Corticospinal Neurons in Macaque Ventral Premotor Cortex with Mirror Properties: A Potential Mechanism for Action Suppression?

Summary The discovery of “mirror neurons” in area F5 of the ventral premotor cortex has prompted many theories as to their possible function. However, the identity of mirror neurons remains unknown. Here, we investigated whether identified pyramidal tract neurons (PTNs) in area F5 of two adult macaques exhibited “mirror-like” activity. About half of the 64 PTNs tested showed significant modulation of their activity while monkeys observed precision grip of an object carried out by an experimenter, with somewhat fewer showing modulation during precision grip without an object or grasping concealed from the monkey. Therefore, mirror-like activity can be transmitted directly to the spinal cord via PTNs. A novel finding is that many PTNs (17/64) showed complete suppression of discharge during action observation, while firing actively when the monkey grasped food rewards. We speculate that this suppression of PTN discharge might be involved in the inhibition of self-movement during action observation.

Second, we recorded a small number of F5 neurons whose activity was related to licking and chewing movements. Covert movements of this kind might be expected to occur during action observation (Cattaneo et al., 2007), when food was being grasped by the experimenter. However, none of these mouth-related neurons showed significant modulation of discharge during action observation.
Finally, because we made simultaneous, multiple-electrode recordings of PTNs and other unidentified neurons we could check whether 'mirror-like' modulation was due to other non-specific changes in the monkey's attention or anticipation. We could demonstrate that while the monkey watched a specific set of actions carried out by the experimenter, some PTNs showed 'mirror-like' activity while others did not.
An example is shown in Fig. S4D and E. One PTN showed pronounced mirror-like facilitation (Fig. S4D), while another, recorded on a separate electrode only a few 100 microns away during the same set of trials, showed no modulation (Fig. S4E).

PTNs respond to grasp not kinematics of the approach movement
During tests for 'mirror-like' activity, all the actions were carried out slowly and deliberately in front of the monkey. We investigated whether PTNs modulated their discharge while the monkey observed the experimenter approaching and beginning to grasp in the 'action observation area' (the 'pre-sensor' period from -750 ms to sensor signal) or while the grasp was maintained for a short period, released and the hand withdrawn (the 'post-sensor' period from sensor signal to + 750 ms). In the example shown in Fig. S5, in which the experimenter performed precision grip with an object, the PTN's discharge was not modulated during the 'pre-sensor' period whereas there was clear suppression of activity in the 'postsensor' period. In seven sessions, we tested the effect of the experimenter approximately halving the speed of approach towards the food target. For 6 out of 8 mirror-like PTNs the time course of its activity was essentially unchanged. One example of such behaviour is shown in Fig. S5. The suppression of PTN discharge during slow and fast approach trials (rank-ordered for speed in Fig. S5B) were very similar when superimposed (Fig. S5C), suggesting that this PTN was mainly responding to the final grasping action of the experimenter, not to the dynamics of the approaching movement.

Mirror like activity for non-grasp condition
In one monkey we performed additional mirror test in which, the experimenter's hand approached the food reward and covered it with her hand, without grasping it. 25% of PTNs (3/12) that showed suppression of discharge during observation of precision grip also showed suppression during these 'flat hand' actions; the other 9 PTNs were unmodulated. Similarly, 33% (3/9) of facilitation PTNs recorded during observation of precision grip were also facilitated during observation of "flat hand" actions; the other 6 PTNs were unmodulated. Each trial started with home pad press (HPP) by the experimenter, then after approximately 1 s the experimenter released her hand (HPR) and started movement, (shown schematically by red dashed line) towards the magnetic sensor (SP)in the action observation area. When her hand touched the sensor an event signal was generated.

HPP HPR
HPP SP 1 s Experimenter Hand Position Figure S3. EMG control.
An example of a PTN recorded in an EMG "contaminated" session. All notations are as on Fig. 1. All trials show EMG activity from three example muscles (Biceps, ECR-L, EDC) are shown. Note the consistent EMG activity during action observation (right panel) just before the sensor touch signal at time zero. Changes in PTN discharge rate overlap with this EMG activity, which was of comparable amplitude to that recorded during active grasp (left panel).