Gravity matters for the neural representations of action semantics.

Abstract

The dynamic relationship between the neural representation of action word semantics and specific sensorimotor experience remains controversial. Here, we temporarily altered human subjects' sensorimotor experience in a 15-day head-down tilt bed rest setting, a ground-based analog of microgravity that disproportionally affects sensorimotor experiences of the lower limbs, and examined whether such effector-dependent activity deprivation specifically affected the neural processes of comprehending verbs of lower-limb actions (e.g. to kick) relative to upper-limb ones (e.g. to pinch). Using functional magnetic resonance imaging, we compared the multivoxel neural patterns for such action words prior to and after bed rest. We found an effector-specific (lower vs. upper limb) experience modulation in subcortical sensorimotor-related and anterior temporal regions. The neural action semantic representations in other effector-specific verb semantic regions (e.g. left lateral posterior temporal cortex) and motor execution regions were robust against such experience alterations. These effector-specific, sensorimotor-experience-sensitive and experience-independent patterns of verb neural representation highlight the multidimensional and dynamic nature of semantic neural representation, and the broad influence of microgravity (hence gravity) environment on cognition.