Limb ownership and voluntary action: human behavioral and neuroimaging studies

Abstract: To be able to interact with our surroundings in a goal directed manner, we need to have sense what our body is made up of as well as a sense of being able to control our body. These two experiences, the sense of body ownership and the sense of agency, respectively, are fundamental to our self-perception but have historically not received any notable attention from the scientific community. This lack of interest probably stems from the fact that these experiences are phenomenologically thin in our everyday lives and that we cannot voluntarily turn them off, they are constantly there. However, for patients suffering from disturbances in the processes underlying these experiences, their importance becomes exceedingly clear. Lesions in the frontal, temporal or parietal lobe can lead to patients losing the sense of ownership of their limb (asomatognosia), and sometimes even attributing the limb to someone else (somatoparaphrenia). Similarly, patients suffering from lesions in the frontal lobe, parietal lobe or corpus callosum can experience a lack of control over their own hand (anarchic hand syndrome), while patients suffering from schizophrenia display difficulties in distinguishing self-generated from externally generated actions, implicating disturbances in the processes underlying the sense of agency. With the discovery of body illusions, combined with functional neuroimaging, it became possible to study the perceptual and neural mechanisms of the sense of body ownership in healthy volunteers. Studies using these illusions have elucidated the perceptual rules of body ownership as well as its neural correlates and has given rise to a number of different philosophical, neurocognitive and computational models of the sense of body ownership. Meanwhile, the sense of agency has mostly been studied disconnected from the sense of body ownership, focusing on agency over self-generated external sensory effects such as auditory tones. This thesis sought to bring these two experiences together and advance our knowledge of the perceptual and neural mechanisms underlying the sense of body ownership and the sense of agency as well how these two experiences interact. Studies I & II investigate certain aspects of the sense of body ownership, and in particular its relation to the visuo-proprioceptive recalibration of limb position often seen in bodily illusions. Study III investigated how this visuo-proprioceptive recalibration is related to voluntary, but unconscious movements. Study IV investigated the neural correlates of the sense of body ownership and agency as well as their interaction. In Study I, we present empirical evidence in favor of models where the subjective sense of limb ownership is not reliant on a visuo-proprioceptive recalibration of perceived limb position. In Study II, we show that the subjective sense of limb ownership and the visuo-proprioceptive recalibration of limb position have similar temporal decay curves, suggestive of a causal relationship between them. In Study III, we show that the increase in the recalibration of limb position seen in active movements is not dependent on conscious intention, action awareness or salient error signals, indicative of an unconscious efference copy-based mechanism. Finally, in Study IV, we identify brain regions in the frontal and parietal lobe which are associated with the sense of body ownership, while brain regions in the frontal and temporal lobe are associated with the sense of agency. We show that the sense of agency in the presence of a sense of body ownership (i.e., agency of bodily actions) is associated with increased activity in the primary sensory cortex, whereas the sense of agency in the absence of ownership (i.e., agency of external events) is associated with increased activity in the visual association cortex. Together, these findings shed light on the perceptual and neural mechanisms underlying the sense of body ownership and agency as well as their interaction.