A collicular-hypothalamic pathway for social visual awareness

Awareness of other individuals is a foundational element of social behavior. Here we examined how specific neural systems detect and signal the visual presence of conspecifics related to social arousal and motivation. We found that visual exposure to videos of other mice can activate hypothalamic oxytocin neurons and promote onset of pup retrieval behavior in naive virgin female mice. A range of social videos depicting conspecifics in diverse contexts, including but not limited to parental behavior, could accelerate onset of pup retrieval compared to non-social controls. Animals would elect to watch social videos over non-social videos. We made photo-tagged recordings from oxytocin neurons of the paraventricular nucleus (PVN), which were preferentially activated during social video viewing. Optogenetic silencing of PVN oxytocin neurons during exposure prevented this behavioral enhancement of pup retrieval onset. We also made photo-tagged recordings from a population of PVN-projecting neurons of the superficial superior colliculus (sSC→PVN units). Compared to other sSC neurons, the sSC→PVN neurons had specialized horizontal direction tuning with robust and sustained responses to social videos. sSC→PVN neurons differentiated visual scenes based on social content, responding most strongly to pup retrieval and less to scenes with increasing numbers of animals. Our results identify a subcortical visual pathway that signals the presence and salience of conspecifics to the oxytocin system, providing a circuit mechanism by which social visual awareness drives neuroendocrine arousal and the acquisition of parental behavior.