Behavioral And Neural Representation Of Bodily Self-Awareness

The ownershipof one's own body is a pillar in the construction of self-consciousness.Having an accurate sense of the spatial boundaries of the body is a prerequisite forinteracting with the environment,and is thus essential for the survival of any organism witha central nervous system.In every second,our brain receivesmultisensory signals from the body across different sensory channels to dynamically construct and maintain a stable representation of the body.Over the last decades,body illusions have become a powerful tool forstudying the mechanisms underlying our sense of body ownership,in which the subjective perception of the body can be experimentally manipulated.Studies of such illusions have shown that multisensory integration withinthe peripersonal space is a key mechanism for bodily self-consciousness.However,it still remains unclear howwe estimate our body's position in space,and build the sense of body-ownership via integration of the internal body representation and external sensory information from multiple modalities.In this dissertation,we used a virtual reality system to induce a body illusionin both humans and macaque monkeys,and to investigate the neural mechanisms of body awareness,relying on a computational model-Bayesian Causal Inference?BCI?.The experimental setup allowed us to establish an objective and quantitative proxy for bodily self-awareness in both humans and macaques.Then,we used this setup toinvestigate putative neural circuits underlying bodily self-awareness in the macaque brain.The main results are summarized as follows:1.In human and monkey behavioral studies,we designed a virtual reality system based on previous human studies,in which a person could see an artificial arm replacing its own unseen arm.By manipulating the similarity?in shape and dynamics?between the illusory and the real arms,one could induce or break the illusion of ownership of the artificial hand.The key virtue of these studies is that breakdown of the illusion results in changes in the trajectory of reach.Our results showed that the exact same pattern of behaviors is observed in humans and monkeys in performing the same reaching task.Conditions that broke the illusion?as reported by humans?produced identical behavioral patterns in humans and monkeys.Without the inquiry directly through language about the introspective experience,this demonstrated,to our knowledge the best that can be done in non-human primates,thatmonkeys experience body illusions and ownership to an external entity much like humans do.2.Together with a hierarchical BCI model,we showed that the patterns of drift,and of P_com predicted by the BCI model in monkeys and humans exhibiteda similar dependence on disparity in both proprioceptive and visual information.In humans,the likelihood that proprioceptive and visual information was inferred to originate from the same?own?source(P_com)was tightly correlated with subjective reports of ownership.Thus,our first result established a tight quantitative relation between a subjective variable?the illusion?and behavior that could be observed in monkeys.3.We then used this objective measure of illusion strength to search for neurons that encoded body-awareness.We demonstrated that a set of neurons in the macaque premotor cortex,which were specifically tuned to integration or segregation of proprioceptive and visual information,encoded the likelihood that an object belonged to the self.4.By replacing the illusory?visual?arm with non-homomorphic objects in both human and monkey studies,we further confirmed a crucial prediction of this model,i.e.,when an artificial object which represents the arm is not homomorphic?i.e.it does not look like an arm?,the body illusion in humans breaks down rapidly even if its dynamics mirror the real arm.We showed that this manipulation also broke down the illusion in monkeys,and that activity of the same neuronal population in the premotor cortex failed to encode the representation of the visual illusion.5.Using a classical rubber hand illusion?RHI?paradigm,we found that both pain and unpleasantness ratings were significantly lower under the illusive condition than those under the other two control conditions,and this analgesic effect was positively correlated with the RHI.These results indicated that thealtered body ownership modulated pain perception.In summary,both behavioral and neural data in monkeys showed that the estimation of body position and the formation of body ownership were determined by both the external property of sensory inputs?the reliability of vision and proprioception,and the disparity between them?,and the internal prior body representation?the probability of visual and proprioceptive signals having the same cause?,and in turn,the change of body representation might influence the sensory reliability via a top-down modulation.