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.

Bottom-Up and Top-Down Visuomotor Responses to Action Observation

“…The results of the first experiment of the present work validate and extend the results of our previous work showing biphasic responses to others' actions in conflictual stimulus-response behavior. The latency of the early response observed in Barchiesi and Cattaneo (2013) was of 250 ms from stimulus onset, while, in the present work, it was confined at 150 ms from movement onset. Though the biphasic pattern is preserved in the 2 experiments, the difference in timing of the early response is due, in our view, to 2 separate phenomena.…”

“…Though the biphasic pattern is preserved in the 2 experiments, the difference in timing of the early response is due, in our view, to 2 separate phenomena. First, the mirror response is highlighted earlier in the present experiment because it is recorded during movement preparation compared with the passive viewing condition of Barchiesi and Cattaneo (2013), thus decreasing the excitability threshold of the motor system. Second, one possible explanation why the mirror response is no longer seen at 250 ms could be that the task stresses the speed of response and the counter-mirror effect is anticipated and therefore it overrides the mirror response at an earlier time than during passive observation.…”

“…It has been referred to as "stimulus-driven," "bottom-up," "automatic," "exogenous," or "the what system." Conversely, the process responsible for the late response has been defined as "goal-driven," "top-down," "voluntary," "executive," or "the how system" (Theeuwes et al 1998;Passingham and Toni 2001;Siebold et al 2011;McBride, Boy, et al 2012;Barchiesi and Cattaneo 2013).…”

The multiform motor cortical output: Kinematic, predictive and response coding

“…We propose it is an associative memory which by default implements a mirroring behavior, but that can adapt through experience to generate complementary responses: the existence of counter-mirror effects supports indeed this hypothesis (Catmur, Walsh, & Heyes, 2007;Barchiesi & Cattaneo, 2013;Cavallo, Heyes, Becchio, Bird, & Catmur, 2013b).…”

Direct mapping rather than motor prediction subserves modulation of corticospinal excitability during observation of actions in real time

“…In contrast with most previous studies, which used slow actions ranging from 2.4 to 5.6 s to track the time course of CSE (e.g., Cavallo et al 2013;Gangitano et al 2001Gangitano et al , 2004Jansen et al 2013;Lago and Fernandez-del-Olmo 2011), in the present study actions were displayed in real time (movement duration was 1.16 s). Note that whereas artificially slow movements used in most action observation studies might enhance the observer's discrimination performance, actions in real time are crucial to maintain the time course of CSE within the physiological range characteristic of natural actions (e.g., Barchiesi and Cattaneo 2013;Cattaneo et al 2009). Another key difference from previous studies was the fast sampling rate used to record CSE (4 TMS pulses were applied within a 240-ms time window), which allowed us to finely track kinematic changes with high temporal resolution.…”