Neurons in the Monkey Amygdala Detect Eye Contact during Naturalistic Social Interactions

Primates explore the visual world through eye-movement sequences. Saccades bring details of interest into the fovea, while fixations stabilize the image. During natural vision, social primates direct their gaze at the eyes of others to communicate their own emotions and intentions and to gather information about the mental states of others. Direct gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status. Despite the great importance of making and breaking eye contact in the behavioral repertoire of primates, little is known about the neural substrates that support these behaviors. Here we show that the monkey amygdala contains neurons that respond selectively to fixations on the eyes of others and to eye contact. These "eye cells" share several features with the canonical, visually responsive neurons in the monkey amygdala; however, they respond to the eyes only when they fall within the fovea of the viewer, either as a result of a deliberate saccade or as eyes move into the fovea of the viewer during a fixation intended to explore a different feature. The presence of eyes in peripheral vision fails to activate the eye cells. These findings link the primate amygdala to eye movements involved in the exploration and selection of details in visual scenes that contain socially and emotionally salient features.