M1 Large-scale Network Dynamics Support Human Motor Resonance and Its Plastic Reshaping

Abstract

Motor resonance - the activation of the observers motor system when viewing others actions - grounds the intertwined nature of action perception and execution, with profound implications for social cognition and action understanding. Despite extensive research, the neural underpinnings supporting motor resonance emergence and rewriting remain unexplored. In this study, we investigated the role of sensorimotor associative learning in motor resonance neural mechanisms. To this aim, we applied cross-systems paired associative stimulation (PAS) to induce novel visuomotor associations in the human brain. This protocol, which repeatedly pairs transcranial magnetic stimulation (TMS) pulses over the primary motor cortex (M1) with visual stimuli of actions, drives the emergence of an atypical, PAS-conditioned motor resonance response. Using TMS and electroencephalography (EEG) co-registration during action observation, we tracked the M1 functional connectivity profile during this process to map the inter-areal connectivity profiles associated with typical and PAS-induced motor resonance phenomena. Besides confirming, at the corticospinal level, the emergence of newly acquired motor resonance responses at the cost of typical ones after PAS administration, our results reveal dissociable aspects of motor resonance in M1 interregional communication. On the one side, typical motor resonance effects acquired through the lifespan are associated with prominent M1 alpha-band and reduced beta-band connectivity, which might facilitate the corticospinal output while integrating visuomotor information. Conversely, the atypical PAS-induced motor resonance is linked to M1 beta-band cortical connectivity modulations, only partially overlapping with interregional communication patterns related to the typical mirroring responses. This evidence suggests that beta-phase synchronization may be the critical mechanism supporting the formation of motor resonance by coordinating the activity of motor regions during action observation, which also involves alpha-band top-down control of frontal areas. These findings provide new insights into the neural dynamics underlying (typical and newly acquired) motor resonance, highlighting the role of large-scale interregional communication in sensorimotor associative learning within the action observation network.