Abstract

Behavioral evidence indicates that angry faces are seen as more threatening, and elicit greater anxiety, when directed at the observer, whereas the influence of gaze on the processing of fearful faces is less consistent. Recent research has also found inconsistent effects of expression and gaze direction on the amygdala response to facial signals of threat. However, such studies have failed to consider the important influence of anxiety on the response to signals of threat; an influence that is well established in behavioral research and recent neuroimaging studies. Here, we investigated the way in which individual differences in anxiety would influence the interactive effect of gaze and expression on the response to angry and fearful faces in the human extended amygdala. Participants viewed images of fearful, angry and neutral faces, either displaying an averted or direct gaze. We found that state anxiety predicted an increased response in the dorsal amygdala/substantia innominata (SI) to angry faces when gazing at, relative to away from the observer. By contrast, high state anxious individuals showed an increased amygdala response to fearful faces that was less dependent on gaze. In addition, the relationship between state anxiety and gaze on emotional intensity ratings mirrored the relationship between anxiety and the amygdala/SI response. These results have implications for understanding the functional role of the amygdala and extended amygdala in processing signals of threat, and are consistent with the proposed role of this region in coding the relevance or significance of a stimulus to the observer.

Highlights

  • Facial expressions of both anger and fear represent potent signals of threat

  • Rating experiment First, we investigated the effect of gaze on the perceived intensity of emotional expression as measured in the rating task completed outside the magnet

  • Our results demonstrate that the response in the extended amygdala to facial signals of anger and fear is differentially modulated by changes in gaze direction and individual levels of anxiety

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Summary

Introduction

Facial expressions of both anger and fear represent potent signals of threat. Across various species, angry expressions are commonly used in face-to-face encounters in order to control or change the behavior of others via the assertion of authority; as when warding off competitors for valued assets, such as food, resources, social status or territory (Averill, 1982; Blanchard and Blanchard, 2003). Numerous behavioral studies suggest that perception of anger in faces is enhanced when their gaze is directed at the observer (Adams and Kleck, 2005; Graham and LaBar, 2007; Sander et al, 2007; Bindemann et al, 2008). Some behavioral studies indicate that the processing of fearful faces is enhanced by averted relative to direct gaze (Adams and Kleck, 2005; Sander et al, 2007), while others have found mixed effects (Graham and LaBar, 2007; Hess et al, 2007; Bindemann et al, 2008)

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