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

Abstract

Action observation produces automatic "mirror" responses in the observers' motor system. However, in daily life, nonimitative actions are often required to be produced in response to others' acts, generating a conflict between automatic and voluntary responses. First, we used single-pulse transcranial magnetic stimulation (TMS) to assess the temporal dynamics of motor output in healthy volunteers preparing rule-based counter-imitative motor responses cued by different observed hand movements. Second, we applied the same paradigm after 1-Hz repetitive TMS (rTMS) of the left posterior parietal cortex (PPC) and of the left dorsolateral prefrontal cortex (dlPFC). The results showed an early (150 ms from onset of visual stimuli) stimulus-driven mirror response that was followed by a later (300 ms) rule-based nonmirror response. rTMS applied to the PPC modulated only the early mirror response. Conversely, rTMS to the dlPFC modulated specifically the late rule-based motor response. The data indicate that a fast bottom-up process mediated by the dorsal visual stream produces automatic imitative responses. Arbitrary rule-based visuomotor associations are on the contrary mediated by a slower system, relying on the prefrontal cortex. The 2 systems are mutually independent and compete for motor output in socially relevant situations only at a distal level.

Motor resonance meets motor performance

“…Previous research on neurophysiological data showed that motor resonance is more likely to appear in early time windows with respect to the onset of the observed action (Ubaldi et al, 2013). If data are in accordance with SM, then the accuracy of responses before motor resonance would be at chance both in the COUNTER and in the NEUTRAL task.…”

“…This assumption has its basis on previous work studying the cortical excitability of the motor system while performing tasks similar to the one used in the present work, both within the action observation domain Ubaldi et al, 2013) and within more general stimulus-response compatibility experiments (Michelet et al, 2010).…”

“…It is worth noticing that according to our previous works in the action observation domain Ubaldi et al, 2013) the duration of the persistence of an imitative motor pattern in the corticospinal system during a counter-imitative task is in the order of 100-150 ms. Such phenomenon has therefore an intrinsic temporal frequency of around 10 Hz.…”

“…The interest in this field has been prompted by the discovery of mirror neurons in the monkeys' premotor cortex 23 years ago (di Pellegrino et al, 1992;Gallese et al, 1996). Action observation has been studied with different techniques, both in monkeys and humans, showing that observing actions performed by others not only involves high-level visual representations but, more interestingly, it recruits representations that are active during the execution of motor acts thanks to an automatic visuo-motor transformation, called almost interchangeably "motor simulation", "motor resonance", or "mirror mechanism" (Avenanti et al, 2007;Cattaneo et al, 2009;Fadiga et al, 1995;Ubaldi et al, 2013).…”

“…Recently we proposed a model based on neurophysiological data that aimed to describe the evolving dynamics of the state of the motor system when participants observed an action in order to react to it following a rule-based visuo-motor matching (Ubaldi et al, 2013). Data showed that requiring the observers to react to an observed action with the opposite one (see action A-do action B, see action B-do action A), caused their motor system to react first by activating the motor representation correspondent to the action observed, and then by activating the task-required motor representation.…”