Neuronal Population Encoding of Identity in Primate Prefrontal Cortex

The ventrolateral prefrontal cortex (VLPFC) shows robust activation during the perception of faces and voices. However, little is known about what categorical features of social stimuli drive neural activity in this region. Since perception of identity and expression are critical social functions, we examined whether neural responses to naturalistic stimuli were driven by these two categorial features in the prefrontal cortex. We recorded single neurons in the VLPFC, while two macaques viewed short audiovisual videos of unfamiliar conspecifics making expressions of aggressive, affiliative, and neutral valence. Of the 285 neurons responsive to the audiovisual stimuli, 111 neurons had a main effect (two-way ANOVA) of identity, expression or their interaction in their stimulus related firing rates; however, decoding of expression and identity using single unit firing rates rendered poor accuracy. Interestingly, when decoding from pseudopopulations of recorded neurons, the accuracy for both expression and identity increased with population size, suggesting that the population transmitted information relevant to both variables. Principal components analysis of mean population activity across time revealed that population responses to the same identity followed similar trajectories in the response space, facilitating segregation from other identities. Our results suggest that identity is a critical feature of social stimuli that dictates the structure of population activity in the VLPFC, during the perception of vocalizations and their corresponding facial expressions. These findings enhance our understanding of social behavior beyond the temporal lobe in macaques and humans. Significance Statement Primates are unique in their ability to process and utilize complex, multisensory social information. The brain networks that support this are distributed across the temporal and frontal lobes. In this study, we characterize how social variables like identity and expression are encoded in the neural activity of the ventrolateral prefrontal cortex (VLPFC), a prefrontal region of the macaque brain. We found that single neurons do not appear to encode these variables, but populations of neurons display similar activity patterns that are primarily differentiated by the identity of the conspecific that a macaque is attending to. Furthermore, by employing dynamic, multisensory stimuli, our experiment better approximates real world conditions, making our findings more generalizable.