Top-down contextual requirement to suppress self-movement influences grasp-specific modulation of corticospinal excitability during action observation

Abstract

Action observation modulates corticospinal excitability (CSE) measured via transcranial magnetic stimulation (TMS) in humans, which presumably exposes the effect of mirror neuron activation on corticospinal pathways. These responses can consist of both facilitation and suppression, and the balance of these two may restrict the outflow of activity into movement. Evidence also suggests that task context can considerably influence CSE changes during action observation. Here, we assessed whether embedding action observation within a Go-NoGo paradigm, emphasizing movement withholding on observation and NoGo trials, influenced CSE modulation. Fourteen healthy subjects received single pulse TMS over left primary motor cortex (M1) during a baseline period, grasp observation onset, or after a NoGo cue, while performing, observing, or withholding two distinct reach-to-grasp actions. We assessed modulation of motor evoked potentials (MEPs) in three intrinsic hand muscles, which were recruited in a grasp-specific manner during action execution. CSE modulation was limited, and predominantly suppressive in nature during grasp observation. Seven subjects performed the same task without the NoGo condition ("Go-only" block) immediately before the "Go&NoGo" block. We found evidence for grasp-specific modulation of CSE, which matched the recruitment pattern of the muscles during action execution. Within these subjects, modulation was attenuated when the NoGo condition was introduced, but was still distinct from modulation in the first group. These results suggest that bottom-up grasp-specific modulation of MEPs during action observation is attenuated by the top-down contextual requirement to suppress self-movement, and facilitation and suppression effects are determined by the balance between these two processes. SIGNIFICANCE STATEMENTAction observation can activate specific pathways in the motor system of the observer, which are also used to perform the same action. This motor resonance, measured via changes in corticospinal excitability using transcranial magnetic stimulation, is susceptible to task context. In this study, we show that observing grasping actions results in grasp-specific changes in excitability, consistent with mirror neuron activation, but this effect is masked when observation is interleaved within a Go-NoGo paradigm, which emphasises suppression of ones own movement. Top-down task requirements to withhold movement within and across trials, which are present in most action observation studies, likely influence the extent of motor resonance, urging caution in the design and interpretation of results in TMS action observation experiments.