Amygdala Activation Predicts Gaze toward Fearful Eyes

Abstract

The human amygdala can be robustly activated by presenting fearful faces, and it has been speculated that this activation has functional relevance for redirecting the gaze toward the eye region. To clarify this relationship between amygdala activation and gaze-orienting behavior, functional magnetic resonance imaging data and eye movements were simultaneously acquired in the current study during the evaluation of facial expressions. Fearful, angry, happy, and neutral faces were briefly presented to healthy volunteers in an event-related manner. We controlled for the initial fixation by unpredictably shifting the faces downward or upward on each trial, such that the eyes or the mouth were presented at fixation. Across emotional expressions, participants showed a bias to shift their gaze toward the eyes, but the magnitude of this effect followed the distribution of diagnostically relevant regions in the face. Amygdala activity was specifically enhanced for fearful faces with the mouth aligned to fixation, and this differential activation predicted gazing behavior preferentially targeting the eye region. These results reveal a direct role of the amygdala in reflexive gaze initiation toward fearfully widened eyes. They mirror deficits observed in patients with amygdala lesions and open a window for future studies on patients with autism spectrum disorder, in which deficits in emotion recognition, probably related to atypical gaze patterns and abnormal amygdala activation, have been observed.