Phd in PHD PROGRAM IN BEHAVIORAL NEUROSCIENCE

Thesis title: Neuronal Correlates of Motor Control and Economic Decision-Making During Social Interactions in Non-Human Primates

A cornerstone of the evolution of human species lies in social behavior and cooperation, suggested to be the third pillar of evolution alongside mutation and natural selection (Nowak, 2006). Among the numerous forms of social behavior, the motor interaction between individuals — named Joint Action — represents the dynamic core of cooperation. Motor control studies focused mainly on solipsistic movement and revealed our motor systems are complex. It was hypothesized the brain uses internal models — neural representations that simulate aspects of the body and environment — allowing for predicting consequences of an action, learn, plan, and control movements, thereby managing the complexity of motor behavior (D. M. Wolpert et al., 1995; Miall & Wolpert, 1996). How these models apply to the motor interaction between subjects, where it is necessary to predict the intentions and movements of the partner, which are characterized by a high intrinsic unpredictability? In understanding others’ actions, the discovery of the mirror neuron system represented a ground-breaking insight into how the brain maps observed behavior onto internal motor processes (Gallese et al., 1996, 2004). Building on this, it has been hypothesized that motor control theories could be extended from solipsistic to social context (Wolpert et al., 2003). However, while these works have served as a foundational pillar in the study of action observation, they do not fully account for motor interactions between individuals, where simultaneous movements of two or more agents occur in interactive settings. Indeed, recent hypothesis suggest that sharing actions require a more sophisticated model of motor control — one that involves a shared representation integrating both one’s own and the partner’s actions (della Gatta et al., 2017; Sacheli et al., 2018; Kourtis et al., 2019; Lacal et al., 2022; Marschner et al., 2024), and relies on a predictive motor representations of collective goals (Pezzulo et al., 2025). It was previously showed that non-human primates are able to coordinate each other in a joint fashion, by dynamically adjusting their motor behavior to foster synchronization (Visco-Comandini et al., 2015). A specialized class of neurons encoding joint actions in dorsal premotor cortex have also been discovered (Ferrari-Toniolo et al., 2019). Furthermore, empirical evidence has been provided that, like humans, also macaques exploit on a shared representation (Lacal et al., 2022), suggesting the formation of dyadic motor plan. Within this framework the first study of this thesis tried to respond to these questions: how such dyadic motor plan are represented at neural population level? Do monkey leverage on proactive mechanisms when engaged in joint actions? Study 1. The aim of the first study was to investigate how Local Field Potentials (LFPs) recorded from dorsal Premotor Cortex (area F2) encode the spatiotemporal components of Joint Action, potentially providing the first neuronal population-level evidence for a dyadic motor representation. To this purpose, we simultaneously recorded LFPs from the PMd of two monkeys engaged in a pre-cued centre-out joint action task. Our findings provided new insights into the population-level neural mechanisms associated with Joint Action coding in the dorsal Premotor Cortex, as reflected in low-frequency LFPs. Surprisingly, these low-frequency LFPs were found to predict the quality of dyadic interaction, and neuronal synchronization in the LFP components mirrored their timing coordination during motor planning. These findings suggest monkeys leveraged on shared motor representations, and provide a neuronal substrate for the predictions necessary for joint temporal and spatial coordination. In the second study we considered the cost of acting together. While joint actions enable individuals to achieve goals that would be unattainable alone, their probability of success may be reduced due to the increased complexity and coordination demands involved. Indeed, when deciding to act together a cognitive effort is required as it is necessary to anticipate the partner’s intentions to successfully perform joint decisions. Added to this is the difficulty of coordinating together within temporal ans spatial constraints. Indeed, despite the implementation of the strategy to reduce individual motor variability to face with the partner’s motor unpredictability, monkeys showed a lower probability to successfully perform joint actions compared to individual actions (Visco-Comandini et al., 2015; Lacal et al., 2022). Therefore, when monkeys are faced with the choice of whether to act alone or with others, decisions might impinge upon a careful cost-benefit evaluation. Thus, in second study we asked whether monkeys consider the cost-benefit of joint action while free to choose whether acting alone or together and whether they are able to update their decision processes to the partner’s intentions. Moreover, we aimed at exploring the neuronal underpinnings of economic decisions during such social context. Study 2. The first goal of this work was to investigate the behavioral strategies that monkeys employ to make joint decisions, using motor control as a window into the underlying decision-making processes (Quarta et al., in in prep.). Specifically, we asked whether monkeys take into account the cost of cooperation, and we aimed at estimate this subjective cost by varying the level of reward payoff associated with individual versus joint actions. To this purpose, we developed a novel joint action choice task in which two monkeys were free to choose between acting alone (SOLO) or jointly (JA), based on the varying quantity of reward associated to each offer. Two targets were presented, each indicating both the reward magnitude and the action type ("SOLO" or "JA") required to obtain the desired reward. Using an isometric joystick, each monkey expressed its choice by guiding a cursor towards the chosen target to gain the reward associated with. Secondly, and most importantly, to investigate the neuronal basis of this process, we focused on the dorsolateral prefrontal cortex (dlPFC), a region previously implicated in social and economic decision-making. Behaviorally, monkeys demonstrated the ability to evaluate the trade-offs between coordination costs and reward benefits. We inferred their subjective cost of cooperation and found that the two monkeys shared a similar valuation. Over time, they showed an increased tendency to choose the joint action, which was accompanied by a reduced subjective cost of cooperation. These findings suggest that monkeys were capable of representing their partner’s choices, and learned to make better joint decisions to maximize overall reward. At neuronal level, preliminary analyses suggest that the dlPFC’s neurons may play a critical role in economic decision-making within social contexts, and may encode the complex cost-benefit computations required when deciding whether to act alone or together. Interestingly, we found neurons modulated by the decision to act together (Joint Action Selection cells), the choice of the partner (Other-Choice cells) and neurons modulated by the joint action during motor planning and execution. While these findings are promising, further investigation is needed to fully characterize the nature and dynamics of these neural signals.