Differential amygdala responses to happy and fearful facial expressions depend on selective attention

Facial expressions of emotion elicit increased activity in the human amygdala. Such increases are particularly evident for expressions that convey potential threat to the observer, and arise even when the face is masked from awareness. We used functional magnetic resonance imaging (fMRI) to examine whether the amygdala responds differentially to threatening (fearful) versus nonthreatening (happy) facial expressions depending on whether the face is attended or actively ignored. In separate runs, participants were cued to attend to a face or a house within semitransparent, spatially overlaid composite pairs, presented either side of fixation, and were required to perform a demanding same/different judgment. We found significant attentional modulation of activity in category-specific 'face' (fusiform gyrus) and 'place' (parahippocampal gyrus) regions, with activity in each area increasing selectively when its preferred stimulus was attended versus ignored. In contrast, activity in the amygdala differed according to the valence of the facial expression and the category of the attended stimulus. For happy faces, activity in the amygdala was greater in the attend-face than in the attend-house condition, whereas for fearful faces, activity was greater in the attend-house than in the attend-face condition. We conclude that differential amygdala responses to fearful versus happy facial expressions are tuned by mechanisms of attention and that the amygdala gives preference to potentially threatening stimuli under conditions of inattention.