Vestibular contribution to bodily self-consciousness and multisensory cortical processing

Christian Pfeiffer
EPFL, 2015
Thèse EPFL

Résumé

How does the self relate to the body? Bodily self-consciousness, i.e. the sense of being a subject bound to a body, involves a first-person perspective (1PP), i.e. the sense of being directed at the world. Prior research suggests that bodily self-consciousness depends on brain mechanisms integrating multisensory bodily signals. However, the specific multisensory mechanisms of 1PP are poorly understood. Here, I defend the thesis that the vestibular system, i.e. the sensory system encoding rotational and linear accelerations of the head, contributes to 1PP and related multisensory processing in the brain. The first part of my thesis presents experimental evidence showing that 1PP was influenced by multisensory conflict about the direction of gravity and the location of the body. 1PP depended on integrated visual-vestibular signals and was functionally distinct from another aspect of bodily self-consciousness: self-identification, i.e. the feeling that a particular body is âmineâ. The second part of my thesis presents the electrical neural correlates by which vestibular stimulation affected somatosensory and visual cortical processing. Passive whole-body yaw rotation naturally and selectively stimulated the vestibular system while the evoked responses to somatosensory or visual stimuli were recorded by electroencephalography. Electrical neuroimaging analysis showed temporal-specific vestibular effects on somatosensory and visual evoked potentials, localized by source estimations to distinct regions of the somatosensory, visual, and vestibular cortical networks. Collectively, the results from my thesis suggest that the vestibular system contributes to 1PP and multisensory cortical processing and imply that the vestibular system should not be neglected when studying higher brain function and neurobiological mechanisms of consciousness.

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https://infoscience.epfl.ch/record/210007?ln=fr

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Christian Pfeiffer
EPFL, 2015
Thèse EPFL

Résumé

Official source

https://infoscience.epfl.ch/record/210007?ln=fr

À propos de ce résultat

Concepts associés (17)

Concepts associés

Chargement

Publications associées (77)

Publications associées

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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

Chargement

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

Chargement

The vestibular system is composed of otolith organs and semi-circular canals that encode linear and angular accelerations, as well as the position of the head with respect to gravity. Thus, the detection of self-motion, the distinction between self- and object-motion, as well as gaze stabilisation and maintenance of postural stability are the core vestibular functions. Recent research shows that vestibular information interacts with higher-level cognitive processes, such as space perception, attention orienting, body schema and bodily self-consciousness. In order to contribute to these faculties, vestibular information is dynamically combined with visual, somatosensory and proprioceptive signals. In the present thesis we explore such multimodal interactions using a human centrifuge (rotating chair). In Part 1 we show that visual and vestibular cues are integrated in accordance with statistical optimality even when large directional conflicts are introduced between these modalities. Participants were significantly better in discriminating rotation magnitude when simultaneously presented with visual and vestibular cues, as compared to each modality independently, despite the fact that the axes of rotation implied by the two cues were different (Study 1). We also demonstrate that visuo-vestibular integration is present and optimal in patients with unilateral vestibular loss (Study 2). Part 2 of the present thesis examined vestibularsomatosensory interactions. We show that vestibular stimulation in the form of passive whole-body rotations increases tactile sensitivity at the fingertips, as compared to a no-rotation baseline (Study 3). We also demonstrate that the effect of vestibular stimulation on touch is not direct, but mediated by visual information about self-motion: visual and vestibular cues first combine, and only subsequently influence tactile sensitivity (Study 4). In Part 3 of this thesis, we explored how vestibular stimulation affects visual attention and awareness. We show that when acting as an exogenous cue, vestibular stimulation orients attention at short cue-to-target delays. When acting as an endogenous cue, vestibular stimulation strongly orients attention at all cue-to-target delays (Study 5). Vestibular stimulation also affects visual awareness. Using a continuous flash suppression paradigm to suppress an optic flow stimulus during passive whole-body rotations, we show that optic flow that is congruent (i.e. counterdirectional) with the direction of the vestibular rotation breaks suppression faster than incongruent optic flow (Study 6). In sum, our findings refine the existing knowledge on multisensory processing in general and vestibular interactions with other senses in particular. Our results are of relevance for the understanding of how visual, vestibular, proprioceptive and somatosensory information are combined by the brain in order to form a coherent representation of the self in space.

EPFL2015

Chargement

EPFL2015

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

Petr Grivaz

EPFL2017