Right insular damage decreases heartbeat awareness and alters cardio-visual effects on bodily self-consciousness

Recent evidence suggests that multisensory integration of bodily signals involving exteroceptive or interoceptive information modulates bodily aspects of self-consciousness such as self-identification and self-location. In the so-called full body illusion subjects watch a virtual body being stroked while they perceive tactile stimulation on their own body inducing illusory self-identification with the virtual body and a change in self-location towards the virtual body. In a related illusion, it has recently been shown that similar changes in self-identification and self-location can be observed when an interoceptive signal is used in association with visual stimulation of the virtual body (i.e., participants observe a virtual body illuminated in synchrony with their heartbeat). Although brain imaging and neuropsychological evidence suggest that the insular cortex is a core region for interoceptive processing (such as cardiac perception and awareness) as well as for self-consciousness, it is currently not known whether the insula mediates cardio-visual modulation of self-consciousness. Here we tested the involvement of insular cortex in heartbeat awareness and cardio-visual manipulation of bodily self-consciousness in a patient before and after resection of a selective right neoplastic insular lesion. Cardio-visual stimulation induced an enhanced alteration of bodily self-consciousness; in addition, cardio-visual manipulation was associated with an experienced loss of the spatial unity of the self (illusory bi-location and duplication of his body), not observed in healthy subjects. Heartbeat awareness was found to decrease after insular resection. Based on these data we propose that the insula mediates interoceptive awareness as well as cardio-visual effects on bodily self-consciousness and that insular processing of interoceptive signals is an important mechanism for the experienced unity of the self.

Interoception and Empathy Impact Perspective Taking

Jane Aspell, Olaf Blanke, Bruno Herbelin, Lukas Heydrich

Adopting the perspective of another person is an important aspect of social cognition and has been shown to depend on multisensory signals from one's own body. Recent work suggests that interoceptive signals not only contribute to own-body perception and self-consciousness, but also to empathy. Here we investigated if social cognition - in particular adopting the perspective of another person - can be altered by a systematic manipulation of interoceptive cues and further, if this effect depends on empathic ability. The own-body transformation task (OBT) - wherein participants are instructed to imagine taking the perspective and position of a virtual body presented on a computer screen - offers an effective way to measure reaction time differences linked to the mental effort of taking an other's perspective. Here, we adapted the OBT with the flashing of a silhouette surrounding the virtual body, either synchronously or asynchronously with the timing of participants' heartbeats. We evaluated the impact of this cardio-visual synchrony on reaction times and accuracy rates in the OBT. Empathy was assessed with the empathy quotient (EQ) questionnaire. Based on previous work using the cardio-visual paradigm, we predicted that synchronous (vs. asynchronous) cardio-visual stimulation would increase self-identification with the virtual body and facilitate participants' ability to adopt the virtual body's perspective, thereby enhancing performance on the task, particularly in participants with higher empathy scores. We report that participants with high empathy showed significantly better performance during the OBT task during synchronous versus asynchronous cardio-visual stimulation. Moreover, we found a significant positive correlation between empathic ability and the synchrony effect (the difference in reaction times between the asynchronous and synchronous conditions). We conclude that synchronous cardio-visual stimulation between the participant's body and a virtual body during an OBT task makes it easier to adopt the virtual body's perspective, presumably based on multisensory integration processes. However, this effect depended on empathic ability, suggesting that empathy, interoception and social perspective taking are inherently linked.

2021

Neuroscience robotics to investigate multisensory integration and bodily awareness

Olaf Blanke, Dominique Chapuis, Julio Duenas, Roger Gassert, Silvio Ionta, Roberto Martuzzi, Christian Pfeiffer

Humans experience the self as localized within their body. This aspect of bodily self-consciousness can be experimentally manipulated by exposing individuals to conflicting multisensory input, or can be abnormal following focal brain injury. Recent technological developments helped to unravel some of the mechanisms underlying multisensory integration and self-location, but the neural underpinnings are still under investigation, and the manual application of stimuli resulted in large variability difficult to control. This paper presents the development and evaluation of an MR-compatible stroking device capable of presenting moving tactile stimuli to both legs and the back of participants lying on a scanner bed while acquiring functional neuroimaging data. The platform consists of four independent stroking devices with a travel of 16-20 cm and a maximum stroking velocity of 15 cm/s, actuated over non-magnetic ultrasonic motors. Complemented with virtual reality, this setup provides a unique research platform allowing to investigate multisensory integration and its effects on self-location under well-controlled experimental conditions. The MR-compatibility of the system was evaluated in both a 3 and a 7 Tesla scanner and showed negligible interference with brain imaging. In a preliminary study using a prototype device with only one tactile stimulator, fMRI data acquired on 12 healthy participants showed visuo-tactile synchrony-related and body-specific modulations of the brain activity in bilateral temporoparietal cortex.

2012

Distinct illusory own-body perceptions caused by damage to posterior insula and extrastriate cortex

Olaf Blanke, Lukas Heydrich

Recent research in cognitive neuroscience using virtual reality, robotic technology and brain imaging has linked self-consciousness to the processing and integration of multisensory bodily signals. This work on bodily self-consciousness has implicated the temporo-parietal, premotor and extrastriate cortex and partly originated in work on neurological patients with different disorders of bodily self-consciousness. One class of such disorders is autoscopic phenomena, which are defined as illusory own-body perceptions, during which patients experience the visual illusory reduplication of their own body in extrapersonal space. Three main forms of autoscopic phenomena have been defined. During autoscopic hallucinations, a second own body is seen without any changes in bodily self-consciousness. During out-of-body experiences, the second own body is seen from an elevated perspective and location associated with disembodiment. During heautoscopy, subjects report strong self-identification with the second own body, often associated with the experience of existing at and perceiving the world from two places at the same time. Although it has been proposed that each autoscopic phenomenon is associated with different impairments of bodily self-consciousness, past research on neurological patients and the development of experimental paradigms for the study of bodily self-consciousness has focused on out-of-body experiences and the association with temporo-parietal cortex. Here, we performed quantitative lesion analysis in the-to date-largest group of patients with autoscopic hallucination and heautoscopy and compared the location of brain damage with those of control patients suffering from complex visual hallucinations. We found that heautoscopy was associated with lesions to the left posterior insula, and that autoscopic hallucinations were associated with damage to the right occipital cortex. Autoscopic hallucination and heautoscopy were further associated with distinct symptoms and deficits. The present data suggest that the autoscopic hallucination is a visuo-somatosensory deficit implicating extrastriate cortex and is, despite the visual hallucination of the own body, not associated with major deficits in bodily self-consciousness. Based on the symptoms and deficits in patients with heautoscopy and the implication of the left posterior insula, we suggest that abnormal bodily self-consciousness during heautoscopy is caused by a breakdown of self-other discrimination regarding affective somatosensory experience due to a disintegration of visuo-somatosensory signals with emotional (and/or interoceptive) bodily signals. These brain mechanisms are distinct from those described for out-of-body experiences. The present data extend previous models of autoscopic phenomena and provide clinical evidence for the importance of emotional and interoceptive signal processing in the posterior insula in relation to bodily self-consciousness.