Spatiotemporal Brain Dynamics of Transitive and Intransitive Action Observation

Abstract

Observing another person's action recruits the action observation network (AON). Evidence suggests that distinct AON pathways are engaged depending on action features, such as their transitivity or the movement's target; however, the spatiotemporal dynamics of these circuitries remain unclear and debated. In the present study, to further explore this aspect, healthy participants completed two experiments involving the passive observation of distinct grasping actions: intransitive (isolated grasp), object-directed (hand grasping a bottle), and socially-directed (hand grasping another person's hand). In Experiment 1, using electroencephalography (EEG), we examined whole-brain temporal patterns of AON activation during the observation of these stimuli through event-related potentials and microstate analyses. In Experiment 2, informed by EEG results, we used transcranial magnetic stimulation (TMS) to assess the temporal dynamics of motor resonance, a corticospinal marker of AON recruitment. Experiment 1 showed that observing transitive and intransitive grasping activates the same core circuit within the AON, albeit with distinct spatiotemporal dynamics emerging in two separate time windows, peaking at approximately 200 and 350 ms after action onset. Specifically, observation of object-directed grasping relies more on the engagement of posterior brain regions. In contrast, intransitive and socially-directed movements recruit anterior areas more quickly, with the activation pattern of the latter class of stimuli likely reflecting the additional visuo-tactile processing associated with the observed action. Experiment 2 showed muscle-specific motor resonance at 200 ms only for intransitive and object-directed grasping, but no corticospinal facilitation at later latencies, where inhibitory patterns instead emerged, suggesting that EEG and TMS capture complementary dynamics underlying action observation and understanding. Overall, our findings suggest that observing transitive and intransitive movements modulates AON activity through shared pathways expressed in specific spatiotemporal gradients, corresponding to distinct cortical and corticospinal signatures that encode the features of the observed action.