Tool-use brain representations are independent of the acting body part and motor experience

Abstract

The sensorimotor system is broadly organized somatotopically. However, an action-type organization has also been found: a division based on action-type independent of acting body parts has been shown for reaching and grasping actions. Does this generalization extend to non-ethological actions? Here, we examined fMRI responses for tool-use actions that participants performed with their hands or feet. We additionally tested individuals born without hands to control for hand motor imagery when performing foot actions. We show that the primary sensorimotor cortices have hand and foot selectivity, consistent with a somatotopic organization. In contrast, higher-level motor areas within the tool-use network, such as the premotor cortex, supplementary motor area, and superior parietal cortices, showed a shared preference for tool-use independent of the executing body part and sensorimotor experience. Multivariate decoding of action-type in these areas generalized between controls hand and foot and was successful in individuals born without hands. Finally, the temporal dynamics pattern in primary and association areas carried effector-specific and action-type information, respectively. Altogether, we show that the tool-use network in motor association areas represents higher-order action information beyond concrete motor parameters associated with specific effectors, and regardless of hand motor experience. This suggests that an action-type, effector-independent organization extends beyond ethological actions, supporting a hierarchical organization in the action domain. Further, it shows that functional organization in congenital handlessness is based on the hierarchical organization of the intact cortex.