Perception of dynamic facial expressions activates a cortico-subcortico-cerebellar network in marmosets

Abstract

The perception and identification of faces and facial emotional expressions are critical for social communication in the daily life of all primates. Here, we investigated the neural network activated by dynamic facial expressions in awake New World common marmosets with ultra-high field fMRI at 9.4T. Our results show that dynamic facial expressions activate several areas along the occipitotemporal axis (V2/V3, V4/TEO, FST, caudal TE, rostral TE, TPO), frontal cortex (areas 45/47, 13, 8a and orbital cortex), amygdala, motion-sensitive areas, premotor area, and in the posterior lobe of the cerebellum. Negative faces increased the monkeys respiration rates and elicited stronger responses along the occipitotemporal cortical axis, in the amygdala and in the hypothalamus. This cortico-subcortico-cerebellar network may play an important role in the perception of behaviorally relevant facial expressions that are vital for social communication in marmosets. Significance StatementRecent research has highlighted the importance of emotional content of faces in social communication in humans and non-human primates. The current study focuses on the neural responses to dynamic emotional facial expressions in the common marmoset (Callithrix jacchus), a New World primate species sharing several similarities of social behavior with humans. Using ultra-high-field fMRI, we show that negative facial expressions activate a cortico-subcortico-cerebellar network and, critically, negative faces increase the level of arousal of marmosets, possibly relayed through a modulation of the activity in the autonomic nervous system via stress-integrative brain centres in the hypothalamus. Our results reveal the existence of specific neural and physiological responses to negative emotional faces suggesting that behaviorally relevant facial expressions are vital for social communication in New World marmosets.