Patterns of Neural Connectivity During an Attention Bias Task Moderate Associations Between Early Childhood Temperament and Internalizing Symptoms in Young Adulthood

Abstract

Background Biased attention to threat is found in both individuals with anxiety symptoms and children with the childhood temperament of behavioral inhibition (BI). Although perturbed fronto-amygdala function is implicated in biased attention among anxious individuals, no work has examined the neural correlates of attention biases in BI. Work in this area may clarify underlying mechanisms for anxiety in a sample at risk for internalizing disorders. We examined the relations among early childhood BI, fronto-amygdala connectivity during an attention bias task in young adulthood, and internalizing symptoms, assessed in young adulthood. Methods Children were assessed for BI at multiple age points from infancy through age seven. Based on a composite of observational and maternal report data, we selected 21 young adults classified as having a history of BI and 23 classified as non-BI for this study (N=44). Participants completed an event-related fMRI attention-bias task involving threat (angry faces) and neutral trials. Internalizing symptoms were assessed by self-report and diagnostic interviews. Results The young adults characterized in childhood with BI exhibited greater strength in threat-related connectivity than non-behaviorally inhibited young adults. Between-group differences manifested in connections between the amygdala and two frontal regions: dorsolateral prefrontal cortex and anterior insula. Amygdala-insula connectivity also interacted with childhood BI to predict young adult internalizing symptoms. Conclusions BI during early childhood predicts differences as young adults in threat and attention-related fronto-amygdala connectivity. Connectivity strength, in turn, moderated the relations between early BI and later psychopathology.

Behavioral Inhibition and Developmental Risk: A Dual-Processing Perspective

“…This includes motor response patterns, markers of activity in the autonomic nervous system (ie, heart rate and vagal tone; Kagan et al, 1987), cortical activity patterns (Calkins et al, 1996;McManis et al, 2002), and neuroendocrine profiles (ie, cortisol; Kagan et al, 1988;Schmidt et al, 1997). Recent advances in neuroscience have allowed this original amygdala-based model to be expanded to include broader perturbations in a distributed neural circuit, encompassing components of the PFC and striatum (Bar-Haim et al, 2009;Bishop et al, 2004;Guyer et al, 2006;Hardee et al, 2013;Helfinstein et al, 2012). Common across these diverse models is an emphasis on the relations between BI and hypersensitivity in neural circuitry rapidly engaged by automatic modes of processing and a resulting behavioral sensitivity to motivationally salient cues.…”

“…This interaction of BI and emotion condition only held under relatively short stimulus presentation conditions suggesting that BI is specifically associated with early, automatic, and reactive attention biases. Similarly, using a subsample of these participants in early adulthood, Hardee et al (2013) used the dot-probe task to link BI to fronto-amygdala connectivity. In this study, fronto-amygdala connectivity was more variable in BI than non-BI subjects, when contrasted across threat and no-threat events appearing in the dot-probe task.…”

“…In a second study, Perez-Edgar et al (2010a) found a similar association in which early BI predicted social withdrawal in adolescence but only for those who also showed an attention bias to threat in adolescence. In the third study, Hardee et al (2013) used fMRI with the dotprobe task in the same cohort studied by Perez-Edgar et al (2010a) but when they were young adults. This latter study found that patterns of amygdala-prefrontal connectivity moderated the relation between childhood BI and internalizing symptoms in young adulthood.…”

Processing of different types of social threat in shyness: Preliminary findings of distinct functional neural connectivity

“…Converging evidence from a series of neuroimaging, electrocortical, and behavioral studies in shy adults and children suggest that temperamental shyness is associated with affect-related attentional biases to potential threat. For example, fMRI studies in shy and behaviorally inhibited adults using socially threatening stimuli that are theoretically immediately threatening, including unfamiliar and angry faces, have found greater amygdala activation (Schwartz, Wright, Shin, Kagan, & Rauch, 2003) and shorter response latencies (Beaton et al, 2008); differential amygdalar connectivity (Hardee et al, 2013); as well as differential patterns of neural activation as a function of morning cortisol changes among shy-sociable [e.g., rostal anterior cingulate cortex (ACC)] and shy-unsociable adults (e.g., amygdala, insula, posterior ACC) (Tang, Beaton, Schulkin, Hall, & Schmidt, 2014).…”

Social anxiety disorder in adolescence: How developmental cognitive neuroscience findings may shape understanding and interventions for psychopathology

“…FMRI studies that have included behaviorally inhibited youth find similar fronto-limbic perturbations as those described in youth with SAD. Notably, studies with adolescents with BI have reported increased responses in the amygdalae to negative emotional expressions, differential striatal responses to the anticipation of monetary and social rewards, and during conflict adaptation (when individuals habituate to successively presented contradictory emotional information) ( Bar-Haim et al, 2009;Guyer et al, 2014;Hardee et al, 2013;Helfinstein et al, 2011;Jarcho et al, 2013aJarcho et al, ,b, 2014Pérez-edgar et al, 2007).…”