Unattended emotional faces elicit early lateralized amygdala-frontal and fusiform activations

Human adaptive behaviour to potential threats involves specialized brain responses allowing rapid and reflexive processing of the sensory input and a more directed processing for later evaluation of the nature of the threat. The amygdalae are known to play a key role in emotion processing. It is suggested that the amygdalae process threat-related information through a fast subcortical route and slower cortical feedback. Evidence from human data supporting this hypothesis is lacking. The present study investigated event-related neural responses during processing of facial emotions in the unattended hemifield using magnetoencephalography (MEG) and found activations of the amygdala and anterior cingulate cortex to fear as early as 100 ms. The right amygdala exhibited temporally dissociated activations to input from different visual fields, suggesting early subcortical versus later cortical processing of fear. We also observed asymmetrical fusiform activity related to lateralized feed-forward processing of the faces in the visual-ventral stream. Results demonstrate fast, automatic, and parallel processing of unattended emotional faces, providing important insights into the specific and dissociated neural pathways in emotion and face perception.