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

Abstract

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: bodily consciousness; body image; body schema; caloric vestibular stimulation; multisensory integration; touch; vestibular system.

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 ventroposterior complex (VPM, ventral posterior medial nucleus; VPI, ventral posterior inferior nucleus; VPL, ventral posterior lateral nucleus), ventroanterior (VA) and ventrolateral (VL) nuclear complex, intralaminar nuclei (IL), thalamic posterior nuclear group (MGN, medial geniculate nucleus; LGN, lateral geniculate nucleus) and lateral posterior nucleus (LP). Most of these thalamic nuclei contain multisensory neurons. A third level of vestibular processing occurs in the cerebral cortex. Neuroimaging studies used caloric (CVS) and galvanic (GVS) vestibular stimulation and revealed activations centered on the insula, parietal operculum, and temporo-parietal junction (Lopez et al., 2012a; zu Eulenburg et al., 2012). This area may be similar to a region known as the parieto-insular vestibular cortex (PIVC) in monkeys (Grüsser et al., 1990a,b; Guldin and Grüsser, 1998; Chen et al., 2010). The PIVC is considered the core region of the vestibular cortex because it is strongly connected or interconnected with most of the other vestibular cortical areas. At least 10 other cortical areas process vestibular signals including somatosensory (areas 2 and 3), superior parietal, cingulate, and premotor cortex.