Development of social systems neuroscience using macaques

Abstract

This paper reviews the literature on social neuroscience studies using macaques in the hope of encouraging as many researchers as possible to participate in this field of research and thereby accelerate the system-level understanding of social cognition and behavior. We describe how different parts of the primate brain are engaged in different aspects of social information processing, with particular emphasis on the use of experimental paradigms involving more than one monkey in laboratory settings. The description begins with how individual neurons are used for evaluating socially relevant information, such as the identity, face, and focus of attention of others in various social contexts. A description of the neural bases of social reward processing and social action monitoring follows. Finally, we provide several perspectives on novel experimental strategies to help clarify the nature of interacting brains under more socially and ecologically plausible conditions.

Primate Amygdala Neurons Simulate Decision Processes of Social Partners

“…These cognitive processes—learning from others and predicting their choices—are critical foundations for primates’ sophisticated social behavior. Yet, despite recent progress in primate social neuroscience (Adolphs, 2006, Chang et al., 2013a, Isoda et al., 2018, Lee and Seo, 2016, Wittmann et al., 2018), their neuronal basis is poorly understood.…”

Levels of naturalism in social neuroscience research

“…Level 4: Real-life social stimuli in lab environments While real-time videos and virtual characters are able to simulate dynamic and contingent social behaviors, the lack of real-life interaction may fail to induce the same behavioral or neural states as in real scenarios. The field of social neuroscience has been moving toward applying a two-person experimental approach (Gallotti and Frith, 2013;Schilbach et al, 2013;Isoda et al, 2018;Redcay and Schilbach, 2019). Recruiting pairs of participants or animals in the laboratory has the potential to capture naturalistic and interactive social behaviors.…”

“…Therefore, despite of existing applications in images and videos, we include virtual avatars in Level 3 given their potential to convey both dynamic and contingent social information. Researchers have begun to embrace the idea of including dyads or triads of real subjects in the laboratory ( Figure 1 , Level 4 ) ( Schilbach et al., 2013 ; Isoda et al., 2018 ). Studies using hyper-scanning via functional near-infrared spectroscopy (fNIRS), electroencephalogram (EEG), functional magnetic resonance imaging (fMRI), as well as simultaneous neuronal recording from multiple agents have revealed novel supports for inter-brain synchronization.…”

Human and macaque pairs employ different coordination strategies in a transparent decision game

“…Macaques play a particularly important role in this context, as the most common nonhuman primate model for studying the neuronal basis of higher socio-cognitive functions 4,13,14 . The realization that primate brain functions are best understood under social conditions in which they evolved sparked a surge of interest in behavioral repertoire and neural correlates of economic and social factors underlying social cognition in humans and nonhuman primates 15,16 .…”

“…The 9 human pairs that did not show significant dynamic coordination used strategies other than turn-taking. These alternative strategies included color-based strategies such as: (i) both agents largely converging on a fixed color (5, 14, 16, 10, 18; indicating that at least one of the two agents understood the value of coordination), (ii) exclusively selecting the respective own preferred color (4,19); and (iii) mixed color-side strategies where one agent consistently selected the non-preferred color while the other seemed to switch randomly between the two colors (11) or selected the right side (15). To summarize these results, more than half of the human pairs exhibited dynamic coordination and aimed for fairness.…”