Activation of human primary motor cortex during action observation: a neuromagnetic study

Abstract

The monkey premotor cortex contains neurons that discharge during action execution and during observation of actions made by others. Transcranial magnetic stimulation experiments suggest that a similar observation/execution matching system also is present in humans. We recorded neuromagnetic oscillatory activity of the human precentral cortex from 10 healthy volunteers while (i) they had no task to perform, (ii) they were manipulating a small object, and (iii) they were observing another individual performing the same task. The left and right median nerves were stimulated alternately (interstimulus interval, 1.5 s) at intensities exceeding motor threshold, and the poststimulus rebound of the rolandic 15- to 25-Hz activity was quantified. In agreement with previous studies, the rebound was strongly suppressed bilaterally during object manipulation. Most interestingly, the rebound also was significantly diminished during action observation (31-46% of the suppression during object manipulation). Control experiments, in which subjects were instructed to observe stationary or moving stimuli, confirmed the specificity of the suppression effect. Because the recorded 15- to 25-Hz activity is known to originate mainly in the precentral motor cortex, we concluded that the human primary motor cortex is activated during observation as well as execution of motor tasks. These findings have implications for a better understanding of the machinery underlying action recognition in humans.

Figure 1

Schematic presentation of the experimental condition. During the experiment the subject was sitting beneath the magnetometer and both median nerves were stimulated alternately. (a) Resting condition: the subject has no task. (b) Acting condition: the subject manipulates a small object with her right hand. (c) Action viewing: the subject views another person performing similar manipulations.

Figure 2

Level of the 15- to 27-Hz activity of subject SS as a function of time, recorded with the 122-channel neurogradiometer during the resting condition. Signals are shown from the time of RMN stimuli to 1,450 ms afterward. The head is viewed from the top. The upper and lower traces of each signal pair refer to the latitudinal and longitudinal gradients, respectively. Inset shows signals from the left rolandic region enlarged and responses from all conditions superimposed.

Figure 3

Source locations of the 20-Hz activity in the left hemisphere of subject SS. The dots illustrate single, equivalent current dipoles used to model the field pattern during single cycles of the 20-Hz oscillation. The clusters are enlarged below and illustrate a clear concentration of sources to the precentral motor cortex, just anterior to the central sulcus. The squares illustrate the source of the 20-ms response to right median nerve stimulation.

Figure 4

Suppression of the 20-Hz rebound, calculated as a percentage of individual suppressions during object manipulation (mean + SEM of eight subjects).