Conserved evolutionary history for quick detection of threatening faces

Abstract

Humans quickly recognize threats such as snakes and threatening faces, suggesting that human ancestors evolved specialized visual systems to detect biologically relevant threat stimuli. Although non-human primates also detect snakes quickly, it is unclear whether primates share the efficient visual systems to process the threatening faces of their conspecifics. Primates may not necessarily process conspecific threats by facial expressions, because threats from conspecifics in natural situations are often accompanied by other cues such as threatening actions (or attacks) and vocal calls. Here, we show a similar threat superiority effect in both humans and macaque Japanese monkeys. In visual search tasks, monkeys and humans both responded to pictures of a threatening face of an unfamiliar adult male monkey among neutral faces faster than to pictures of a neutral face among threatening faces. However, the monkeys’ response times to detect deviant pictures of a non-face stimulus were not slower when it was shown among threat faces than when it was shown among neutral faces. These results provide the first evidence that monkeys have an attentional bias toward the threatening faces of conspecifics and suggest that threatening faces are evolutionarily relevant fear stimuli. The subcortical visual systems in primates likely process not only snakes, but also more general biological threat-relevant stimuli, including threatening conspecific faces.