Hierarchical Action Encoding Within the Human Brain

Abstract

Humans are able to interact with objects with extreme flexibility. To achieve this ability, the brain does not only control specific muscular patterns, but it also needs to represent the abstract goal of an action, irrespective of its implementation. It is debated, however, how abstract action goals are implemented in the brain. To address this question, we used multivariate pattern analysis of functional magnetic resonance imaging data. Human participants performed grasping actions (precision grip, whole hand grip) with two different wrist orientations (canonical, rotated), using either the left or right hand. This design permitted to investigate a hierarchical organization consisting of three levels of abstraction: 1) "concrete action" encoding; 2) "effector-dependent goal" encoding (invariant to wrist orientation); and 3) "effector-independent goal" encoding (invariant to effector and wrist orientation). We found that motor cortices hosted joint encoding of concrete actions and of effector-dependent goals, while the parietal lobe housed a convergence of all three representations, comprising action goals within and across effectors. The left lateral occipito-temporal cortex showed effector-independent goal encoding, but no convergence across the three levels of representation. Our results support a hierarchical organization of action encoding, shedding light on the neural substrates supporting the extraordinary flexibility of human hand behavior.

Keywords: MVPA; action; fMRI; grasping; motor system.