Neuroscience robotics to investigate multisensory integration and bodily awareness

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.

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

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

Olaf Blanke, Petr Grivaz, Andrea Serino

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.

Elsevier2017

Multisensory interactions in peripersonal space and their contributions to bodily self-consciousness

Petr Grivaz

What is the relevance of the body and body-transformed sensory information for subjective experience? In the last two decades, paradigms from cognitive neuroscience have demonstrated that the subjective sensations of possessing a body (body ownership, BO), of being located in space (self-location) and being directed at the world (first-person perspective, 1PP), crucially rely on and can be manipulated by exposure to conflicting sensory information in so called bodily illusions. These aspects of subjective experience that are attached to the body, or bodily self-consciousness (BSC), are therefore malleable in healthy participants and accessible to experimental manipulations. BSC is argued to rely on multisensory integration mechanisms within the space directly surrounding the body (i.e. the peripersonal space, PPS). Amply supported by behavioral evidence, data from the brain is sparse. To help elucidate, in terms of neural activity, the relationship between PPS and an aspect of BSC, namely BO, in the first part of my thesis, I will present the results from an fMRI study and a meta-analysis, whereby I globally show that visual and tactile information presented within PPS is processed predominantly within the fronto-parietal and temporo-parietal regions of the brain whereas BO is processed in fronto-parietal and insular regions. Critically, both PPS and BO processing converges only in the left superior parietal cortex (intraparietal sulcus and area 2), thus suggesting both a level of neural integration and dissociation. The subjective 1PP is also argued to rely on multisensory mechanisms and in particular vestibular signals, but the underlying behavioral and neural mechanisms remain largely unexplored. Thus, in the second part of my thesis, I present a behavioral study and a clinical case report. In the prior, we exposed healthy subjects in a supine posture to touch on their backs and synchronous or asynchronous touch on the back of an observed avatar. We further simulated visual gravity using virtual balls falling either in the same or opposite direction with respect to the pull of physical gravity. In line with our expectations, the latter biased the direction of the 1PP to that suggested by the visual gravity (thus subjects reported looking downwards). The visual gravity information also interacted with the synchrony of stroking to affect 1PP and a more frequent downward 1PP was associated with a higher self-elevation rating. Also in line with the idea that BSC and in particular the 1PP relies on multisensory (in particular visuo-vestibular) integration, in the clinical case report we describe a male patient with peripheral vestibulopathy experiencing out-of-body experiences, who fails to integrate visual and vestibular information and is sensitive to visuo-tactile conflicts in bodily illusions. The results from my thesis collectively reinforce the current view that BSC can be manipulated by and thus crucially relies on multisensory mechanisms within PPS as shown both behaviorally for 1PP and in terms of neural correlates for BO. The results also suggest that different combinations of sensory stimuli manipulate most effectively these aspects, with synchronous visuo-tactile stroking affecting BO whereas asynchronous visuo-tactile stroking and vestibular information affecting 1PP. Apprehending better these mechanisms will be an important milestone to understanding how sensory information shapes subjective experience.

EPFL2017