Local field potentials are influenced by cooperative joint-action in frontal and parietal cortex of macaque monkeys

The importance of social interaction in human and cultural evolution is οnly surpassed by the extreme complexity of social brain functions, making neural processes underlying social behavior difficult to study. Actions are identified as own or alien and in some cases alien actions trigger the same neural activity as own actions. However, evidence of neuronal activity associated to joint action in a social context is scant. We studied extracellular local field potentials (LFPs:1-100 Hz) from premotor cortex (PM) and inferior parietal lobule (IPL) in two rhesus monkeys, during a joint-action task. Our goal was to determine not only the relationship between behavior and LFPs, but more importantly the context influence of an obligatory joint-action with a partner on neural activity. Monkeys were trained in a center-out task in two conditions. In the first condition (SELF) each monkey, individually, had to move its cursor from the center toward a peripheral target, by applying a force on an isometric joystick, while the partner monkey observed the action. In the second condition (cooperative joint action: COOP), both monkeys had to move their cursors simultaneously toward the same peripheral target, constrained by a maximum inter-cursor distance limit visualized as an outlined circle encompassing the two cursors. Thus, in this condition they had to cooperate to reach a common goal. We recorded neural activity from 236 PM and 166 IPL sites together with behavioral key events, simultaneously from homologous areas of both monkeys, by using two multiple-electrode arrays. Offline, we defined two epochs of interest, reaction time (RT: 0.2 s from target onset) and movement time (MT: 0.2 s from movement onset). For each trial we calculated the peak-to-peak LFP amplitude in each epoch. Finally we compared these values between the self-acting (SELF) and joint acting (COOP) and between peripheral target directions. Behavioral analysis of reaction time and movement time showed that monkeys adapted their behavior during the joint-action condition in order to accommodate the partner’s behavior. A two way ANOVA showed a significant difference of LFP activity during RT or MT between SELF and COOP conditions in 25.8 % PM and 21.1% IPL sites and between peripheral target directions in 41.9% PM and 36.7 % IPL sites with an interaction factor that resulted significant in 11% PM and 13% IPL sites. Our data show that there exists in the parieto-frontal system an action cooperation network which is set in motion during cooperative joint-action. We also show that LFP, reflecting cell assembly coordination, can disclose executive and higher-order neural processes.