A neuroscientific account of how vestibular disorders impair bodily self-consciousness

PERSPECTIVE ARTICLE published: 06 December 2013 doi: 10.3389/fnint.2013.00091 A neuroscientific account of how vestibular disorders impair bodily self-consciousness Christophe Lopez* Laboratoire de Neurosciences Intégratives et Adaptatives - UMR 7260, Centre Saint Charles, Fédération de Recherche 3C, Centre National de la Recherche Scientifique - Aix-Marseille Université, Marseille, France Edited by: Pierre Denise, Université de Caen Basse-Normandie, France Reviewed by: John S. Butler, Albert Einstein College of Medicine, USA Isabella Pasqualini, Ecole Polytechnique Fédérale de Lausanne, Switzerland *Correspondence: Christophe Lopez, Laboratoire de Neurosciences Intégratives et Adaptatives - UMR 7260, Centre Saint Charles, Fédération de Recherche 3C - Case B, Centre National de la Recherche Scientifique - Aix-Marseille Université, 3 Place Victor Hugo, 13331 Marseille Cedex 03, France e-mail: The consequences of vestibular disorders on balance, oculomotor control, and self-motion perception have been extensively described in humans and animals. More recently, vestibular disorders have been related to cognitive deficits in spatial navigation and memory tasks. Less frequently, abnormal bodily perceptions have been described in patients with vestibular disorders. Altered forms of bodily self-consciousness include distorted body image and body schema, disembodied self-location (out-of-body experience), altered sense of agency, as well as more complex experiences of dissociation and detachment from the self (depersonalization). In this article, I suggest that vestibular disorders create sensory conflict or mismatch in multisensory brain regions, producing perceptual incoherence and abnormal body and self perceptions. This hypothesis is based on recent functional mapping of the human vestibular cortex, showing vestibular projections to the primary and secondary somatosensory cortex and in several multisensory areas found to be crucial for bodily self-consciousness. Keywords: vestibular system, body schema, body image, touch, caloric vestibular stimulation, bodily consciousness, multisensory integration INTRODUCTION The consequences of vestibular disorders are dramatic as they incorporate a wide range of symptoms including vertigo, loss of balance, and blurred vision. It is accepted that vertigo results from the activation of the vestibulo-thalamo-cortical pathways, postural instability and falls from abnormal vestibulo-spinal reflexes, and blurred vision from impaired vestibulo-ocular reflexes (Curthoys and Halmagyi, 1995; Borel et al., 2008). More recently, deficits in spatial navigation and memory tasks have been related to vestibular disorders, presumably due to vestibular projections to the cortex and hippocampus (Smith, 1997; Brandt et al., 2005). In addition to these deficits, vestibular patients sometimes report abnormal bodily perceptions. The role of vestibular organs in bodily perceptions has captured the attention of pioneering researches on body representations such as those of Bonnier (1893, 1905), Schilder (1935); Lhermitte (1939), and Menninger-Lerchenthal (1946). These authors reported cases of patients losing connections with their body, experiencing deformations of their body, or disembodiment. Yet, the mechanisms underpinning these disorders remain poorly understood. One reason is that bodily disorders have to date not been quantified experimentally in vestibular patients despite the development of psychophysical methods to measure various bodily experiences (Blanke, 2012). Secondly, the comprehension of how vestibular dysfunction modifies bodily consciousness has been hampered by scarce descriptions of the vestibular cortex. In the present article, I argue that recent progresses in functional mapping of the human vestibular cortex and advances in the neuroscience of bodily self-consciousness afford a neuroscientific explanation of the mechanisms at the basis of bodily disorders in vestibular patients. Frontiers in Integrative Neuroscience A NEUROSCIENTIFIC FRAMEWORK BASED ON THE MULTISENSORY NATURE OF THE VESTIBULO-THALAMO-CORTICAL PATHWAYS The neuroscientific framework to understand bodily disorders in vestibular patients is based on the multisensory nature of the vestibulo-thalamo-cortical pathways, a finding that was unknown from Bonnier and Schilder when they described the consequences of vertigo on body perception. A vestibulo-visuo-somatosensory convergence has been found in all vestibular relays, including vestibular nuclei, thalamus, and cerebral cortex (see Figure 1 and Table 1 for details). Normal sensorimotor development calibrates synergies between actions and their sensory consequences at both behavioral and neural levels (Held and Hein, 1963). For example, head rotations to the right are normally encoded with leftward optic flow and matching proprioceptive signals from the neck. Corresponding synergistic responses exist in all vestibulo-thalamo-cortical structures and recent studies showed that vestibular and visual responses combine “in a statistically optimal fashion,” in accordance with the predictions of Bayesian models (MacNeilage et al., 2007; Fetsch et al., 2012). Importantly, sensory conflicts may disorganize calibrated synergies at the neural level (e.g., visuo-vestibular mismatch alters neural responses in vestibular nuclei; Waespe and Henn, 1978). Here, I propose similar mismatch is produced by various peripheral vestibular disorders (e.g., Menière’s disease, vestibular neuritis). I suggest that vestibular disorders provide the brain with erroneous vestibular signals about current selfmotion and position, and create sensory conflicts (or mismatch) leading to a perceptual incoherence. That is, abnormal vestibular signals would induce misinterpretation of tactile, proprioceptive www.frontiersin.org December 2013 | Volume 7 | Article 91 | 1 “fnint-07-00091” — 2013/12/4 — 17:23 — page 1 — #1 Lopez Vestibular disorders and self-consciousness Other studies suggest that during multisensory conflicts, vestibular cues are weighted higher (Butler et al., 2010; Fetsch et al., 2012). These data indicate that participants strongly rely on vestibular signals, even when this information contradicts other sensory cues. In the following sections, I describe a detailed neuroscientific account of how vestibular dysfunction can distort various aspects of the bodily self. DISTORTED BODY SCHEMA AND BODY IMAGE CLINICAL DESCRIPTION FIGURE 1 | Convergence of vestibular, visual, and somatosensory signals in vestibulo-thalamo-cortical structures. The schema summarizes animal and human data, showing multisensory convergence in three vestibular relays (see also Table 1 for details): Vestibular signals are first processed in the vestibular nuclei in the brainstem, a region that is highly multisensory. A second level of vestibular processing takes place in the thalamus. Multiple thalamic nuclei contain neurons that respond to vestibular stimulation such as the vent (...truncated)