Early and late motor responses to action observation

Abstract

Is a short visuomotor associative training sufficient to reverse the visuomotor tuning of mirror neurons in adult humans? We tested the effects of associative training on corticospinal modulation during action observation in the 100-320 ms interval after action onset. In two separate experiments, the acceleration of transcranial magnetic stimulation (TMS)-induced movements was recorded before and after training participants to respond to observed acts with an opposite or similar behavior. Before training, TMS-induced accelerations mirrored the observed action at 250 and 320 ms. After training, responses at 250 ms were unchanged and still mirrored the stimuli, without any effect of training direction. Only at 320 ms, we observed training-dependent changes in evoked responses. A control experiment with non-biological rotational movements as visual stimuli indicated that spatial stimulus-response compatibility is not sufficient to account for the results of the two main experiments. We show that the effects of a short visuomotor associative training are not pervasive on the automatic mirror responses. 'Early' (250 ms) responses were not influenced by training. Conversely only 'late' (320 ms) responses changed according to the training direction. This biphasic time course indicates that two distinct mechanisms produce the automatic mirror responses and the newly learned visuomotor associations.

Keywords: action observation; action selection; associative sequence learning; mirror neurons; transcranial magnetic stimulation; visual motor training.

Fig. 1

Frame-by-frame representation of the movements presented to the participants in the (A) counter-imitative and imitative experiments. Every clip showed a right hand in egocentric perspective turning a lid clockwise (CW trials), counterclockwise (CCW trials) or simply moving down from the lid (Mov trials). In 9% of trials, a red dot appeared on the screen, to which participants had to respond as fast as possible with a left-hand button press.

Fig. 2

Frame-by-frame representation of the movements presented to the participants in the spatial-compatibility experiment.

Fig. 3

Schematization of the experimental setup showing orientation of the x, y and z axes.

Fig. 4

Plot from one representative participant, taken from the pilot evaluation, of the mean x-axis W-Acc (upper panel) and forearm EMG recordings (lower panel) obtained from 25 consecutive ‘passive’ trials and 25 consecutive ‘active’ trials. The dashed vertical line represents the time of TMS. The onset latency of the MEP is of 17 ms. Initial deflection of accelerations at 22 ms. Initial deviation of the acceleration trace due to voluntary interference is at 112 ms. The colored shadings represent the s.e.m. of acceleration signals. The gray shading represents the 30–90 ms interval that we subsequently chose to consider for analysis in the main experiment.

Fig. 5

Time course of the mean reaction times recorded during the behavioral trainings of the two main experiments and the control experiment. Asterisks indicate significant differences between consecutive blocks in paired-sample t-tests. Error bars represent 95% CI.

Fig. 6

Results of the counter-imitative (upper panel), imitative (middle panel) and spatial-compatibility (lower panel) experiments. The plot represents the mean of TMS-evoked W-Acc values measured on the x-axis of the accelerometer (±95% CI) in CCW and CW trials for all four ISIs, before training and after training. Error bars indicate 95% CI. The results of the two-way ANOVAs on single ISIs made to explore the three-way interaction are shown above each ISI; n.s. = non-significant.