Grasp-specific motor resonance is influenced by the visibility of the observed actor

Karen L Bunday, Roger N Lemon, James M Kilner, Marco Davare, Guy A Orban, Karen L Bunday, Roger N Lemon, James M Kilner, Marco Davare, Guy A Orban

Abstract

Motor resonance is the modulation of M1 corticospinal excitability induced by observation of others' actions. Recent brain imaging studies have revealed that viewing videos of grasping actions led to a differential activation of the ventral premotor cortex depending on whether the entire person is viewed versus only their disembodied hand. Here we used transcranial magnetic stimulation (TMS) to examine motor evoked potentials (MEPs) in the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) during observation of videos or static images in which a whole person or merely the hand was seen reaching and grasping a peanut (precision grip) or an apple (whole hand grasp). Participants were presented with six visual conditions in which visual stimuli (video vs static image), view (whole person vs hand) and grasp (precision grip vs whole hand grasp) were varied in a 2 × 2 × 2 factorial design. Observing videos, but not static images, of a hand grasping different objects resulted in a grasp-specific interaction, such that FDI and ADM MEPs were differentially modulated depending on the type of grasp being observed (precision grip vs whole hand grasp). This interaction was present when observing the hand acting, but not when observing the whole person acting. Additional experiments revealed that these results were unlikely to be due to the relative size of the hand being observed. Our results suggest that observation of videos rather than static images is critical for motor resonance. Importantly, observing the whole person performing the action abolished the grasp-specific effect, which could be due to a variety of PMv inputs converging on M1.

Keywords: Action observation; F5c; MEPs; Motor resonance; Videos.

Copyright © 2016 The Authors. Published by Elsevier Ltd.. All rights reserved.

Figures

Fig. 1
Fig. 1
Observed actions and experimental design. A. Observed actions shown in the videos and static images (frame depicts first contact with the object); hand alone grasping an apple (whole hand grasp), hand alone grasping a peanut (precision grip), whole person grasping an apple (whole hand grasp) and whole person grasping a peanut (precision grip). B. Experimental design showing 4 blocks containing a baseline without visual stimuli (15 MEPs evoked during rest periods), each condition (5 MEPs per condition) and the inter-trial interval (ITI) (15 MEPs evoked during this interval), with a final rest baseline (15 MEPs). Thus, in total an experiment consisted of 75 rest MEPs, 20 MEP per observation condition (160 in total for each muscle) and 60 ITI MEPs. C. An ITI preceded the video and image presentations. After a 5 sec delay (or 7 sec if TMS is given) the video began; the object is presented, followed by reaching to the object, contact of the hand with the object and grasping and lift off. TMS was given at object contact (2500 msec). The video ended at 4500 msec. The static image was presented for 4500 msec. TMS was given at 2750 msec (the average between precision grip and whole hand grasp contact).
Fig. 2
Fig. 2
Without visual stimuli and inter-trial-interval baseline MEPs. Group data showing the mean FDI (A) and ADM (B) amplitude of MEPs evoked in the baseline without visual stimuli (open circles) and inter-trial-interval (ITI) (closed triangles) periods, across each block. The baseline without visual stimuli MEPs were recorded just prior to each block, whilst ITI MEPs were recorded randomly within each observation block. The abscissa shows the block number (1, 2, 3, 4). The ordinate shows the mean MEP amplitude (mV). Note that the ITI MEPs are significantly larger than MEPs without visual stimuli. Error bars indicate SE. *p < .05.
Fig. 3
Fig. 3
Without visual stimuli and ITI Normalised MEPs during observation of videos and static images. Group data showing the mean FDI (closed circles) and ADM (open circles) MEP size during observation of precision grip and whole hand grasp when subjects viewed videos (A, C), or static images (B, D) of precision grip and whole hand grasp. The abscissa shows the type of grasp observed (precision grip: PG, whole hand grasp: WHG). The ordinate shows MEP size expressed as a ratio of the MEP recorded during ITI (A, B) or trials without visual stimuli (C, D), where a value of 1 indicates that the baseline and observation MEPs were of equal amplitude. Note that when normalised to ITI trials, MEPs are suppressed compared with baseline ITI MEPs, whereas when normalised to trials without visual stimuli MEPs are facilitated. Error bars indicate SE. *p < .05.
Fig. 4
Fig. 4
ITI normalised MEPs during observation of hand alone and whole person. Group data showing the mean FDI (closed circles) and ADM (open circles) MEP size during observation when viewing only the hand (A) or the whole person (B; collapse across videos and images). The abscissa shows the type of grasp observed (precision grip: PG, whole hand grasp: WHG). The ordinate shows MEP size expressed as a ratio of the MEP recorded during ITI trials, where a value of 1 indicates that MEPs during the ITI and observation conditions were of equal amplitude. Note that during the hand alone videos, but not whole person videos, a significant grasp × muscle interaction is present. Error bars indicate SE. *p < .05.
Fig. 5
Fig. 5
ITI normalised MEPs during observation of hand and person videos. Group data showing the mean FDI (closed circles) and ADM (open circles) MEP size during observation of videos when viewing only the hand (A) or the person (B). The abscissa shows the type of grasp observed (precision grip: PG, whole hand grasp: WHG). The ordinate shows MEP size expressed as a ratio of the MEP recorded during ITI trials, where a value of 1 indicates that MEPs during the ITI and observation conditions were of equal amplitude. Note that during the hand videos, but not person videos, a significant grasp × muscle interaction is present. Error bars indicate SE. *p < .05.
Fig. 6
Fig. 6
ITI normalised MEPs during observation of hand alone and small hand alone videos. Group data showing the mean FDI (closed circles) and ADM (open circles) MEP size during observation of videos when viewing only the hand (A) or the person (B). The abscissa shows the type of grasp observed (precision grip: PG, whole hand grasp: WHG). The ordinate shows MEP size expressed as a ratio of the MEP recorded during ITI trials, where a value of 1 indicates that MEPs during the ITI and observation conditions were of equal amplitude. Note that during observation both the hand and small hand alone videos a significant grasp × muscle interaction is present. Error bars indicate SE. *p < .05.

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