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The Journal of Neuroscience, July 2, 2003, 23(13):5627-5633

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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 ¹Psychology, ²Psychiatry, and ³Neuroscience, Stanford University, Stanford, California 94305

The present study examined whether automaticity, defined here as independence from attentional modulation, is a fundamental principle 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 fundamental 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

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Received Jan. 28, 2003; revised Apr. 15, 2003; accepted Apr. 17, 2003.

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