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.

No abstract

As a part of self-consciousness, sense of agency (SoA) refers to our sensation that we initiate actions that lead to ensuing perceptual consequences. Previous neuroimaging studies manipulated voluntary actions to create differential levels of SoA, and found that the SoA network largely overlaps with the sensorimotor network. It is thus unclear whether effects observed in these regions are attributable to SoA or some specific aspects of action processes (e.g., intentionality of action) related to voluntary action control, or both. To disentangle the effect of action processes, here we utilized virtual reality (VR) technology to induce an illusive SoA in the absence of voluntary action, and examined it by functional magnetic resonance imaging (fMRI). Participants' experience of controlling an avatar hand elicited a persistent increase in temporal binding, a behavioral marker of SoA, when they merely observed the avatar hand's movement in the scanner. fMRI results showed that the SoA with the non-action was associated with a cluster centered in right angular gyrus, extending to right inferior parietal lobule and the right precuneus. These high-level associative areas have been implicated in SoA with voluntary actions for their role in perceptual-motor mismatch detection and action awareness. Other traditional SoA areas, especially those governing action intentionality and motor planning, were not implicated. Hence, controlling a virtual body can generate a salient SoA whose neural correlates are distinct from those supporting action control but partially overlapping with those governing post voluntary-action SoA processes. These findings also highlight the role of angular gyrus in giving rise to the self-consciousness changes associated with virtual body embodiment in VR and metaverse.