Cortical kinematic processing of executed and observed goal-directed hand actions

• ¹ Université Libre de Bruxelles, Belgium
• ² Aalto University, School of Science, Finland

Purpose Motor information conveyed by viewing the kinematics of an agent’s action helps to predict how the action will unfold. Still, how observed movement kinematics is processed in the brain remains to be clarified. Here, we used magnetic source imaging to investigate at which frequencies and where in the brain significant coupling occurs between cortical activity and the kinematics of both executed and observed repetitive goal-directed hand movements. Furthermore, we investigate whether rolandic mu rhythm is dynamically modulated by the movement kinematics. Methods We recorded 306-channel magnetoencephalography (MEG; Elekta Oy; 0.1–330 Hz, sampled at 1 kHz) data from 11 right-handed healthy subjects (6 F, 5 M; mean age 31.1 yrs) during two conditions (Self and Other), each lasting 5 min. During Self, subjects pinched one-by-one green foam-made pieces mixed in a heap with pieces of other colors placed on the MEG table, and put them in a plastic pot placed on the right of the heap. During Other, subjects watched an actor performing the same task sitting at 1.5 m in front of them (factor hidden by a screen). Subjects and actor’s forefinger movements were monitored with a 3-axis accelerometer (Acc). Electromyograms (EMG) were recorded from the subjects’ and actor’s first dorsal interosseous and extensor digitorum communis muscles bilaterally. Subjects’ heartbeat, eye-blink, and eye-movement artifacts were subtracted from MEG data with an independent-component-analysis-based method. Coherence was computed between the Euclidian norm of Acc signals and the MEG sensors signals (CohMEG) as well as their envelopes of α (8¬–12 Hz, Cohα) and β (15–25 Hz, Cohβ) bands using 3-s epochs. Cortical sources coherent with Acc signals were identified using dynamic imaging of coherent sources (Gross et al. PNAS 2001). Coherence was computed between subjects’ rectified EMG signals and subjects’ (Self) or actor’s (Other) Acc signals. Results At the sensor level, statistically significant (p < 0.05, surrogate-data-based statistics) CohMEG peaked at movement frequency (F0) in 11 subjects and its first harmonic (F1) in 10 subjects in both movement conditions. Cohα peaked at movement frequency (F0) in 5 subjects during Self and in 4 subjects during Other, while significant Cohβ peaked at F0 in 8 subjects during Self and in 6 subjects during Other. Apart from visual cortices, source reconstruction and group-level analysis identified for CohMEG statistically significant (p < 0.05, permutation statistics) coherent local maxima in the right posterior superior temporal gyrus (F0), bilateral primary sensorimotor (SM1) hand areas (F0 or F1) and posterior parietal cortices (F0 or F1) in both movement conditions. Significant coherence local maxima were found at bilateral SM1 hand areas for Cohβ during both Self and Other whereas no significant Cohα was found. EMG–Acc coherence analysis demonstrated the absence of subjects’ movements in phase with actor’s movements in Other. Conclusion This study suggests the activation of a dorsal visuo-sensorimotor stream for the kinematic representation of executed and observed goal-directed hand actions. These data demonstrates that observing others’ action engages—in the viewer’s brain—similar kinematics-related dynamic modulation of SM1 activity as during identical action execution. These kinematics-related phenomena might help to better understand how an observed action is performed. Présentation Les informations motrices provenant de l’observation de la cinématique de l’action d’un tiers aident à prédire comment cette action se déroulera. Cependant la manière dont la cinématique d’un mouvement observé est traitée dans le cerveau reste à éclaircir. Nous avons ici utilisé la magnétoencéphalographie pour étudier à quelles fréquences et à quels endroits se produit dans le cerveau un couplage significatif entre l’activité corticale et la cinématique d’un mouvement répétitif de la main dirigé vers un but , mouvement tour à tour exécuté et observé par un sujet. Nous avons en outre étudié si le rythme mu est modulé par la cinématique du mouvement.