Whole-agent selectivity within the macaque face-processing system

Abstract

The primate brain contains a set of face-selective areas, which are thought to extract the rich social information that faces provide, such as emotional state and personal identity. The nature of this information raises a fundamental question about these face-selective areas: Do they respond to a face purely because of its visual attributes, or because the face embodies a larger social agent? Here, we used functional magnetic resonance imaging to determine whether the macaque face patch system exhibits a whole-agent response above and beyond its responses to individually presented faces and bodies. We found a systematic development of whole-agent preference through the face patches, from subadditive integration of face and body responses in posterior face patches to superadditive integration in anterior face patches. Superadditivity was not observed for faces atop nonbody objects, implying categorical specificity of face–body interaction. Furthermore, superadditivity was robust to visual degradation of facial detail, suggesting whole-agent selectivity does not require prior face recognition. In contrast, even the body patches immediately adjacent to anterior face areas did not exhibit superadditivity. This asymmetry between face- and body-processing systems may explain why observers attribute bodies’ social signals to faces, and not vice versa. The development of whole-agent selectivity from posterior to anterior face patches, in concert with the recently described development of natural motion selectivity from ventral to dorsal face patches, identifies a single face patch, AF (anterior fundus), as a likely link between the analysis of facial shape and semantic inferences about other agents.

Face Processing Systems: From Neurons to Real-World Social Perception

“…Functional specializations along the ventral series of face areas follow a progression similar to that in the macaque monkey, suggesting a hierarchical organization: in the occipito-temporal direction face selectivity increases (Bell et al 2009), position dependence decreases (Hemond et al 2007), mirror symmetric confusion of facial profile views emerges (Axelrod & Yovel 2012, Kietzmann et al 2012), and facial identity selectivity grows stronger (Yang, Susilo, & Duchaine, in press). Similarly, in both macaque and human face areas, the response to faces is augmented in the presence of an anatomically correctly placed body, and this augmentation grows stronger from posterior to anterior face areas (Bernstein et al 2014, Fisher & Freiwald 2015b, Song et al 2013). Furthermore selectivity for facial motion is highly pronounced in dorsal areas, but not in ventral ones (Fox et al 2009, Pitcher et al 2011a).…”

Marmosets: A Neuroscientific Model of Human Social Behavior

“…Brain imaging and electrophysiological experiments have shown that multiple ‘face patches’ are evident in the temporal lobe of humans, rhesus monkeys, and marmosets (Hung et al, 2015; Kanwisher et al, 1997; Tsao et al, 2008), suggesting that such a network might be a core feature of the primate social brain. Current studies are investigating specialization among such regions for extracting different types of information from faces, such as head orientation, direction of gaze, individual identity, body context, and facial motion (Fisher and Freiwald, 2015a, b; Freiwald and Tsao, 2010; Hoffman and Haxby, 2000; Leopold et al, 2006; Polosecki et al, 2013). …”

Two areas for familiar face recognition in the primate brain

“…Fourth, generalizing past electrophysiological findings of personal familiarity (39), which had suggested localized representations (39–41), response enhancement by personal familiarity was ubiquitous within face selective areas. Thus the faces that shape face-selective cortex throughout ontogeny appear to alter all the different face representations that the face-processing system harbors (15, 17, 42). Finally, familiarity effects did not grow stronger as face representations get transformed from picture to identity-based formats from posterior to anterior IT core face areas.…”