Common and distinct brain regions processing multisensory bodily signals for peripersonal space and body ownership

We take the feeling that our body belongs to us for granted. However, recent research has shown that it is possible to alter the subjective sensation of body ownership (BO) by manipulating multisensory bodily inputs. Several frontal and parietal regions are known to specifically process multisensory cues presented close to the body, i.e., within the peripersonal space (PPS). It has been proposed that these PPS fronto-parietal regions also underlie BO. However, most previous studies investigated the brain mechanisms of either BO or of PPS processing separately and by using a variety of paradigms. Here, we conducted an extensive meta-analysis of functional neuroimaging studies to investigate PPS and BO processing in humans in order to: a) assess quantitatively where each one of these functions was individually processed in the brain; b) identify whether and where these processes shared common or engaged distinct brain mechanisms; c) characterize these areas in terms of whole-brain co-activation networks and functions, respectively. We identified (i) a bilateral PPS network including superior parietal, temporo-parietal and ventral premotor regions and (ii) a BO network including posterior parietal cortex (right intraparietal sulcus, IPS; and left IPS and superior parietal lobule, SPL), right ventral premotor cortex, and the left anterior insula. Co-activation maps related to both PPS and BO encompassed largely overlapping fronto-parietal networks, but whereas the PPS network was more frequently associated with sensorimotor tasks, the BO network was rather associated with attention and awareness tasks. Finally, the conjunction analysis showed that (iii) PPS and BO tasks anatomically overlapped only in two clusters located in the left parietal cortex (dorsally at the intersection between the SPL, the IPS and area 2 and ventrally between areas 2 and IPS). Distinct activations were located for PPS at the temporo-parietal junction and for BO in the anterior insula. These results in PPS and BO and provide evidence-based insight about the overlap of the two processes in the IPS region and the extensive connectivity between the two associated co-activation networks. They also show significant dissociations, with PPS fronto-parietal areas located more proximal to the central sulcus than BO areas. Such anatomical distinction may also reflect the different functions of the two processes, whereby PPS areas underlie a multisensory-motor interface for body-objects interaction and BO areas being involved in bodily awareness and self-consciousness.

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

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

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.