Subcortical contributions to the sense of body ownership.

The sense of body ownership (i.e. the feeling that our body or its parts belong to us) plays a key role in bodily self-consciousness and is believed to stem from multisensory integration. Experimental paradigms such as the rubber hand illusion have been developed to allow the controlled manipulation of body ownership in laboratory settings, providing effective tools for investigating malleability in the sense of body ownership and the boundaries that distinguish self from other. Neuroimaging studies of body ownership converge on the involvement of several cortical regions, including the premotor cortex and posterior parietal cortex. However, relatively less attention has been paid to subcortical structures that may also contribute to body ownership perception, such as the cerebellum and putamen. Here, on the basis of neuroimaging and neuropsychological observations, we provide an overview of relevant subcortical regions and consider their potential role in generating and maintaining a sense of ownership over the body. We also suggest novel avenues for future research targeting the role of subcortical regions in making sense of the body as our own.

Sense of own body shapes neural processes of memory encoding and reinstatement.

How is the fundamental sense of one's body, a basic aspect of selfhood, incorporated into memories for events? Disrupting bodily self-awareness during encoding impairs functioning of the left posterior hippocampus during retrieval, which implies weakened encoding. However, how changes in bodily self-awareness influence neural encoding is unknown. We investigated how the sense of body ownership, a core aspect of the bodily self, impacts encoding in the left posterior hippocampus and additional core memory regions including the angular gyrus. Furthermore, we assessed the degree to which memories are reinstated according to body ownership during encoding and vividness during retrieval as a measure of memory strength. We immersed participants in naturalistic scenes where events unfolded while we manipulated feelings of body ownership with a full-body-illusion during functional magnetic resonance imaging scanning. One week later, participants retrieved memories for the videos during functional magnetic resonance imaging scanning. A whole brain analysis revealed that patterns of activity in regions including the right hippocampus and angular gyrus distinguished between events encoded with strong versus weak body ownership. A planned region-of-interest analysis showed that patterns of activity in the left posterior hippocampus specifically could predict body ownership during memory encoding. Using the wider network of regions sensitive to body ownership during encoding and the left posterior hippocampus as separate regions-of-interest, we observed that patterns of activity present at encoding were reinstated more during the retrieval of events encoded with strong body ownership and high memory vividness. Our results demonstrate how the sense of physical self is bound within an event during encoding, which facilitates reactivation of a memory trace during retrieval.

Texture congruence modulates perceptual bias but not sensitivity to visuotactile stimulation during the rubber hand illusion.

The sense of body ownership is the feeling that one's body belongs to oneself. To study body ownership, researchers use bodily illusions, such as the rubber hand illusion (RHI), which involves experiencing a visible rubber hand as part of one's body when the rubber hand is stroked simultaneously with the hidden real hand. The RHI is based on a combination of vision, touch, and proprioceptive information following the principles of multisensory integration. It has been posited that texture incongruence between rubber hand and real hand weakens the RHI, but the underlying mechanisms remain poorly understood. To investigate this, we recently developed a novel psychophysical RHI paradigm. Based on fitting psychometric functions, we discovered the RHI resulted in shifts in the point of subjective equality when the rubber hand and the real hand were stroked with matching materials. We analysed these datasets further by using signal detection theory analysis, which distinguishes between the participants' sensitivity to visuotactile stimulation and the associated perceptual bias. We found that texture incongruence influences the RHI's perceptual bias but not its sensitivity to visuotactile stimulation. We observed that the texture congruence bias effect was the strongest in shorter visuotactile asynchronies (50-100 ms) and weaker in longer asynchronies (200 ms). These results suggest texture-related perceptual bias is most prominent when the illusion's sensitivity is at its lowest. Our findings shed light on the intricate interactions between top-down and bottom-up processes in body ownership, the links between body ownership and multisensory integration, and the impact of texture congruence on the RHI.

Active self-touch restores bodily proprioceptive spatial awareness following disruption by 'rubber hand illusion'.

Bodily self-awareness relies on a constant integration of visual, tactile, proprioceptive, and motor signals. In the 'rubber hand illusion' (RHI), conflicting visuo-tactile stimuli lead to changes in self-awareness. It remains unclear whether other, somatic signals could compensate for the alterations in self-awareness caused by visual information about the body. Here, we used the RHI in combination with robot-mediated self-touch to systematically investigate the role of tactile, proprioceptive and motor signals in maintaining and restoring bodily self-awareness. Participants moved the handle of a leader robot with their right hand and simultaneously received corresponding tactile feedback on their left hand from a follower robot. This self-touch stimulation was performed either before or after the induction of a classical RHI. Across three experiments, active self-touch delivered after-but not before-the RHI, significantly reduced the proprioceptive drift caused by RHI, supporting a restorative role of active self-touch on bodily self-awareness. The effect was not present during involuntary self-touch. Unimodal control conditions confirmed that both tactile and motor components of self-touch were necessary to restore bodily self-awareness. We hypothesize that active self-touch transiently boosts the precision of proprioceptive representation of the touched body part, thus counteracting the visual capture effects that underlie the RHI.

Body ownership and kinaesthetic illusions: Dissociated bodily experiences for distinct levels of body consciousness?

Seeing an embodied humanoid avatar move its arms can induce in the observer the illusion that its own (static) arms are moving accordingly, the kinematic signals emanating from this avatar thus being considered like those from the biological body. Here, we investigated the causal relationship between these kinaesthetic illusions and the illusion of body ownership, manipulated through visuomotor synchronisation. The results of two experiments revealed that the sense of body ownership over an avatar seen from a first-person perspective was intimately linked to visuomotor synchrony. This was not the case for kinaesthetic illusions indicating that when superimposed on the biological body, the avatar is inevitably treated at the sensorimotor level as one's own body, whether consciously considered as such or not. The question of whether these two bodily experiences (body ownership and kinaesthetic illusion) are underpinned by distinct representations, the body image, and the body schema, is discussed.

Malleability of the sense of bodily self in early childhood: 5- and 6-year-old children show the enfacement illusion.

The mechanisms underlying the developing sense of bodily self are debated. Whereas some scholars stress the role of sensory factors, others propose the importance of contextual factors. By manipulating multisensory stimulation and social familiarity with the other person, we explored two factors that are proposed to relate to young children's developing sense of bodily self. Including an adult sample allowed us to investigate age-related differences of the malleability of the bodily self. To this end, the study implemented an enfacement illusion with children (N = 64) and adults (N = 33). Participants were exposed to one trial with synchronous interpersonal multisensory stimulation and one trial with asynchronous interpersonal multisensory stimulation-either with a stranger or with the mother as the other person. A self-recognition task using morph videos of self and other and an enfacement questionnaire were implemented as dependent measures. Results revealed evidence for the presence of the enfacement effect in children in both measures. The identity of the other person had a significant effect on the self-recognition task. Contrary to our hypothesis, the effect was significantly smaller in the caregiver condition. No significant differences between children and adults emerged. Our results demonstrate the role of both multisensory stimulation and contextual-here social familiarity-factors for the construction and development of a bodily self. The study provides developmental science with a novel approach to the bodily self by showing the validity of the self-recognition task in a child sample. Overall, the study supports proposals that the sense of bodily self is malleable early in development.

Body Evaluation and Body Ownership in Patients with Inflammatory Bowel Disease: the Role of Interoceptive Sensibility and Childhood Maltreatment.

OBJECTIVE: Inflammatory bowel diseases (IBD) are accompanied by symptoms that can vastly affect patients' representations of their bodies. The aim of this study was to investigate alterations in body evaluation and body ownership in IBD and their link to interoceptive sensibility, gastrointestinal-specific anxiety, and history of childhood maltreatment. METHODS: Body evaluation and ownership was assessed in 41 clinically remitted patients with IBD and 44 healthy controls (HC) using a topographical self-report method. Interoceptive sensibility, gastrointestinal-specific anxiety and a history of childhood maltreatment were assessed via self-report questionnaires. RESULTS: Patients reporting higher interoceptive sensibility perceived their bodies in a more positive manner. Higher gastrointestinal-specific anxiety was linked to a more negative body evaluation particularly of the abdomen in patients with IBD. Childhood maltreatment severity strengthened the positive association between interoceptive sensibility and body ownership only in those patients reporting higher trauma load. CONCLUSION: Altered body representations of areas associated with abdominal pain are linked to higher symptom-specific anxiety and lower levels of interoceptive sensibility in IBD. Particularly in patients with a history of childhood maltreatment, higher levels of interoceptive sensibility might have a beneficial effect on the patients' sense of body ownership.

Disentangling the neural correlates of agency, ownership and multisensory processing.

The experience of the self as an embodied agent in the world is an essential aspect of human consciousness. This experience arises from the feeling of control over one's bodily actions, termed the Sense of Agency, and the feeling that the body belongs to the self, Body Ownership. Despite longstanding philosophical and scientific interest in the relationship between the body and brain, the neural systems involved in Body Ownership and Sense of Agency, and especially their interactions, are not yet understood. In this preregistered study using the Moving Rubber Hand Illusion inside an MR-scanner, we aimed to uncover the relationship between Body Ownership and Sense of Agency in the human brain. Importantly, by using both visuomotor and visuotactile stimulations and measuring online trial-by-trial fluctuations in the illusion magnitude, we were able to disentangle brain systems related to objective sensory stimulation and subjective judgments of the bodily-self. Our results indicate that at both the behavioral and neural levels, Body Ownership and Sense of Agency are strongly interrelated. Multisensory regions in the occipital and fronto-parietal regions encoded convergence of sensory stimulation conditions. The subjective judgments of the bodily-self were related to BOLD fluctuations in the Somatosensory cortex and in regions not activated by the sensory conditions, such as the insular cortex and precuneus. Our results highlight the convergence of multisensory processing in specific neural systems for both Body Ownership and Sense of Agency with partially dissociable regions for subjective judgments in regions of the Default Mode Network.

Synchronous motor imagery and visual feedback of finger movement elicit the moving rubber hand illusion, at least in illusion-susceptible individuals.

Recent evidence suggests that imagined auditory and visual sensory stimuli can be integrated with real sensory information from a different sensory modality to change the perception of external events via cross-modal multisensory integration mechanisms. Here, we explored whether imagined voluntary movements can integrate visual and proprioceptive cues to change how we perceive our own limbs in space. Participants viewed a robotic hand wearing a glove repetitively moving its right index finger up and down at a frequency of 1 Hz, while they imagined executing the corresponding movements synchronously or asynchronously (kinesthetic-motor imagery); electromyography (EMG) from the participants' right index flexor muscle confirmed that the participants kept their hand relaxed while imagining the movements. The questionnaire results revealed that the synchronously imagined movements elicited illusory ownership and a sense of agency over the moving robotic hand-the moving rubber hand illusion-compared with asynchronously imagined movements; individuals who affirmed experiencing the illusion with real synchronous movement also did so with synchronous imagined movements. The results from a proprioceptive drift task further demonstrated a shift in the perceived location of the participants' real hand toward the robotic hand in the synchronous versus the asynchronous motor imagery condition. These results suggest that kinesthetic motor imagery can be used to replace veridical congruent somatosensory feedback from a moving finger in the moving rubber hand illusion to trigger illusory body ownership and agency, but only if the temporal congruence rule of the illusion is obeyed. This observation extends previous studies on the integration of mental imagery and sensory perception to the case of multisensory bodily awareness, which has potentially important implications for research into embodiment of brain-computer interface controlled robotic prostheses and computer-generated limbs in virtual reality.

Self-touch facilitates the recognition of the dis-owned left hand in somatoparaphrenia: a single case study.

We investigated whether self-administered tactile stimulation could act as a temporary restorative mechanism for body ownership disorders, both implicitly and explicitly. We tested this hypothesis in a patient with somatoparaphrenia, who displayed increased accuracy in explicitly recognizing their left hand during self-touch. Furthermore, the patient implicitly perceived their hand and the experimenter's hand as more belonging to their own body compared to conditions where vision was the sole sensory input. These findings highlight the importance of self-touch in maintaining a coherent body representation, while also demonstrating the potential dissociation between the recovery of explicit and implicit perceptions of body ownership.

Splitting the Unity of Bodily Self: Toward a Comprehensive Review of Phenomenology and Psychopathology of Heautoscopy.

BACKGROUND: Heautoscopy refers to a pathological experience of visual reduplication of one's body with an ambiguous sense of self-location and a disturbing sensation of owning the illusory body. It has been recognized to occur in the course of strikingly diverse psychiatric and neurological disorders, such as schizophrenia, space-occupying lesions, frequently of the temporal or parietal lobes, migraine, epilepsy, and depression. The literature on the subject suffers from numerous conceptual inconsistencies, scarcity of clinical data, and a lack of theoretical integratory framework that could explain the uniqueness of these symptoms. AIMS: In the study, we aimed to review all case reports on heautoscopy we could cull from the literature with an attempt to extract common factors and to foster a theoretical synthesis. METHODS: All medical and psychological databases were rigorously searched, along with reference lists of the preselected articles. First-person reports were classified according to aspects of bodily self-consciousness primarily affected: body ownership, self-location, sense of agency and consequently, collated with their etiological backgrounds. RESULTS: Out of over 140 case studies, a total of only 9 patients with heautoscopy were selected as satisfying functional criteria, carefully distinguishing heautoscopy from other typically conflated full-body anomalies: autoscopy, out-of-body experience, or feeling of presence. Numerous cases turned out to be mislabeling autoscopy or out-of-body experience as heautoscopy. In addition, several problems with existing neuroimaging experiments were identified. CONCLUSION: Phenomenological analysis revealed that from the patients' perspective, heautoscopy resembles a somatesthetic-proprioceptive illusion, rather than a cognitive delusion, and occurs much less frequently than reported. A most peculiar symptom, described by some as a sense of "bilocation," appears to stem from dynamic shifts in self-location and expanded body ownership, rather than an expanded first-person perspective. Although extremely rare in its pure form, heautoscopy gives a unique opportunity to explore the brain limits to the plasticity of bodily boundaries and the origin of the first-person spatial perspective.

The role of visual expectations in acupuncture analgesia: A quantitative electroencephalography study.

Acupuncture is a complex treatment comprising multisensory stimulation, including visual and tactile sensations and experiences of body ownership. The purpose of this study was to investigate the role of these three components of acupuncture stimulation in acupuncture analgesia. 40 healthy volunteers participated in the study and received acupuncture treatment under three different conditions (real-hand, rubber-hand synchronous, and rubber-hand asynchronous). The tolerance for heat pain stimuli was measured before and after treatment. Brain oscillation changes were also measured using electroencephalography (EEG). The pain tolerance was significantly increased after acupuncture treatment under all three conditions. Noticeable deqi (needle) sensations in response to acupuncture stimulation of the rubber hand were found under both rubber-hand synchronous and rubber-hand asynchronous conditions. Deqi sensations were significantly correlated with acupuncture analgesia only under the rubber-hand synchronous condition. Increased delta and decreased theta, alpha, beta, and gamma waves were observed after acupuncture treatment under all three conditions. Our findings clarified the role of cognitive components of acupuncture treatment in acupuncture analgesia through the rubber-hand illusion. This study is a first step toward separating various components of acupuncture analgesia, i.e. visual, tactile, and body ownership, and utilizing those components to maximize analgesic effects.

Bodily self-recognition in patients with pathological embodiment.

The ability to discriminate between one's own and others' body parts can be lost after brain damage, as in patients who misidentify someone else's hand as their own (pathological embodiment). Surprisingly, these patients do not use visual information to discriminate between the own and the alien hand. We asked whether this impaired visual discrimination emerges only in the ecological evaluation when the pathological embodiment is triggered by the physical alien hand (the examiner's one) or whether it emerges also when hand images are displayed on a screen. Forty right brain-damaged patients, with (E+ = 20) and without (E- = 20) pathological embodiment, and 24 healthy controls underwent two tasks in which stimuli depicting self and other hands was adopted. In the Implicit task, where participants judged which of two images matched a central target, the self-advantage (better performance with Self than Other stimuli) selectively emerges in controls, but not in patients. Moreover, E+ patients show a significantly lower performance with respect to both controls and E- patients, whereas E- patients were comparable to controls. In the Explicit task, where participants judged which stimuli belonged to themselves, both E- and E+ patients performed worst when compared to controls, but only E+ patients hyper-attributed others' hand to themselves (i.e., false alarms) as observed during the ecological evaluation. The VLSM revealed that SLF damage was significantly associated with the tendency of committing false alarm errors. We demonstrate that, in E+ patients, the ability to visually recognize the own body is lost, at both implicit and explicit level.

The relationship between the effect of hand visibility on visuotactile temporal resolution and autistic traits.

Individuals with autism spectrum disorder (ASD) have atypical sensory processing, particularly when sensory stimuli are delivered from different modalities with a temporal lag of subseconds. Previous studies have suggested that individuals with ASD require a longer temporal lag to judge temporal orders of successive audiovisual stimuli than neurotypical individuals; however, it remains unclear whether a lower temporal resolution in the visuotactile domain is associated with an individual's autistic traits. In addition, a previous study demonstrated that visuotactile temporal resolution degraded when the participants saw a hand image on a display. In this study, we investigated whether the temporal resolution of the visuotactile stimuli degrades when the participant's own hand or rubber hands are visible, and whether the effect of the hand's visibility on the temporal resolution decreases according to an individual's autistic traits. We used the temporal order judgment (TOJ) of the vibrotactile stimulus delivered to the participant's index finger and an LED attached above their own hand or rubber hand. Our findings suggest that when participants could not see their hand, temporal order judgment tended to be coarser in participants with higher autistic traits. However, this tendency was not observed when they could see both their own or the rubber hands. Moreover, temporal resolution degraded when the participants could see their own hands. These results indicate that autistic traits influence the temporal resolution of visuotactile stimuli if they are delivered as external signals in TOJ.

Understanding components of embodiment: Evidence from the mirror box illusion.

Past studies have examined embodiment in the rubber hand illusion, using principal components analysis (PCA) to identify factors from questionnaire responses during synchronous and asynchronous stroking. To better understand the phenomenology of embodiment, we used PCA in the mirror box illusion to examine performance across conditions that varied in movement synchrony to examine multisensory integration and movement type to vary the amount of multisensory congruence. We found three dissociable components in all conditions: embodiment, deafference and attentiveness. We also examined how these embodiment ratings varied across the four conditions. As hypothesized, embodiment ratings were highest for synchronous movement, with feelings of deafference highest for asynchronous movement. Furthermore, there was a movement by timing interaction, such that sliding resulted in greater differences in synchronous versus asynchronous ratings than tapping. These results suggest that embodiment or deafference can be changed as a function of the amount of multisensory congruence.

Tactile temporal order judgment during rubber hand illusion: Distinct modulation of the point of subjective simultaneity and temporal resolution.

During the rubber hand illusion (RHI), individuals feel a fake hand as their own (ownership) and a perceived position of their real hand shifts toward the fake hand (proprioceptive drift; PD), which represents updating of multisensory hand representations. Bimanual tactile temporal order judgment (TOJ) includes processes of localizing tactile stimuli in space, for which multisensory hand representations are essential. According to the common processes, we examined tactile TOJ performance during the RHI and non-RHI. Temporal resolution (TR) as TOJ accuracy worsened during the non-RHI compared to the RHI. Additionally, a significant correlation between TR and PD was observed only in the non-RHI condition. However, the point of subjective simultaneity (PSS), which offers relative weighting of tactile inputs from the right and left hands, was correlated with illusory hand ownership. These results suggest that PSS and TR from tactile TOJ during RHI relate to self-attribution and localization of the hand, respectively.

Exploring the development of high-level contributions to body representation using the rubber hand illusion and the monkey hand illusion.

During development our body undergoes significant changes, yet we are able to maintain a coherent experience of our body and sense of self. Bodily experience is thought to comprise integration of multisensory signals (vision, touch, and proprioception) constrained by top-down knowledge of body appearance. Evidence from developmental studies suggests that low-level multisensory integration develops throughout childhood, reaching adult levels by 10 years of age. However, how high-level cognitive knowledge changes during childhood to constrain our multisensory body experience is unknown. This study describes four experiments examining high-level contributions to the bodily experience in children compared with adults using the rubber hand illusion and a monkey hand illusion. We found that children (5-17 years of age) exhibited more flexible body representations, showing stronger illusions for small and fantastical (monkey) fake hands compared with adults. Conversely, using a task indirectly capturing changes in hand size, we found that children and adults demonstrated statistically equivalent increases and decreases in hand size following illusions over large and small hands, respectively. Interestingly, at baseline children showed a bias in reporting larger hand size judgments that decreased with age. Finally, we did not find a relationship between individual differences in fantasy proneness and illusion strength for a fantastical (monkey) hand for children or adults, suggesting that developmental changes of top-down constraints are not purely driven by more diffuse boundaries between imagination and reality. These data suggest that high-level constraints acting on our multisensory body experience change during development, allowing children a more flexible bodily experience compared with adults.

Agency and responsibility over virtual movements controlled through different paradigms of brain-computer interface.

KEY POINTS: Embodiment of a virtual body was induced and its movements were controlled by two different brain-computer interface (BCI) paradigms - one based on signals from sensorimotor versus one from visual cortical areas. BCI-control of movements engenders agency, but not equally for all paradigms. Cortical sensorimotor activation correlates with agency and responsibility. This has significant implications for neurological rehabilitation and neuroethics. ABSTRACT: Agency is the attribution of an action to the self and is a prerequisite for experiencing responsibility over its consequences. Here we investigated agency and responsibility by studying the control of movements of an embodied avatar, via brain-computer interface (BCI) technology, in immersive virtual reality. After induction of virtual body ownership by visuomotor correlations, healthy participants performed a motor task with their virtual body. We compared the passive observation of the subject's 'own' virtual arm performing the task with (1) the control of the movement through activation of sensorimotor areas (motor imagery) and (2) the control of the movement through activation of visual areas (steady-state visually evoked potentials). The latter two conditions were carried out using a BCI and both shared the intention and the resulting action. We found that BCI-control of movements engenders the sense of agency, which is strongest for sensorimotor area activation. Furthermore, increased activity of sensorimotor areas, as measured using EEG, correlates with levels of agency and responsibility. We discuss the implications of these results for the neural basis of agency.

I'm a believer: Illusory self-generated touch elicits sensory attenuation and somatosensory evoked potentials similar to the real self-touch.

Sensory attenuation (i.e., the phenomenon whereby self-produced sensations are perceived as less intense compared to externally occurring ones) is among the neurocognitive processes that help distinguishing ourselves from others. It is thought to be rooted in the motor system (e.g., related to motor intention and prediction), while the role of body awareness, which necessarily accompanies any voluntary movement, in this phenomenon is largely unknown. To fill this gap, here we compared the perceived intensity, somatosensory evoked potentials, and alpha-band desynchronization for self-generated, other-generated, and embodied-fake-hand-generated somatosensory stimuli. We showed that sensory attenuation triggered by the own hand and by the embodied fake hand had the same behavioral and neurophysiological signatures (reduced subjective intensity, reduced of N140 and P200 SEP components and post-stimulus alpha-band desynchronization). Therefore, signals subserving body ownership influenced attenuation of somatosensory stimuli, possibly in a postdictive manner. This indicates that body ownership is crucial for distinguishing the source of the perceived sensations.

Little evidence for an effect of the rubber hand illusion on basic movement.

Body ownership refers to the distinct sensation that our observed body belongs to us, which is believed to stem from multisensory integration. This is commonly shown through the rubber hand illusion (RHI), which induces a sense of ownership over a false limb. Whilst the RHI may interfere with object-directed action and alter motor cortical activity, it is not yet clear whether a sense of ownership over an artificial hand has functional consequences for movement production per se. As such, we performed two motion-tracking experiments (n = 117) to examine the effects of the RHI on the reaction time, acceleration, and velocity of rapid index finger abduction. We observed little convincing evidence that the induction of the RHI altered these kinematic variables. Moreover, the subjective sensations of rubber hand ownership, referral of touch, and agency did not convincingly correlate with kinematic variables, and nor did proprioceptive drift, suggesting that changes in body representation elicited by the RHI may not influence basic movement. Whilst experiment 1 suggested that individuals reporting a greater sensation of the real hand disappearing performed movements with smaller acceleration and velocity following illusion induction, we did not replicate this effect in a second experiment, suggesting that these effects may be small or not particularly robust. Overall, these results indicate that manipulating the conscious experience of body ownership has little impact on basic motor control, at least in the RHI with healthy participants.