A Neurobehavioral Mechanism Linking Behaviorally Inhibited Temperament and Later Adolescent Social Anxiety

Abstract

Objective Behavioral inhibition (BI) is a temperament identified in early childhood that is a risk factor for later social anxiety. However, mechanisms underlying development of social anxiety remain unclear. To better understand the emergence of social anxiety, longitudinal studies investigating changes at both behavioral neural levels are needed. Method BI was assessed in the laboratory at ages 2 and 3 (N = 268). Children returned at age 12, and electroencephalography (EEG) was recorded while performing a flanker task under two conditions: once while believing they were being observed by peers, and once while not being observed. This methodology isolated changes in error monitoring (error-related negativity; ERN) and behavior (post-error reaction time [RT] slowing) as a function of social context. At age 12, current social anxiety symptoms and lifetime diagnoses of social anxiety were obtained. Results Childhood BI prospectively predicted social-specific ERN increases and social anxiety symptoms in adolescence; these symptoms directly related to clinical diagnoses. Serial mediation analysis revealed social ERN changes explained relations between BI and both social anxiety symptoms (n = 107) and diagnosis (n = 92), but only insofar as social context also led to increased post-error RT slowing (a measure of error preoccupation); this model was not significantly related to generalized anxiety. Conclusion Results extend prior work on socially-induced changes in error monitoring and error preoccupation. These measures may index a neurobehavioral mechanism linking behavioral inhibition to adolescent social anxiety symptoms and diagnosis. This mechanism may relate more strongly to social than generalized anxiety in the peri-adolescent period.

Social influences of error monitoring in adolescent girls

“…Similarly, we observed a larger ERN in social contexts as compared to nonsocial contexts among younger adolescents. These findings are in agreement with previous research that has found enhancements of the ERN in motivationally significant contexts (Boksem, Tops et al, 2006;Buzzell, Troller-Renfree et al, 2017;Hajcak et al, 2005;Kim et al, 2005;Potts, 2011;Van Meel & Van Heijningen, 2010). In addition, our findings confirm previous work that the ERN is also sensitive to social factors (Barker et al, 2015;Buzzell, Troller-Renfree et al, 2017;Kim et al, 2005), likely reflecting increased motivation (Blascovich et al, 1999;Blascovich & Tomaka, 1996).…”

“…Although there is strong evidence that the ERN is sensitive to social factors in adults, little research has examined whether the ERN is also influenced by social contexts in adolescence, a developmental period characterized by heightened social motivation and social evaluation (Crone & Dahl, 2012). We recently found that the ERN was enhanced during social contexts as compared to nonsocial contexts in middle adolescence (Buzzell, Troller-Renfree et al, 2017). However, the age range of the sample was relatively restricted, limiting the ability to examine whether the degree of ERN enhancement in social contexts changes across adolescence.…”

“…In line with biopsychosocial theories of social motivation, the ERN is enhanced by social observation and evaluation (Barker, Troller‐Renfree, Pine, & Fox, ; Hajcak et al, ; Masaki, Maruo, Meyer, & Hajcak, ; Schillinger, Smedt, & Grabner, ; Van Meel & Van Heijningen, ). In children and adolescents, social factors enhance the ERN (Buzzell, Troller‐Renfree et al, ; Kim, Iwaki, Uno, & Fujita, ), whereas nonsocial factors (i.e., monetary rewards) appear to not influence the ERN (Maruo, Sommer, & Masaki, ; Torpey, Hajcak, & Klein, ). However, children with attention deficit hyperactivity disorder (ADHD), a disorder in part characterized by altered motivational systems (Haenlein & Caul, ; Sergeant, ; Tripp & Wickens, ), display an increased ERN only when performance is extrinsically rewarded (Groom et al, ), suggesting the importance of within‐individual valuation of context in influencing ERN magnitude in development.…”

“…We hypothesized that a social context, relative to nonsocial context, would increase the ERN in adolescent girls based on previous findings in adult and developmental populations (Barker et al, ; Buzzell, Troller‐Renfree et al, ; Hajcak et al, ; Kim et al, ). In addition, we hypothesized that age would moderate the degree to which the ERN was enhanced in social contexts, based on theoretical models of social motivation in adolescence (Casey et al, ; Ernst et al, ; Shulman et al, ).…”

Advancing clinical neuroscience through enhanced tools: Pediatric social anxiety as an example

“…between anxiety symptoms and the number of errors in the peer condition, it is not uncommon that tasks, and specifically the Flanker task, fail to elicit proposed behavioral differences (Barker et al, 2015;Buzzell et al, 2017). Because this study contains a small number of participants, we anticipate that anxiety-related differences will emerge in a larger sample.…”