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Vestibular and multisensory investigations of bodily self-consciousness

Final Report Summary - BODILYSELF (Vestibular and multisensory investigations of bodily self-consciousness)

Despite recent neuroscientific efforts to study the mechanisms of consciousness, self-consciousness has received much less attention as it is difficult to approach empirically. However, philosophers and neuroscientists have argued that self-consciousness relies on several bodily experiences, and that the investigation of the sensory and neural mechanisms involved in these bodily experiences is crucial for the understanding of self-consciousness. Bodily experiences that seem important for the self comprise first-person perspective taking, embodied self-location, and the sense of ownership of the body. Multisensory processing has been proven to be of key importance for bodily experiences and the self, although research has focused mostly on the contribution of visual and somatosensory signals. The investigation of vestibular signals (from the balance system in the inner ear) has received much less attention despite its key importance in coding whole-body motion and orientation in space.

The BODILYSELF Project investigates vestibular contributions to whole-body experiences, in particular self-location, first-person perspective taking and self-other distinction and mirroring. For this, the BODILYSELF Project links vestibular physiology with cognitive science of the self. We used artificial stimulation of the vestibular system and multisensory conflicts – in combination with neuroimaging – to explore the mechanisms of bodily self-consciousness. The strength and novelty of the BODILYSELF Project lies in joining approaches from cognitive neuroscience, vestibular physiology and oto-neurology, in collaboration with a philosopher of mind. This may lead to findings that are relevant across research fields in the cognitive neurosciences of the self, philosophy of mind, neurology and oto-neurology.

Summary of the project objectives:
The BODILYSELF Project specifically aims at determining the role of the vestibular system in self-consciousness. The main goals of the BODILYSELF Project are to determine: (1) The vestibular and multisensory mechanisms of self-location, perspective taking and self-identification with another body in healthy subjects and patients with vestibular loss; (2) The changes in vestibular processing during mental simulation of disembodied self-location and perspective; (3) The mechanisms of first- and third-person perspective taking; (4) The contribution of vestibular signals to self-other distinction and mirroring.

Description of the work performed and summary of the main results:
We have developed a solid theoretical framework, which we believe will foster the current neuroscientific, psychological and philosophical models of the self. For example, we showed that connecting vestibular signals to the sense of self and bodily consciousness may impact otorhinolaryngology, neurology and neuropsychology by improving the understanding of the consequences of a peripheral vestibular disorders and damage to the vestibular cortex for self-perception and awareness (see Lopez, 2016. Current Opinion in Neurology; Lenggenhager & Lopez, 2015. “Open Mind”).

Theoretical predictions have been put under scientific scrutiny by testing the consequences of vestibular disorders on simulated disembodied self-location and viewpoint. In the to date largest sample of patients with dizziness, we measured how vestibular disorders may induce complex experiences of detachment, such as depersonalization (experience that the self is strange or unreal) and out-of-body-experience (the experience that the self or centre of awareness is outside of the physical body) (see Lopez & Elzière, 2017. Cortex). We showed that vestibular disorders significantly increased the likelihood of reporting out-of-body experience, in otherwise fully awake and non-delusional patients. In addition, depersonalization was high in patients with vestibular disorders. Statistical models revealed precipitating factors of abnormal sense of self-location: out-of-body experiences in patients with dizziness may arise from a combination of perceptual incoherence (due to multisensory conflicts in the brain between visual, somatosensory postural and vestibular signals) evoked by the vestibular dysfunction with psychological factors (depersonalization, depression and anxiety) and neurological factors (migraine). Natural and artificial vestibular stimulation have also been employed in healthy participants to demonstrate the vestibular contributions to self-location and perspective taking. In a study conducted in healthy participants, we merged natural full-body vestibular stimulations on a rotating chair and explicit visuo-spatial perspective taking tasks in virtual environments (Deroualle et al., 2015. Neuropsychologia). Results show that vestibular signals have a direction-specific influence on visuo-spatial perspective taking (self-centred mental imagery), but not a general effect on mental imagery. Findings from this study suggest that vestibular signals contribute to one of the most crucial mechanisms of social cognition: understanding others’ actions. Another study conducted in collaboration with Dr. Ferrè and Prof. Haggard (University College London, Royal Holloway) measured the influence of galvanic vestibular stimulation (GVS) on perspective taking using a non-visual task. Low-intensity GVS augmented the natural vestibular contribution to embodiment, providing the first experimental evidence that vestibular inputs promote a first-person perspective in participants involved in tactile perception tasks (Ferrè, Lopez & Haggard, 2014. Psychological Science). Similarly, we showed that low-intensity GVS promoted visuo-spatial processing according to a first-person viewpoint (Pavlidou, Ferrè & Lopez, Cortex, in minor revision). Altogether, these data indicate that vestibular signals contribute to anchoring the self and viewpoint to the body.

Several electrophysiological investigations were conducted to measure vestibular processing during experimentally induced changes in self-location and viewpoint. We have successfully set up a unique and innovative experimental environment merging state-of-the-art electromyography, electroencephalography, electrooculography, repeated GVS of the vestibular nerves, and social tasks embedded in virtual environments (in a head-mounted display). In a first study, we investigated how explicit third-person perspective modulates vestibular-evoked myogenic potentials (VEMPs) recorded using electromyography. Analyses of the VEMPs waveform and the amplitude of the p13 component indicate that the angle of perspective taking (i.e. the angle between the participant’s and avatar’s viewpoint) modulates early vestibulospinal responses, around 11-19 ms poststimulus. We found that the largest angle of perspective taking tends to evoke the largest VEMPs. This suggests that mental simulation of the viewpoint of a distant avatar involves more strongly brain structures supporting vestibular information processing and vestibulospinal reflexes. Correlation analyses showed larger p13 amplitude in participants with lower empathy scores, providing the first evidence that the ability to empathize also influences vestibular information processing and even modulates short-latency vestibulospinal reflexes.
In a second study, we investigate how observing passive motion of another body or the self-body changes vestibular processing, with the aim of demonstrating self-other resonance in the vestibulo-thalamo-cortical system, as already found for tactile, pain, and motor processing in the brain. Participants were shown in a head-mounted display videos depicting passive rotations of their own body, someone else's body, or an object. VEMPs amplitude was significantly reduced for “self” and “other” videos when compared to “object” videos. VEMPs were even smaller for “self” than “other” videos, revealing a social modulation of vestibular information processing. This study provides the first evidence that social cognition has a pre-reflective influence on vestibular processing. In a third study conducted in our international partner’s lab (Prof. Blanke, EPFL, Lausanne), EEG was used to measure brain responses to natural whole-body rotations in healthy participants. Data from this study show that continuous and transient whole-body rotations evoke alpha band suppression over bilateral temporo-parietal scalp regions (Gale et al., 2016. Journal of Neurophysiology).

Impact of the project and applications: Investigating bodily consciousness is not only important for basic research and theoretical developments; it has also strong clinical implications. Indeed, disorders of bodily consciousness occur in a large variety of neurological and psychiatric diseases (reviewed in Dieguez & Lopez, 2017. Annals of Physical and Rehabilitation Medicine). It is not rare that patients with vestibular disorders report abnormal body image, depersonalization and derealization, but the origin of these symptoms is unclear. Because of the lack of empirical knowledge about the effect of vestibular disorders on bodily representations, oto-neurologists are confronted by a lack of therapeutic strategy. Vestibular stimulation may be used to treat bodily disorders, including body integrity image disorder and thalamic pain syndrome.

Website: More information can be found on the BODILYSELF Project website: http://lnia.fr/corps-et-cognition/bodilyself-vestibular-and-multisensory-investigations-of-bodily-self-consciousness/