Frontolimbic functioning during threat-related attention: Relations to early behavioral inhibition and anxiety in children

Abstract

Children with behavioral inhibition (BI), a temperament characterized by biologically-based hyper-vigilance to novelty, display threat-related attention biases (AB) that shape developmental trajectories of risk for anxiety. Here we explore the relations between BI, neural function, and anxiety. Fifty-six 9–12-year-olds (23 behaviorally inhibited) performed the dot-probe task while undergoing fMRI. AB scores were not associated with BI group or parent-rated anxiety symptoms. Trials requiring attention orienting away from threat engaged an executive and threat-attention network (dlPFC, vlPFC, mPFC, and amygdala). Within that network, behaviorally inhibited children showed greater activation in the right dlPFC. Heightened dlPFC activation related to increased anxiety, and BI levels accounted for the direct relation between dlPFC activation and anxiety. Behaviorally inhibited children may engage the executive attention system during threat-related processing as a compensatory mechanism. We provide preliminary evidence that the link between PFC functioning and anxiety might be attributed to early-emerging temperamental vulnerabilities present before the emergence of clinical anxiety.

Altered Prefrontal Cortex Function Marks Heightened Anxiety Risk in Children

“…24,65 However, amygdala hyperactivity was observed in inhibited children using an executive-attention task. 26 Studies that include multiple different tasks will be instrumental in elucidating task effects. A second possibility is that amygdala hyperactivity is specific to anxiety 62 and is not a neural correlate of anxiety risk.…”

“…Advertisements were for children who were “quiet,” “cautious,” “shy,” “outgoing,” and general recruitment for a study on “temperament and brain function.” Prior to the first study visit, parents completed a brief online screening, including the Behavioral Inhibition Questionnaire-Parent (BIQ-P), 37 a validated measure of childhood inhibited temperament, which has been used for screening in a recent neuroimaging study 26 and shows convergent validity with behavioral measures and other measures of social inhibition. 37–39 Although four questions in the questionnaire refer to younger age groups, these questions were highly correlated with other items in the scale and therefore were retained as written.…”

“…Children were selected based on a temperament score ± one standard deviation from the mean based on published norms (inhibited > 123; uninhibited < 59); 37 these norms were similar to those identified in children ages 4–15 39 and those used in a recent similar neuroimaging study. 26 …”

“…22,23 Inhibited adolescents and young adults show both increased and decreased prefrontal cortex (PFC) function across studies: decreased dorsal anterior cingulate cortex (dACC) and dorsolateral PFC (dlPFC) activation when viewing expected negative social stimuli; 22 increased rostral ACC (rACC) and dACC activation when anticipating fear faces; 24 and increased dorsomedial PFC, dlPFC, and rACC activity when performing a task that requires cognitive control. 25,26 A recent study in inhibited children found heightened dlPFC response during a threat executive-attention task. 26 Studies examining risk versus resilience in inhibited temperament have highlighted that greater PFC activity during emotional tasks that require cognitive control predicts resilience to anxiety disorders, suggesting that lack of PFC activity may be associated with anxiety risk.…”

“…25,26 A recent study in inhibited children found heightened dlPFC response during a threat executive-attention task. 26 Studies examining risk versus resilience in inhibited temperament have highlighted that greater PFC activity during emotional tasks that require cognitive control predicts resilience to anxiety disorders, suggesting that lack of PFC activity may be associated with anxiety risk. 16,24,27 During non-emotional tasks, over-control has also been associated with anxiety risk.…”