Fear, faces, and the human amygdala

Abstract

The amygdala's historical role in processing stimuli related to threat and fear is being modified to suggest a role that is broader and more abstract. Amygdala lesions impair the ability to seek out and make use of the eye region of faces, resulting in impaired fear perception. Other studies in rats and humans revive earlier proposals that the amygdala is important not only for fear perception as such, but also for detecting saliency and biological relevance. Debates about some features of this processing now suggest that while the amygdala can process fearful facial expressions in the absence of conscious perception, and while there is some degree of preattentive processing, this depends on the context and is not necessarily more rapid than cortical processing routes. A large current research effort extends the amygdala's putative role to a number of psychiatric illnesses.

Figure 1

Rapid responses to eyes drive fear discrimination. ERPs recorded from right and left (dashed lines) occipitotemporal electrodes are plotted versus time (in ms) relative to the onset of sparsely revealed faces. The peak of this ERP response, corresponding to the classic “N170” is denoted by the blue boxes. Classification images derived by regressing the magnitude of the ERP response (in 4 ms time epochs) onto the randomly sampled location of facial features shown in the sparse stimuli are shown at the bottom. The ERP magnitude is shown by the blue curves; the overall sensitivity of the ERP to facial information is denoted by the red curves. Modified from [45••]; courtesy of Philippe Schyns.

Figure 2

Bilateral amygdala lesions impair the use of the eyes and gaze to the eyes during emotion judgment. Data are from patient SM, who has complete bilateral amygdala lesions and is impaired in recognizing fear [2]. Using sparsely revealed faces to identify face areas used during emotion judgment, patient SM (brain shown in c) differed from controls such that controls exhibited much greater use of the eyes than SM, while SM did not rely more on any area of the face than did controls (a). While looking at whole faces, SM exhibited abnormal face gaze (b), making far fewer fixations to the eyes than did controls. When SM was instructed to look at the eyes (d, “SM eyes”) in a whole face, she could do this, resulting in a remarkable recovery in ability to recognize the facial expression of fear compared to her accuracy prior to this instruction (d, “SM free”). Modified from [54].