Where is my Mind? Separating the Self from the Body through Perspective Taking

Recent theories suggest that self-consciousness, in its most elementary form, is separate from the own body. Patients with psychosis frequently misattribute their thoughts and actions to external sources; and in certain out-of-body experiences, lucid states, and dreams body-ownership is absent but self-identification is preserved. We hypothesized that self-identification depends on inferring self-location at the right Angular Gyrus (perspective-taking). This process relates to the discrimination of self-produced signals (endogenous attention) from environmental stimulation (exogenous attention). We combined a Full-body Illusion paradigm with brain stimulation (HDtDCS) and found a clear causal association between right Angular Gyrus activation and alterations in self-location (perspective-taking). Anodal versus sham HD-tDCS resulted in: a more profound out-of-body shift (with reduced sense-of-agency); and a weakened ability to discriminate self from other perspectives. We conclude that self-identification is mediated in the brain by inferring self-location (perspective-taking). Self-identification can be decoupled from the bodily self, explaining phenomena associated with disembodiment. Introduction Recent theories suggest that self-consciousness, in its most elementary form, is separate from the own body (see discussion on Minimal Phenomenal Selfhood 1, 2). In out-of-body experiences the brain perceives the locus of the Self as being outside of the body (3); and in hallucinations and delusions thoughts and actions are frequently misattributed to external sources (see psychosis 4). Here, it is proposed that these forms of disembodiment arise by unusual right Angular Gyrus activation and failure of the brain to identify self-produced signals (resp. exogenous vs. endogenous attention 5, Fig. 1). To examine this hypothesis, we combined a full-body illusion paradigm with brain stimulation using high-definition tDCS. These paradigms manipulate bodyownership and offer a way to examine how (bodily) self-consciousness is constructed (1; for a critical review 6). In a typical full-body illusion people observe a virtual body a few feet in front of them through a Head-mounted Display. For a few minutes they see in front of them what they feel happening to them (e.g., back stroking). This leads people to identify with the virtual body and judge their spatial location to be closer to the external body than their actual location (7, 8). However, because of technical restrictions and safety issues, paradigms involving Head-mounted Displays are difficult to combine with existing neuroscience techniques. Due to this, the neural mechanisms underlying such illusions remain understudied (for one study 9). To address this problem, we developed a stereoscopic 3D-projection of a Full-body Illusion: video-captured images were LIVE-streamed to a computer and in real-time merged and projected onto a large screen. Unlike previous paradigms, this allowed us to simultaneously modify the brain function of healthy volunteers undergoing a full-body illusion and characterize the role of self-location, i.e., where someone experiences themselves to be. Previous studies have shown that electrical stimulation of the right Angular Gyrus induces out-of-body experiences (10, 11 & Penfield in 3); and hinders the recognition of self-produced signals and self-identification (12-14; also see 15). What connects these findings and the precise role of the right Angular Gyrus remains unclear. The brain's ability to recognize and discriminate self-produced signals from external stimulation is tied to the process of sensory gating. Sensory information is transformed in the brain through a complex system of gating steps that filter out irrelevant noise and excessive sensory information (16). When you lift your arm, for instance, efference copies are generated. Efference copies are neural representations or ‘copies’ of motor commands that travel to the sensory cortex and attenuate feedback stemming from our own sensory systems (see also comparator models 17). Sensory attenuation (18) thus informs the brain whenever it is stimulating itself, and accounts for why we cannot tickle ourselves (17, 19) and why we are unaware of our eye-saccades (20, 21). In psychosis these systems appear to be compromised (16). Recent studies (22-25) show that people who experience hallucinations and delusions are unable to monitor self-produced signals (prospective agency), but are able to compensate for this by relying on external cues to attribute actions to oneself (retrospective agency). A defect in predicting one’s own body signals thus causes the brain to no longer recognize being in control of them (sense-of-agency 26, 27), resulting in altered sensations and perceptions. Interestingly, recent studies in psychosis (25, 28) and Movement Disorders (29) report decreased and altered connectivity between the frontoparietal control network and the right Angular Gyrus. Furthermore, a recent meta-analysis of tDCS studies found a causal link between sense-of-agency and action selection in the dorsolateral prefrontal cortex (dlPFC) (30). It appears that exactly the inverse coupling between the dlPFC (endogenous attention) and the right Angular Gyrus (exogenous attention) is impaired in psychosis: when the brain selects a voluntary movement, the inhibitory control of the frontal cortex to the right Angular Gyrus is lost (25). These recently overlooked findings shed light on the origin of disembodied phenomena and neural basis of self-identification, see Fig. 1. Fig. 1. Endogenous (dorsal) versus Exogenous (ventral) Attention Systems. Dorsal (blue) and ventral (yellow) frontoparietal attention systems (as outlined by Corbetta & Schulman, 2002). Humans can perceive the world from different perspectives: from an endogenous (Self) versus exogenous (Other) focus of attention. Self-produced signals are predicted in the brain (e.g., by efference copies), whereas external signals are not. These predictions allow the brain to early discriminate self-produced signals from external stimulation and keep track of its own spatiotemporal location (perspective). Endogenous attention: the dorsal system is goal-directed and processes self-produced signals. ‘Cognitive control’ enables the top-down voluntary selection of stimuli and responses, resp.: dorsolateral prefrontal cortex (dlPFC), frontal eye field (FEF), intraparietal sulcus (IPS) & visual cortex. Exogenous attention * lateralized to the right hemisphere: the ventral system is stimulus-driven and processes external signals. ‘Stimulus control’ enables the automatic orientation and bottom-up detection of behaviorally relevant stimuli, resp.: visual cortex, angular gyrus (AG; as part of the larger temporoparietal junction) & the ventral frontal cortex. These attention systems keep external and self-produced signal processing separated and interconnect at the right AG (double arrow). At any given time, the right AG may orient attention outwards to salient or unexpected external events, acting as a ‘circuit breaker’ for the dorsal system; in return, when the dlPFC detects self-produced signals AG’s function is inhibited, silencing the ventral system. When this decoupling fails, self-produced signals are processed as if uncontrolled by oneself (e.g., delusion of control 4); and (over)stimulation of the right AG (e.g., electrical stimulation, epileptic seizures) results in signals being processed as if they are localized outside the own body (i.e., out-of-body experience). Endogenous = ‘of internal origin;’ exogenous = ‘of external origin.’ Figure adapted from (5). In the present study we sought to obtain direct evidence for a causal link between abnormal right Angular Gyrus activation and altered spatiotemporal self-location (perspective-taking). To achieve this, right Angular Gyrus function was systematically manipulated with high-definition transcranial direct current stimulation (HD-tDCS) while healthy volunteers (i) underwent a fullbody illusion, and (ii) carried out a perspective-taking task. It was hypothesized that anodal (vs. sham) right Angular Gyrus stimulation would: (i) make individuals feel more localized towards the virtual body; while (ii) reducing their ability to discriminate between perspectives. This setup allowed us to look at self-identification separately from body-ownership. Our results suggest that self-location (perspective-taking) is the key mechanism of self-identification. Results The experiment had two sessions that each included a (i) Full-body Illusion (FBI) paradigm; and a (ii) Self-Other perspective-taking (PT) task (i.e., Own-body Transformation (OBT) vs. control Lateralization (LAT) task 31). The two tasks were randomized and counterbalanced over HDtDCS conditions. This resulted in four experimental conditions: FBI-PT with active stimulation on Session 1 (FBI-PT 1) or Session 2 (FBI-PT 2); and PT-FBI with active stimulation on Session 1 (PT-FBI 1) or Session 2 (PT-FBI 2). Sham stimulation was presented on all other occasions. Thirty-six prescreened participants (see Materials and Methods) were randomly assigned to one of the four conditions, resulting in nine participants in each group. One participant was excluded from the FBI-analysis due to unforeseen technical problems (group PT-FBI 1; female; FBI N = 35). Two other participants were excluded from the PT-analysis because of chance-level performance (group PT-FBI 1 & FBI-PT 2; females; OBT & LAT N = 34). Occasional outliers in reaction times (< 1% data points LAT: RT < 160 ms / > 1000 ms; OBT: RT < 200 ms / > 2000 ms) and missing values (< 3 % data points PT-task) were replaced by mean values. Statistical analyses were performed in SPSS v25.0 and are reported using a 0.05 significance level. Full-body Illusion (FBI) Statistics pooled over the sessions revealed that the average reported displacement towards the projected image was 69.1 cm in Session 1 and 72.4 cm in