Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys

Significance The primate brain is specialized for social interaction, and a complex network of brain regions supports this important function. Face perception is central to social development, and both humans and nonhuman primates exhibit a spontaneous viewing preference for faces. This shared involuntary response underscores the importance of faces in the earliest stages of cognitive development, yet its neural basis is not well understood. Here we report that bilateral amygdala lesions in rhesus monkeys eliminate the robust viewing preference for both real faces and illusory faces. This demonstrates a fundamental role for the amygdala in guiding eye movements toward face stimuli, a critical behavior for normal social development and social interaction. In free-viewing experiments, primates orient preferentially toward faces and face-like stimuli. To investigate the neural basis of this behavior, we measured the spontaneous viewing preferences of monkeys with selective bilateral amygdala lesions. The results revealed that when faces and nonface objects were presented simultaneously, monkeys with amygdala lesions had no viewing preference for either conspecific faces or illusory facial features in everyday objects. Instead of directing eye movements toward socially relevant features in natural images, we found that, after amygdala loss, monkeys are biased toward features with increased low-level salience. We conclude that the amygdala has a role in our earliest specialized response to faces, a behavior thought to be a precursor for efficient social communication and essential for the development of face-selective cortex.