Social and asocial prefrontal cortex neurons: a new look at social facilitation and the social brain

A fundamental aspect of behavior in many animal species is 'social facilitation', the positive effect of the mere presence of conspecifics on performance. To date, the neuronal counterpart of this ubiquitous phenomenon is unknown. We recorded the activity of single neurons from two prefrontal cortex regions, the dorsolateral part and the anterior cingulate cortex in monkeys as they performed a visuomotor task, either in the presence of a conspecific (Presence condition) or alone. Monkeys performed better in the presence condition than alone (social facilitation), and analyses of outcome-related activity of 342 prefrontal neurons revealed that most of them (86%) were sensitive to the performance context. Two populations of neurons were discovered: 'social neurons', preferentially active under social presence and 'asocial neurons', preferentially active under social isolation. The activity of these neurons correlated positively with performance only in their preferred context (social neurons under social presence; asocial neurons under social isolation), thereby providing a potential neuronal mechanism of social facilitation. More generally, the fact that identical tasks recruited either social or asocial neurons depending on the presence or absence of a conspecific also brings a new look at the social brain hypothesis.