A dedicated network for social interaction processing in the primate brain

Abstract

Primate cognition requires interaction processing. Interactions can reveal otherwise hidden properties of intentional agents, such as thoughts and feelings, and of inanimate objects, such as mass and material. Where and how interaction analyses are implemented in the brain is unknown. Using whole-brain functional magnetic resonance imaging in macaque monkeys, we discovered a network centered in the medial and ventrolateral prefrontal cortex that is exclusively engaged in social interaction analysis. Exclusivity of specialization was found for no other function anywhere in the brain. Two additional networks, a parieto-premotor and a temporal one, exhibited both social and physical interaction preference, which, in the temporal lobe, mapped onto a fine-grain pattern of object, body, and face selectivity. Extent and location of a dedicated system for social interaction analysis suggest that this function is an evolutionary forerunner of human mind-reading capabilities.

Neural processing of social interaction: Coordinate‐based meta‐analytic evidence from human neuroimaging studies

“…This hypothesis is supported by recent fMRI data from monkeys engaged in the visual processing of interactions (Sliwa & Freiwald, ), in which planned contrasts allowed to ascribe the recruitment of classical visuomotor areas to the decoding of agents' actions. Instead, medial prefrontal regions displayed a selective response to interactions.…”

“…Instead, medial prefrontal regions displayed a selective response to interactions. The spatial overlap between these regions and the human mentalizing network suggested a role for such “ exclusively social interaction network ” in drawing inferences about the intentional states underlying the observed interactions, which in turn might have represented a potential evolutionary pressure to the development of mentalizing skills (Sliwa & Freiwald, ). We thus assessed whether available evidence from published studies supports the existence of “ exclusively social ” brain activations also in the human brain, or rather the neural processing of interactions can be reduced to the joint engagement of the mirror and mentalizing networks.…”

Perceiving social interactions in the posterior superior temporal sulcus

“…Of note, a recent study in macaques found regions of the frontal and parietal cortex that responded exclusively to movies of monkey social interactions and not to movies of monkeys conducting independent actions or of interactions between inanimate objects (4). If humans have a similarly selective cortical response to social interactions, where might it be found in the brain?…”

“…We see not just agents and objects, but also agents interacting with each other. The ability to perceive and understand social interactions arises early in development (1) and is shared with other primates (2)(3)(4). Although considerable evidence has implicated particular brain regions in perceiving the characteristics of individual agents-including their age, sex, emotions, actions, thoughts, and direction of attention-whether specific regions in the human brain are systematically engaged in the perception of third-party social interactions is unknown.…”

The Active Inference Approach to Ecological Perception: General Information Dynamics for Natural and Artificial Embodied Cognition

“…There is evidence of this mechanism in brain scans of primates (Sliwa and Freiwald, 2017) and human infants (de Haan andNelson, 1999, Southgate et al, 2008), and from human in utero behavioral experiments (Reid et al, 2017). This mechanism would plausibly underpin the fundamentality of social cooperation to human cognition (Barrett et al, 2010, Cortina andLiotti, 2010); a related point has been made about language, noting the fundamentality of dialog from which monolog is derived (Pickering and Garrod, 2004).…”