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The coordinated interplay between prefrontal areas and amygdala in social gaze dynamics and decision-making

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Gaze interaction is central to social behavior in humans and non-human primates, and is often used as a proxy for social attention. However, the neural mechanisms underlying contingent and spontaneous social gaze events as they unfold over time remain elusive. Recently, we have been using a real-life social gaze interaction paradigm to study neurophysiological mechanisms underlying spontaneous and contingent gaze dynamics occurring between pairs of rhesus macaques (Macaca mulatta). This naturalistic setting combined with high-resolution eye position monitoring of both animals allows for the necessary quantification of social gaze dynamics while increasing ecological validity. We have previously used this task to document that certain aspects of social gaze behaviors are not reliably captured using pictures and movies of conspecific monkeys (Dal Monte et al., 2016, J Neurophys), and also to report a combinatorial boost in social attention and contingent gaze dynamics when oxytocin processing is enhanced while opioid processing is concurrently attenuated using naloxone (Dal Monte et al., 2017, PNAS). Using this paradigm, here we investigated the contribution of the basolateral amygdala (BLA) and three prefrontal structures – the anterior cingulate gyrus (ACCg), the orbitofrontal cortex (OFC), and the dorsomedial prefrontal cortex (dmPFC) – in live social gaze interactions. Both spiking and local field potential activity were recorded from one of the prefrontal structures simultaneously with the BLA, allowing us to examine neural coordination patterns between each prefrontal region and the BLA in mediating social gaze behaviors. Neural data were aligned to diverse gaze events, such as looking at the partner’s eyes (in the contexts of mutual gaze or exclusive gaze), other regions of conspecific’s face, or non-social objects of interest.While neurons from all brain regions signaled various social gaze events, they displayed marked heterogeneities in the temporal dynamics of spiking activity when encoding these events. Across these brain regions, the proportion of cells that differentiated looking at the eyes from other parts of the face and those that exhibited face-selective signals also differed, suggesting distinct contributions of different brain regions. Furthermore, between the prefrontal regions and the BLA, divergent coupling patterns in the gamma band tracked social gaze events, depending on the specific prefrontal node being examined with respect to the BLA. For the ACCg-BLA pairing, we were also able to examine their interplay in a social decision-making context using a social reward allocation task, in which monkeys make decisions impacting the reward outcome of a conspecific monkey in the room, without affecting their own reward outcomes, in two separate decision contexts (Chang et al., 2013, Nat Neurosci). In this task, monkeys typically exhibit a prosocial preference in one context but an antisocial preference in the other context. The ACCg-BLA coherence patterns markedly differed across the gamma and beta bands between the two decision-making contexts, and these coherence patterns could be used to decode the prosocial preference of the animals. Our findings overall suggest that dynamic coordination between the prefrontal structures and the amygdala may play a central role in guiding social behavior.


Steven Chang (Yale University)

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Deutsches Primatenzentrum

Leibniz WissenschaftsCampus


Benedict Wild & Igor Kagan

Kognitive Neurowissenschaften

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