Face recognition as a function of social attention in non-human primates: an ERP study

Epidural event related potentials (ERPs) were recorded from four squirrel monkeys (Saimiri sciureus) during the presentation of pictoral stimuli that comprised real human and monkey faces. Subjects viewed tachistoscopically presented stimuli belonging to four different categories: familiar and unfamiliar human faces, and familiar and unfamiliar monkey faces. Familiar faces were subcategorized into top, middle and bottom according to the perceived individual's dominance ranking in a social hierarchy, as rated by human judges observing the group's social behavior. Waveform peak components to monkey and human faces showed similarities in their spatial distribution. However, larger amplitude N1 and N2 components were elicited in response to monkey compared to human faces, particularly over lateral temporo-parietal sites. A similar trend was observed for the P3 component, with maximal differences along midline electrode site. Responses to familiar and unfamiliar monkey faces showed larger N1s to familiar monkey faces and larger P3s to unfamiliar monkey faces. N1 and P3 components elicited by human faces showed no significant differences between conditions. N2 amplitudes were larger over posterior sites for top-ranked monkeys and larger over frontal sites for middle- and bottom-ranked monkeys. Top-ranked human faces elicited the largest N2 components, middle-ranked faces the next largest, and bottom-ranked faces the smallest. N1, N2, and P3 latencies were similarly sensitive to the ranking of human but not monkey faces. These data suggest that non-human primates exhibit evoked potentials to conspecific and non-conspecific faces that are similar in morphology but different in function. Larger amplitude responses to monkey faces suggests increased processing for that category of stimuli. Additionally, monkey ERPs reflect familiarity with conspecifics but not with human faces. Finally, the social status of the perceived individual, or at least the perceived threat posed by an individual, affects the latencies and magnitudes of ERP components produced by the viewer. These data are consistent with social attention hypotheses which propose that higher status (i.e. more dominant or socially meaningful) members of a group receive more attention than lower status individuals.