Facial-Expression and Gaze-Selective Responses in the Monkey Amygdala

The social behavior of both human and nonhuman primates relies on specializations for the recognition of individuals, their facial expressions, and their direction of gaze. A broad network of cortical and subcortical structures has been implicated in face processing, yet it is unclear whether co-occurring dimensions of face stimuli, such as expression and direction of gaze, are processed jointly or independently by anatomically and functionally segregated neural structures. Awake macaques were presented with a set of monkey faces displaying aggressive, neutral, and appeasing expressions with head and eyes either averted or directed. BOLD responses to these faces as compared to Fourier-phase-scrambled images revealed widespread activation of the superior temporal sulcus and inferotemporal cortex and included activity in the amygdala. The different dimensions of the face stimuli elicited distinct activation patterns among the amygdaloid nuclei. The basolateral amygdala, including the lateral, basal, and accessory basal nuclei, produced a stronger response for threatening than appeasing expressions. The central nucleus and bed nucleus of the stria terminalis responded more to averted than directed-gaze faces. Independent behavioral measures confirmed that faces with averted gaze were more arousing, suggesting the activity in the central nucleus may be related to attention and arousal.