M1 large-scale network dynamics support human motor resonance and its plastic reshaping

• Published in: NeuroImage (Orlando, Fla.) Vol. 308; p. 121082
• Main Authors: Guidali, Giacomo, Arrigoni, Eleonora, Bolognini, Nadia, Pisoni, Alberto
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.03.2025; Elsevier Limited; Elsevier
• Subjects: Action observation network; Adult; Association Learning - physiology; Associative learning; Cognition; Communication; Connectivity; Contraindications; Cortex (motor); EEG; Electroencephalography; Evoked Potentials, Motor - physiology; Excitability; Female; Humans; Life span; Magnetic fields; Male; Motor Cortex - physiology; Motor resonance; Motor skill learning; Motor task performance; Nerve Net - physiology; Neural networks; Neuronal Plasticity - physiology; Paired associative stimulation; Sensorimotor integration; Sensorimotor system; Social interactions; Social organization; Statistical power; Synchronization; TMS-EEG; Transcranial Magnetic Stimulation; Visual stimuli; Young Adult; Connectivity; TMS-EEG; Motor resonance; Action observation network; Paired associative stimulation
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2025.121082

•Visuomotor PAS drives the emergence of atypical corticospinal motor resonance at the cost of the typical response.•Typical motor resonance is characterized by prominent alpha-band and reduced beta-band M1-connectivity.•PAS-induced motor resonance is specifically supported by beta-band M1 cortical networks.•Sensorimotor learning within the action observation network exploits connectivity mechanisms distinct from those established throughout lifetime experience. Motor resonance – the facilitation of corticospinal excitability during action observation – is considered a proxy of Action Observation Network (AON) recruitment in humans, 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 neural mechanisms underlying the motor resonance phenomenon. 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 AON.