TMS highlights the functional relevance and malleability of cortico-cortical connections to motion and action perception

In social environments the human brain evolves systems to make sense of others’ actions and behaviours, allowing the development of social interactions and reactions. Influential theories posit that the understanding of others’ actions is realised through the activation of one’s motor system that internally simulates the kinematics of the ongoing action and predicts its sensorial outcome. This process engages an action observation network (AON) that encompasses temporal-occipital visual and parietal-frontal motor regions. The flowing visual information is coupled with motor representations through recursive bidirectional fronto-temporal interactions that are modelled by sensorimotor experience allegedly via Hebbian plastic mechanisms. However, to date there is no direct evidence on the role that connectivity plays in carrying crucial information for the AON functioning. Recent studies demonstrated the efficacy of a TMS protocol, named cortico-cortical paired associative stimulation (ccPAS), able to induce transient Hebbian-like plastic potentiation in motor neural circuits. For a mechanistic understanding of AON connections relevance for simulative processes and action prediction, we used ccPAS with the aim of empowering the synaptic efficacy of the connections between the nodes of the system. ccPAS impact on behaviour and neurophysiological responses was evaluated. On motor behaviour, a ccPAS to empower premotor-motor connectivity led to improved dexterity (Study I) revealing the circuit’s functional malleability. On low-level perception, ccPAS, boosting the re-entrant connectivity of visual cortices revealed changes in motion perception and in specific features of it (Studies II-III). We then demonstrated that premotor-motor circuit conveys crucial information for the motor simulation of observed movements (Study IV), and finally, that empowering feedback connectivity in the AON enhances action prediction accuracy (Study V). We therefore provided evidence on the functional relevance of AON connectivity that supports theoretical models, and we developed an innovative tool able to promote AON functionality by inducing plastic changes in its connections.