Action observation responses in macaque frontal cortex

Neurons that are active during action execution and action observation (i.e. Action Observation/Execution Neurons, AOENs) are distributed across the brain in a network of parietal, motor, and prefrontal areas. In a previous study, we showed that most AOENs in ventral premotor area F5c, where they were discovered three decades ago, responded in a highly phasic way during the observation of a grasping action, did not require the perception of causality or a meaningful action, and even responded to static frames of the action videos. To assess whether these characteristics are shared with AOENs in other areas of the AOE network, we performed the first large-scale neural recordings during action execution and action observation in multiple frontal areas including dorsal premotor (PMd) area F2, primary motor (M1) cortex, ventral premotor area F5p, frontal eye field (FEF) and 45B. In all areas, AOENs displayed highly phasic responses during specific epochs of the action video and, in addition, strong responses to a moving object, similar to F5c. In addition, the population dynamics in PMv, PMd and M1 showed a shared representation between action execution and action observation, with an overlap that was as large as the overlap between action execution and passive viewing of translation movements. These results pose important constraints on the interpretation of action observation responses in frontal cortical areas. • We performed large-scale neural recordings of action execution/observation neurons (AOENs) in multiple frontal areas. • In all areas, AOENs displayed highly phasic responses during specific epochs of the action video. • In all frontal areas, AOENs showed strong responses to movements of a simple object, similar to F5c. • The population dynamics in PMv, PMd and M1 showed a shared representation between action execution and action observation.