TMS-induced control of bodily self-consciousness by combining non-invasive brain stimulation and immersive virtual reality

Our brain constantly receives and integrates a flow of sensory and motor information that shapes the way our body is represented. Several experimental approaches have been proposed to alter the body representation, by manipulating exteroceptive or interoceptive bodily signals. During my thesis, I studied the contribution of central, rather than peripheral, motor brain mechanisms underlying bodily self-consciousness (BSC). For this purpose, I attempted to manipulate BSC, specifically inducing embodiment for a fake hand in healthy participants, by using a novel method that combines non-invasive transcranial magnetic stimulation (TMS) with immersive virtual reality (VR). First, we managed to induce embodiment for a virtual hand utilizing the spatio-temporal coherence between an artificial TMS-induced activation of the motor system and movement-related visual feedback in VR (Study 1). I observed that embodiment for a virtual hand was induced only when the provided stimulation is supra-threshold but not when TMS is delivered sub-threshold. I argue that such TMS-induced illusory embodiment is due to neuro-visual integration between TMS-induced primary motor cortex (M1) activation and hand twitches with visual VR feedback. In a second study (Study 2), by refining the parameters of our TMS-VR protocol we investigated the different peripheral components elicited by TMS with a special focus on hand perception. Our data revealed the main features of TMS-evoked hand perceptions (in terms of threshold and evoked subjective perceptions) and show that these are discernible from MEPs and TMS-evoked movements associated with single-pulse TMS over M1. Finally, we combined the TMS-VR setup (Study 1) and our stimulation protocol (Study 2) to investigate whether the awareness of peripheral bodily stimuli is necessary to induce changes in BSC (Study 3). Our findings reveal a prominent role of conscious bodily perceptions in triggering illusory embodiment, even in the absence of peripheral stimuli. Furthermore, I have been involved in other projects investigating the plasticity of body and space representation in healthy young and elderly participants (listed in appendix 1 & 2) and the robotically controlled induction of presence hallucinations (appendix 3). The present work provides important findings and promising tools regarding the role of non-invasive brain stimulation and virtual technology in the study of BSC. In particular, I showed that it is possible to manipulate BSC by directly stimulating the M1 cortical representation of the hand inducing embodiment for a virtual hand. Furthermore, I investigated the role of the TMS-evoked hand sensations and their role in the embodiment showing that the hand ownership is mainly driven by the detection of TMS stimuli on the hand.

Bodily self and human grid cell-like activity: probing spatial representation with immersive virtual reality

Hyukjun Moon

Grid cells are place-modulated neurons that encode the location of an agent in space, relying on the integration of various sensorimotor signals from the body. Of note, the integration of those signals is also fundamental for the agent's conscious experience of selfhood, referred to as bodily self-consciousness (BSC). Although both grid cells and BSC systems are related to the brain mechanisms of self-location and are based on multimodal signal integration, their interplay has never been investigated. My thesis aimed at revealing their links in humans by assessing the impact of BSC modulations on grid cell-like representation (GCLR): an fMRI proxy of grid cell activity in entorhinal cortex (EC). In Study 1, I assessed whether manipulation on BSC, specifically enhancing self-identification, affects GCLR during spatial navigation in a virtual reality (VR) environment. I implemented a novel fMRI paradigm integrating a spatial navigation task with online BSC manipulation through a motion-mimicking avatar. The data showed a significant reduction of GCLR as well as improved spatial navigation performance in the condition with the self-identified avatar, linking entorhinal grid cell activity and BSC through bodily self-motion cues provided online during spatial navigation. These behavioral and neural changes were further associated with increased activity in posterior parietal and retrosplenial cortex, collectively suggesting the impact of BSC on a distributed spatial navigation networks in the human brain. Consistent with the previous BSC research, in Study1, I observed illusory drifts in experienced self-location toward the self-identified avatar. In Study2, I further investigated whether illusory self-location changes would be sufficient to elicit GCLR in the absence of active spatial navigation. Adopting the Full-body illusion (FBI) paradigm to the MRI scanner, my data extend changes in self-location related to multisensory stimulation and demonstrated that these indeed evoke GCLR. Although the amplitude of GCLR during the FBI was smaller than the one during virtual navigation, their grid orientations were similar. These data suggest that the brain mechanisms underlying the BSC-induced illusory self-location are similar and comparable, albeit weaker, to the ones during virtual navigation.Temporal Interference (TI) stimulation is a novel method that can excite or inhibit neurons in the deep brain by combining high-frequency electrical fields. Building on the previous studies, in study3, I probed the causal link between GCLR and spatial navigation by applying TI stimulation to EC of participants while they were performing a VR navigation task in the scanner. The preliminary results showed that their spatial navigation was improved by excitatory stimuli compared to the control, while it deteriorated during the inhibition. Besides, I found that modulated GCLR was also associated with improved performance in the excitatory condition. Together, these data provide the first causal link between GCLR and spatial navigation, showing potential future avenues for navigation enhancement in humans. To summarize, I investigated BSC and grid cell systems jointly in humans and, for the first time, uncovered their links through robust evidence based on both behavioral and neuroimaging data. My thesis shed new light on the research of both systems which are closely intermingled but have hitherto been considered separately.

EPFL2021

Turning Body and Self Inside Out

Lukas Heydrich

What is the self? This major philosophical question has been considered too complex to be studied in neuroscience. However, during the last 20 years, researchers from different disciplines within the cognitive neurosciences have started investigating the neural correlates of self-consciousness, using a range of behavioural paradigms and functional imaging techniques. Where as many researchers have studied highorder representational aspects of self-consciousness, such as language (i.e. the use of the self-referential pronoun "I" or "Me"), converging evidence suggests that the most basic sense of self, e.g. the sensation that we possess a stable and coherent representation of our body, that we identify with our body and that we perceive the self as being located within the bodily boundaries (e.g. bodily self-consciousness), is due to integration of bodily signals from different exteroceptive sensory modalities (vision, touch, proprioception). Others have highlighted the importance signals related to internal signals (homeostasis, interoception) for self-consciousness. Using lesion analysis, we could demonstrate a causal link between damage to the right temporo-parietal junction and an altered state of bodily self-consciousness, e.g out-of-body experiences. This was confirmed using functional magnetic resonance imaging, multisensory exteroceptive conflicts and virtual reality: if healthy participants perceived themselves as "disembodied", activity in the same cortical region (i.e. temporo-parietal junction) was systematically modulated. Moreover, we were able to demonstrate in a second line of experiments that interoceptive signals can be used to systematically alter bodily self-consciousness and somatosensory processing, extending previous paradigms that focused exclusively on exteroceptive signals. This was strengthened by our finding that the left posterior insula, repeatedly linked to the representation and integration of internal and external bodily signals, is implicated in another state of altered bodily self-consciousness, e.g. heautoscopy. Our results demonstrate that bodily self-consciousness is based on a neural network that represents and integrates both external and internal signals from the body.

EPFL2012

Visuo-vestibular mechanisms of bodily self-consciousness

Joachim Jean-Marie Forget

Bodily self-consciousness is linked to multisensory integration and is particularly dependent on vestibular perception providing the brain with the main sensory cues about body motion and location in space. Vestibular and visual inputs are permanently balanced and integrated to encode the most optimal representation of the external world and of the observer in the central nervous system. Vection, an illusory self-motion experience induced only by visual stimuli, illustrates the fact that the visual and the vestibular systems share common neural underpinnings and a similar phenomenology. Optokinetic stimulation inducing vection and direct vestibular stimulation induce whole-body motion sensations that can be used to explore multisensory interactions. A failure in visuo-vestibular integration, artificially induced by the methods of cognitive psychology or in pathological conditions, has also been reported to altered own body perception and bodily self-consciousness. The respective contributions of the vestibular and visual systems to bodily self-consciousness amongst other polymodal sensory mechanisms, and the neural correlates of visuo-vestibular convergence, should be better understood. We first performed a neuroimaging study of brain regions where optokinetic and vestibular stimuli converge, using 7T functional magnetic resonance imaging in individual subjects. We identified three main regions of convergence: (1) the depth of supramarginal gyrus or retroinsular cortex, (2) the surface of supramarginal gyrus at the temporo-parietal junction, (3) and the posterior part of middle temporal gyrus and superior temporal sulcus. Then, we aimed to induce the embodiment of an external fake rubber hand through visuo-tactile conflict - the so-called rubber hand illusion paradigm, and studied how this integration is modulated by vection. Subjects experiencing vection in the direction of the rubber hand mislocalised the position of their real hand towards the rubber hand indicating that visuo-vestibular stimuli can enhance visuo-tactile integration. We also investigated if visuo-proprioceptive and tactile integration in peripersonal space could be dynamically updated based on the congruency of visual and proprioceptive feedback. A pair of rubber hands or feet provided visual feedback. Fake and real limbs were crossed or uncrossed. We showed that sensory cues were integrated in peripersonal space, dynamically reshaped but only for hands. Finally, we investigated a rare case of an illusory own body perception in an epileptic patient suffering from multiple daily disembodiments during seizures. Seizures were associated to a focal cortical microdysplasia juxtaposed to a developmental venous anomaly in the left angular gyrus, a brain region known to be important for visuo-vestibular integration and bodily self-consciousness. Our results characterize the inferior parietal lobule as a crucial structure in merging visual, vestibular, tactile and proprioceptive inputs, allowing the emergence of the global and unified experience of being âI.â Multisensory body representation can be reshaped transiently using visual and vestibular signals or in relation to a medical condition affecting the temporo-parietal junction. The integration of visual and vestibular signals, aims to adapt dynamically our internal representations to constant changes occurring in our environment.

EPFL2015