Neural representations of self and other’s actions in the monkey putamen nucleus

It is widely accepted that the cortical motor system plays a pivotal role not only in motor control, but in a variety of advanced perceptual, cognitive, and social functions as well. When observing the actions of others, an extended Action Observation Network (AON) encompassing cortical regions devoted to action planning and execution becomes active. Anatomical data in monkeys demonstrated that areas of the AON send convergent projections to overlapping territories of the putamen nucleus in the basal ganglia, suggesting that this nucleus may not only contribute to the selection of one’s own action, but also to the representation of the action of others. To address this issue, we recorded neuronal activity from 573 single-units in the putamen nucleus of two male rhesus macaques (Macaca mulatta) during a Mutual Action Task in which each animal and an experimenter facing the same device in a shared operational space in between them, took turns based on learned contextual cues to grasp or observe the other agent grasping and lifting the same multi-affordance object, which could be grasped wither with a precision grip (PG) or with a whole hand prehension (WH). Most of the recorded neurons (n = 301) exhibited a modulation during the reaching-grasping period of the task performed by the animals, most often with an increase of their firing rate with respect to the baseline. Almost 40% of the motor-related units (n = 120) showed a significantly different discharge between the two examined grip types, with a similar number of neurons exhibiting a preference for PG and WH prehension. Amongst those neurons whose activity was modulated during the reaching-grasping epoch of the task, we found that the great majority encoded selectively monkeys’ own action (self-type, n = 212), a smaller fraction was active only during action observation (other-type, n = 66), whereas the remaining discharged in both conditions (self-other type, n = 89). During active movement facilitated neurons prevailed over suppressed ones, whereas in observation trials we found a balanced number of excited an inhibited cells. Amongst self-other type neurons, the majority exhibited a “classical” MN activity, being facilitated during both action execution and observation (FF-type, n = 41), however we also recorded a sizeable fraction of cells being consistently suppressed during both conditions (SS-type, n = 26), or that showed opposite discharge patterns depending on which subject was performing the action (FS- and SF-type). Our findings constitute one of the first empirical demonstrations of the existence of putamen neurons specifically modulated by others’ observed actions, supporting the hypothesis of an involvement of the basal ganglia in the AON and indicating the need to causally investigate its overall modulatory impact on the functioning of the cortical AON.