Neural Substrates of Body Ownership and Agency during Voluntary Movement.

Body ownership and the sense of agency are two central aspects of bodily self-consciousness. While multiple neuroimaging studies have investigated the neural correlates of body ownership and agency separately, few studies have investigated the relationship between these two aspects during voluntary movement when such experiences naturally combine. By eliciting the moving rubber hand illusion with active or passive finger movements during functional magnetic resonance imaging, we isolated activations reflecting the sense of body ownership and agency, respectively, as well as their interaction, and assessed their overlap and anatomic segregation. We found that perceived hand ownership was associated with activity in premotor, posterior parietal, and cerebellar regions, whereas the sense of agency over the movements of the hand was related to activity in the dorsal premotor cortex and superior temporal cortex. Moreover, one section of the dorsal premotor cortex showed overlapping activity for ownership and agency, and somatosensory cortical activity reflected the interaction of ownership and agency with higher activity when both agency and ownership were experienced. We further found that activations previously attributed to agency in the left insular cortex and right temporoparietal junction reflected the synchrony or asynchrony of visuoproprioceptive stimuli rather than agency. Collectively, these results reveal the neural bases of agency and ownership during voluntary movement. Although the neural representations of these two experiences are largely distinct, there are interactions and functional neuroanatomical overlap during their combination, which has bearing on theories on bodily self-consciousness.SIGNIFICANCE STATEMENT How does the brain generate the sense of being in control of bodily movement (agency) and the sense that body parts belong to one's body (body ownership)? Using fMRI and a bodily illusion triggered by movement, we found that agency is associated with activity in premotor cortex and temporal cortex, and body ownership with activity in premotor, posterior parietal, and cerebellar regions. The activations reflecting the two sensations were largely distinct, but there was overlap in premotor cortex and an interaction in somatosensory cortex. These findings advance our understanding of the neural bases of and interplay between agency and body ownership during voluntary movement, which has implications for the development of advanced controllable prosthetic limbs that feel like real limbs.

Recalibration of hand position sense during unconscious active and passive movement.

Precise knowledge of one's limbs' position in space is fundamental for goal-directed action. The brain's representation of the body in space is thought to be generated through a process of multisensory integration of visual, tactile and proprioceptive signals. In this study, we devised a setup that allowed us to displace participants' right hand without their subjective awareness. We accomplished this task by instructing the participants to view a live video feed of their hand from the first-person perspective. In the active condition, we used a sensorimotor illusion that caused the participants to actively but unknowingly displace their unseen right hand to a location 8 cm lateral to the image of their hand. In the passive condition, we mechanically displaced the participants' hand-at a slow, unnoticeable velocity-to the same location. We found that during active displacement, the participants indicated that the location of their hand was closer to the digital image of the hand rather than the veridical location of the hand, as compared with the passive condition, in which the participants indicated that the locations of their hand were closer to the actual location. These results indicated that, compared with passive displacement, active movements cause greater recalibration of the hand's spatial position and that the boosted spatial recalibration of hand position sense in the active task is driven by error-based sensorimotor corrections. These results have bearing on the perceptual mechanisms of recalibration of perceived limb location.

Patterns of neural activity in the human ventral premotor cortex reflect a whole-body multisensory percept.

Previous research has shown that the integration of multisensory signals from the body in fronto-parietal association areas underlies the perception of a body part as belonging to one's physical self. What are the neural mechanisms that enable the perception of one's entire body as a unified entity? In one behavioral and one fMRI multivoxel pattern analysis experiment, we used a full-body illusion to investigate how congruent visuo-tactile signals from a single body part facilitate the emergence of the sense of ownership of the entire body. To elicit this illusion, participants viewed the body of a mannequin from the first-person perspective via head-mounted displays while synchronous touches were applied to the hand, abdomen, or leg of the bodies of the participant and the mannequin; asynchronous visuo-tactile stimuli served as controls. The psychometric data indicated that the participants perceived ownership of the entire artificial body regardless of the body segment that received the synchronous visuo-tactile stimuli. Based on multivoxel pattern analysis, we found that the neural responses in the left ventral premotor cortex displayed illusion-specific activity patterns that generalized across all tested pairs of body parts. Crucially, a tripartite generalization analysis revealed the whole-body specificity of these premotor activity patterns. Finally, we also identified multivoxel patterns in the premotor, intraparietal, and lateral occipital cortices and in the putamen that reflected multisensory responses specific to individual body parts. Based on these results, we propose that the dynamic formation of a whole-body percept may be mediated by neuronal populations in the ventral premotor cortex that contain visuo-tactile receptive fields encompassing multiple body segments.

No causal link between changes in hand position sense and feeling of limb ownership in the rubber hand illusion.

The rubber hand illusion is a perceptual illusion in which participants experience an inanimate rubber hand as belonging to their own body. The illusion is elicited by synchronously stroking the rubber hand and the participant's real hand, which is hidden from sight. The feeling of owning the rubber hand is accompanied by changes in hand position sense (proprioception), so that when participants are asked to indicate the location of their (unseen) hand, they indicate that it is located closer to the rubber hand. This "proprioceptive drift" is the most widely used objective measure of the rubber hand illusion, and from a theoretical perspective, it suggests a close link between proprioception and the feeling of body ownership. However, the critical question of whether a causal relationship exists between changes in hand position sense and changes in limb ownership is unknown. Here we addressed this question by devising a novel setup that allowed us to mechanically manipulate the position of the participant's hand without the participant noticing, while the rubber hand illusion was being elicited. Our results showed that changing the sensed position closer to or farther away from the rubber hand did not change the strength of the rubber hand illusion. Thus, the illusion is not dependent on changes in hand position sense. This finding supports models of body ownership and central body representation that hold that proprioceptive drift and the subjective illusion are related to different central processes.

Illusory ownership of an invisible body reduces autonomic and subjective social anxiety responses.

What is it like to be invisible? This question has long fascinated man and has been the central theme of many classic literary works. Recent advances in materials science suggest that invisibility cloaking of the human body may be possible in the not-so-distant future. However, it remains unknown how invisibility affects body perception and embodied cognition. To address these questions, we developed a perceptual illusion of having an entire invisible body. Through a series of experiments, we characterized the multisensory rules that govern the elicitation of the illusion and show that the experience of having an invisible body reduces the social anxiety response to standing in front of an audience. This study provides an experimental model of what it is like to be invisible and shows that this experience affects bodily self-perception and social cognition.