MEG Multivariate Analysis Reveals Early Abstract Action Representations in the Lateral Occipitotemporal Cortex

Understanding other people's actions is a fundamental prerequisite for social interactions. Whether action understanding relies on simulating the actions of others in the observers' motor system or on the access to conceptual knowledge stored in nonmotor areas is strongly debated. It has been argued previously that areas that play a crucial role in action understanding should (1) distinguish between different actions, (2) generalize across the ways in which actions are performed (Dinstein et al., 2008; Oosterhof et al., 2013; Caramazza et al., 2014), and (3) have access to action information around the time of action recognition (Hauk et al., 2008). Whereas previous studies focused on the first two criteria, little is known about the dynamics underlying action understanding. We examined which human brain regions are able to distinguish between pointing and grasping, regardless of reach direction (left or right) and effector (left or right hand), using multivariate pattern analysis of magnetoencephalography data. We show that the lateral occipitotemporal cortex (LOTC) has the earliest access to abstract action representations, which coincides with the time point from which there was enough information to allow discriminating between the two actions. By contrast, precentral regions, though recruited early, have access to such abstract representations substantially later. Our results demonstrate that in contrast to the LOTC, the early recruitment of precentral regions does not contain the detailed information that is required to recognize an action. We discuss previous theoretical claims of motor theories and how they are incompatible with our data.

SIGNIFICANCE STATEMENT It is debated whether our ability to understand other people's actions relies on the simulation of actions in the observers' motor system, or is based on access to conceptual knowledge stored in nonmotor areas. Here, using magnetoencephalography in combination with machine learning, we examined where in the brain and at which point in time it is possible to distinguish between pointing and grasping actions regardless of the way in which they are performed (effector, reach direction). We show that, in contrast to the predictions of motor theories of action understanding, the lateral occipitotemporal cortex has access to abstract action representations substantially earlier than precentral regions.