An intracranial insight into (the timing of) the action observation network

Abstract

The Action Observation Network (AON) is a large-scale brain network that supports the perceptual encoding and recognition of actions performed by others. The identification of the nodes of the human AON has been clarified over the past 30 years thanks to the high spatial resolution of neuroimaging techniques. The temporal dynamics underpinning their activations is in contrast still unsettled, because of methodological constraints. Here we investigate the timing of the AON components by intracranially recording gamma-band oscillations from 23 drug-resistant epileptic patients during the observation, and execution, of naturalistic, complex actions (including reaching, grasping, and object manipulation). Our analysis enabled us to decompose the AON into 10 distinct spatio-temporal clusters, five of which are composed of multiple cortical territories that are synergistically activated. The resulting four-dimensional representation of the AON, examined alongside its counterpart during the execution of the same action, highlights the specific functions fulfilled by each territory, distinguishing regions that process lower-order visual aspects from those that mirror specific aspects of the action. These include two spatio-temporal clusters located in dorsal and ventral fronto-parieto-temporal territories, specifically encoding the reaching phase (dorsal) and the object-contact phase (ventral). A third cluster, confined to the posterior perisylvian region, is associated with object manipulation. Overall, our work brings out the overlooked temporal details of the AON in humans and assesses their relationship with the execution of a real-time full-fledged action, spotlighting the importance of a fourth dimension in investigating the motor system.