence and increased risk for anxiety problems later in development. However, not all behaviorally inhibited children develop signs of anxiety. One mechanism that might contribute to the variability in developmental trajectories is the recruitment of cognitive-control resources. The current study measured N2 activation, an ERP (event-related potential) associated with cognitive control, and modeled source-space activation (LORETA; Low Resolution Brain Electromagnetic Tomography) at 7 years of age while children performed a go/no-go task. Activation was estimated for the entire cortex and then exported for four regions of interest: ventromedial prefrontal cortex (VMPFC), ventrolateral prefrontal cortex (VLPFC), dorsal anterior cingulate cortex (dorsal ACC), and dorsal lateral prefrontal cortex (DLPFC). BI was measured in early childhood (ages 2 and 3 years). Anxiety problems and social reticence were measured at 7 years of age to ascertain stability of temperamental style. Results revealed that BI was associated with increased performance accuracy, longer reaction times, greater (more negative) N2 activation, and higher estimated dorsal ACC and DLPFC activation. Furthermore, early BI was only associated with social reticence at age 7 at higher (more negative) levels of N2 activation or higher estimated dorsal ACC or DLPFC activation. Results are discussed in the context of overcontrolled behavior contributing to social reticence and signs of anxiety in middle childhood.

Cognitive conflict links behavioral inhibition and social problem solving during social exclusion in childhood.

Behavioral inhibition (BI) is a temperament characterized by heightened negative affect and social reticence to unfamiliar peers. In a longitudinal study, 291 infants were assessed for BI at 24 and 36 months of age. At age 7, N2 amplitude was measured during a Flanker task. Also at age 7, children experienced social exclusion in the lab during an interaction with an unfamiliar peer and an experimenter. Our findings indicate that children characterized as high in BI, relative to those low in BI, had larger (i.e., more negative) N2 amplitudes. Additionally, among children with a large N2, BI was positively related to withdrawal and negatively related to assertiveness during social exclusion. These findings suggest that variations in conflict detection among behaviorally inhibited children plays a role in their social behavior during stressful social situations.