anderson, et al - j of neurosci, 2003 - neural correlates of threat facial signals

Anderson, et al - j of neurosci, 2003 - neural correlates of threat facial signals

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Behavioral/Systems/Cognitive Neural Correlates of the Automatic Processing of Threat Facial Signals Adam K. Anderson, 1 Kalina Christoff, 1 David Panitz, 1 Eve De Rosa, 2 and John D. E. Gabrieli 1,3 Departments of 1 Psychology, 2 Psychiatry, and 3 Neuroscience, Stanford University, Stanford, California 94305 The present study examined whether automaticity, defined here as independence from attentional modulation, is a fundamental prin- ciple of the neural systems specialized for processing social signals of environmental threat. Attention was focused on either scenes or faces presented in a single overlapping display. Facial expressions were neutral, fearful, or disgusted. Amygdala responses to facial expressions of fear, a signifier of potential physical attack, were not reduced with reduced attention to faces. In contrast, anterior insular responses to facial expressions of disgust, a signifier of potential physical contamination, were reduced with reduced attention. However, reduced attention enhanced the amygdala response to disgust expressions; this enhanced amygdala response to disgust correlated with the magnitude of attentional reduction in the anterior insular response to disgust. These results suggest that automaticity is not funda- mental to the processing of all facial signals of threat, but is unique to amygdala processing of fear. Furthermore, amygdala processing of fear was not entirely automatic, coming at the expense of specificity of response. Amygdala processing is thus specific to fear only during attended processing, when cortical processing is undiminished, and more broadly tuned to threat during unattended processing, when cortical processing is diminished. Key words: amygdala; insula; fear; disgust; attention; emotion; faces; fMRI Introduction Facial expressions serve as important social signals of imminent environmental conditions. It is now known that distinct expres- sions signaling environmental threat draw on distinct neural sub- strates specialized for their evaluation. Patient and neuroimaging studies suggest that the amygdala is critical for evaluating fearful facial expressions (Adolphs et al., 1994; Breiter et al., 1996; Morris et al., 1996; Whalen et al., 1998). Similar evidence indicates that the anterior insula, a region of primary gustatory cortex substan- tially connected with the amygdala (Mesulam and Mufson, 1982), is specialized for evaluating facial expressions of disgust (Phillips et al., 1997, 1998; Calder et al., 2000). The evidence that expressions of fear, a form of threat related to physical attack (Gray, 1987), and expressions of disgust, a form of threat related to physical contamination and disease (Rozin and Fallon, 1987), draw on specialized brain substrates is one measure of the special informational status the human brain places on social signals of potential environmental threats. Another measure of the special status of social signals of threat is the proposal that their process- ing occurs automatically, proceeding largely independently of
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Anderson, et al - j of neurosci, 2003 - neural correlates of threat facial signals

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