Largely shared neural codes for biological and nonbiological observed movements but not for executed actions in monkey premotor areas

The neural processing of others' observed actions recruits a large network of brain regions (the action observation network; AON) in which frontal motor areas are thought to play a crucial role. As the discovery of mirror neurons (MNs) in the ventral premotor cortex, it has been assumed that their activation was conditional upon the presentation of biological rather than nonbiological motion stimuli, supporting a form of direct visuomotor matching. Nonetheless, nonbiological observed movements have rarely been used as control stimuli to evaluate visual specificity, thereby leaving the issue of similarity among neural codes for executed actions and biological or nonbiological observed movements unresolved. Here, we addressed this issue by recording from two nodes of the AON that are attracting increasing interest, namely, the ventrorostral part of the dorsal premotor area F2 and the mesial presupplementary motor area F6 of macaques while they ) executed a reaching-grasping task, ) observed an experimenter performing the task, and ) observed a nonbiological effector moving in the same context. Our findings revealed stronger neuronal responses to the observation of biological than nonbiological movement, but biological and nonbiological visual stimuli produced highly similar neural dynamics and relied on largely shared neural codes, which in turn remarkably differed from those associated with executed actions. These results indicate that, in highly familiar contexts, visuomotor remapping processes in premotor areas hosting MNs are more complex and flexible than predicted by a direct visuomotor matching hypothesis. Pioneering studies on mirror neurons (MNs) in premotor areas emphasized the absence of response to the sight of nonbiological moving objects, suggesting a match between execution and observation activities. This study shows that although premotor neurons can discriminate between biological and nonbiological observed movements, these visual stimuli rely on largely shared neural codes, which differ strongly from those associated with executed actions.