Action-type mapping principles extend beyond evolutionarily conserved actions, even in people born without hands

Abstract

How are actions represented in the motor system? Although the sensorimotor system is broadly organized somatotopically, higher-level sensorimotor areas encode action-type information for reaching and grasping actions—regardless of the acting body part. Does the brain similarly support generalization across acting body parts for more evolutionarily recent actions, such as tool-use? We tested whether there is a body-part-independent action-type organization in sensorimotor areas by examining fMRI responses for tool-use actions that participants performed with their hands or feet. We additionally included individuals born without hands to test whether hand sensorimotor experience is necessary for the development of this action-type organization. Across analyses, we found a consistent dissociation in the motor system. The primary sensorimotor cortices encoded concrete, body-part specific information in both groups. In contrast, higher-level motor areas within the tool-use network represent abstract, action-type information independent of the body part for both groups. Together, our results suggest that the hierarchical organization of the motor system is not dependent on a long evolutionary history of an action. Further, this organization is not dependent on an individual’s manual sensorimotor experience. Our results also show that the functional reorganization in congenital handlessness follows the hierarchical organization of the intact cortex, revealing the limitations of brain plasticity. Finally, the results support using a readout of a more abstract code for hierarchical brain–computer interfaces.