Mirror neuron activation prior to action observation in a predictable context

Abstract

A fundamental capacity of social animals consists in the predictive representation of upcoming events in the outside world, such as the actions of others. Here, we tested the activity of ventral premotor area F5 mirror neurons (MNs) while monkeys observed an experimenter performing (Action condition) or withholding (Inaction condition) a grasping action, which could be predicted on the basis of previously presented auditory instructions. Many of the recorded MNs discharged only during action observation (Action MNs), but one-third also encoded the experimenter's withheld action (Inaction MNs). Interestingly, while most of Action MNs exhibited reactive discharge during action observation, becoming active after the go signal, the majority of Inaction MNs showed predictive discharge. MN population activity as a whole displayed an overall predictive activation pattern, becoming active, on average, 340 ms before the go signal. Furthermore, MNs became active earlier when the observed action was performed in the monkeys' extrapersonal rather than peripersonal space, suggesting that context-based neural prediction of others' actions plays different roles depending on the monkeys' ability to interact with the observed agent.

Keywords: area F5; contextual information; motor prediction.

Figure 1.

A, Phases of the tasks. Note that the temporal structure and task phases of the OT and ET are identical. B, Examples of the visual and motor responses of Action and Inaction MNs showing reactive or predictive discharge during the OT. Rasters and histograms are aligned on the cue sound offset (go/no-go signal, dashed vertical lines). The gray-shaded regions indicate the time windows used for the statistical analysis. Yellow, object presentation; orange, detachment of hand from the starting position (reaching onset); blue, object-pulling onset. Green arrows indicate the timing of discharge onset (see Materials and Methods for details on the procedure for the identification of discharge onset timing). C, Pie charts showing the percentage of Action and Inaction MNs with predictive or reactive discharge.

Figure 2.

Population activity of Action and Inaction MNs during both Action (green) and Inaction (red) conditions of the OT. In each part, the left side is aligned on the cue sound onset and object presentation (dashed vertical lines), while the right side is aligned on the go/no-go signal. The median time of reaching onset and object-pulling onset are indicated with the orange and blue markers, respectively, above each population plot. Shaded areas around each marker represent the 25th and 75th percentile times of other events of the same type. The green arrows indicate the onset timing of the action observation response. The green and red shadings around each curve represent 1 SE.

Figure 3.

A, Distribution of the discharge onset timing, relative to the go-signal, of MNs discharging in the extrapersonal (green) or peripersonal (blue) space overlapped. B, Scatter plot and histograms illustrating the distribution of discharge onset timing among MNs responding to the observation of actions in both the peripersonal and extrapersonal space. The dashed line indicates the function x = y. C, Examples of two MNs discharging during the observation of actions in the peripersonal and extrapersonal space. Green and blue arrows specify the timing of discharge onset in the extrapersonal and peripersonal space, respectively. Other conventions are as in Figure 1.