Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations

Abstract

Debate continues as to the automaticity of the amygdala's response to threat. Accounts taking a strong automaticity line suggest that the amygdala's response to threat is both involuntary and independent of attentional resources. Building on these accounts, prominent models have suggested that anxiety modulates the output of an amygdala-based preattentive threat evaluation system. Here, we argue for a modification of these models. Functional magnetic resonance imaging data were collected while volunteers performed a letter search task of high or low perceptual load superimposed on fearful or neutral face distractors. Neither high- nor low-anxious volunteers showed an increased amygdala response to threat distractors under high perceptual load, contrary to a strong automaticity account of amygdala function. Under low perceptual load, elevated state anxiety was associated with a heightened response to threat distractors in the amygdala and superior temporal sulcus, whereas individuals high in trait anxiety showed a reduced prefrontal response to these stimuli, consistent with weakened recruitment of control mechanisms used to prevent the further processing of salient distractors. These findings suggest that anxiety modulates processing subsequent to competition for perceptual processing resources, with state and trait anxiety having distinguishable influences upon the neural mechanisms underlying threat evaluation and "top-down" control.