Prefrontal and Amygdalar Mechanisms of Live Social Gaze Interaction

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Project Summary Social interactions are marked by contingent and dynamic gaze exchanges among individuals, and these exchanges powerfully shape inter-individual communication and coordinated social behaviors. Consequentially, divergent social gaze interactions frequently lead to challenges in gathering and processing information from others and further disrupt other social cognition. An excellent use of a non-human primate model is to study neural circuits underlying contingent and dynamic social gaze, and test for their causal contributions. We have shown that interacting with a real partner leads to drastically different social gaze dynamics compared to observing the same conspecific in pictures or videos. Furthermore, using this live social gaze interaction paradigm, we have recently found robust neural correlates of social gaze interaction in the orbitofrontal cortex (OFC) and the basolateral amygdala (BLA). However, causal roles of OFC and BLA, and the OFC-BLA interplay, in regulating social gaze interaction remain unestablished. Informed by our latest data and other emerging findings from the field, we hypothesize that (1) BLA is required for preferentially directing attention to social stimuli by processing social gaze valence, whereas (2) OFC is required for regulating social gaze interaction according to social context, and that (3) the communication between OFC and BLA is required for contingent and dynamic social gaze interaction. To test this overarching hypothesis, we will first examine the functional relationship between social gaze preference and value processing in OFC and BLA neurons. We hypothesize that BLA neurons process social gaze interaction using a valence schema, whereas OFC neurons do not. Second, we will examine the necessity of OFC, BLA, and the OFC-BLA interplay in social gaze interaction by temporarily inactivating OFC or BLA, or cross-inactivating OFC and BLA. We hypothesize that BLA is necessary for preferentially directing attention to partner’s eyes and processing them, whereas OFC is necessary for social context-dependent changes in gaze dynamics linked to dominance and familiarity between pairs. We also predict that the direct communication between OFC and BLA is particularly crucial for interactive aspects of social gaze. Finally, by recording neural activity from one area while temporarily inactivating the other area, we will examine the neural representations of social gaze interaction in OFC and BLA that require functioning BLA or OFC, respectively. Results from this proposal will provide functionally informed causal contributions of the OFC-BLA circuits in real-life social gaze interaction.