Quantitative analysis of motor behavior and neural activity associated to joint-action during social cooperation in frontal and parietal cortex of macaque monkeys

The neural mechanisms related to the ability of humans and non-human primates to interact through joint-action are still poorly investigated. In the domain of motor functions, the study of goal-directed movement showed that no obligatory relationship exists between neural activity and movement, but rather movement-related activity is context-dependent and linked to different cognitive states. So far, neural activity in different cortical areas has been studied in a single brain in action, thus missing all information typical of interacting brains through a joint action task. To study both behavioral parameters and potential neural codes for joint action, two macaque monkeys were trained to perform a cooperative joint action task. Monkeys were required to perform individual or cooperative actions, exerting a force on an isometric joystick. Extracellular single-unit activity (SUA) was recorded from dorsal premotor cortex (PMd) and inferior parietal lobule (IPL), simultaneously from homologous areas of both monkeys by using two multiple-electrode arrays. We showed that in monkeys does not exist a single motor strategy to execute cooperative action. High variability of all the considered parameters has been observed across directions of movement, monkeys and conditions, indicating that different strategies are used by the partners to accomplish a common goal, depending on types of movement to be executed. However, specific temporal and spatial parameters (RTs, peak velocity and inter-cursor distance) indicate that monkeys during the cooperative condition adapt their own behavior to the other’s action in order to successfully achieve their common goal. Furthermore, through the study of Granger method we observed causality relations between cursors’ trajectories during cooperative actions. Regarding the analysis of neural activity, we endorsed the hypothesis that frontal and parietal regions contribute to the coding of motor behavior specifically during the execution of a joint action task. These findings provide a quantitative descriptions of motor behavior of two cooperating monkeys and represent a first step toward the description of the neural operations underlying motor functions in a cooperative context and suggest that within this action cooperation network different areas encode joint-action.