Progressively shifting patterns of co-modulation among premotor cortex neurons carry dynamically similar signals during action execution and observation

ABSTRACT Neurons in macaque premotor cortex show firing rate modulation whether the subject performs an action or observes another individual performing a similar action. Although such mirror neurons have been thought to have highly congruent discharge during execution and observation, many if not most, show non-congruent activity. Studies of reaching movements, for which low-dimensional neural trajectories exhibit comparatively simple dynamical motifs, have shown that these prevalent patterns of co-modulation pass through subspaces which are shared in part, but in part are visited exclusively during either execution or observation. The neural dynamics of hand movements are more complex, however. We developed a novel approach to examine prevalent patterns of co-modulation during execution and observation of a task that involved reaching, grasping, and manipulation. Rather than following neural trajectories in subspaces that contain their entire time course, we identified time series of instantaneous subspaces, calculated principal angles among them, sampled trajectory segments at the times of selected behavioral events, and projected those segments into the time series of instantaneous subspaces. These instantaneous neural subspaces most often remained distinct during execution versus observation. Nevertheless, latent dynamics during execution and observation could be partially aligned with canonical correlation, indicating some similarity of the relationships among neural representations of different movements relative to one another during execution and observation. We also found that during action execution, mirror neurons showed consistent patterns of co-modulation both within and between sessions, but other non-mirror neurons that were modulated only during action execution and not during observation showed considerable variability of co-modulation.