Recent discoveries have emphasized the role of the vestibular system in cognitive processes such as memory, spatial navigation and bodily self-consciousness. A precise understanding of the vestibular pathways involved is essential to understand the consequences of vestibular diseases for cognition, as well as develop therapeutic strategies to facilitate recovery. The knowledge of the “vestibular cortical projection areas”, defined as the cortical areas activated by vestibular stimulation, has dramatically increased over the last several years from both anatomical and functional points of view. Four major pathways have been hypothesized to transmit vestibular information to the vestibular cortex: (1) the vestibulo-thalamo-cortical pathway, which probably transmits spatial information about the environment via the parietal, entorhinal and perirhinal cortices to the hippocampus and is associated with spatial representation and self-versus object motion distinctions; (2) the pathway from the dorsal tegmental nucleus via the lateral mammillary nucleus, the anterodorsal nucleus of the thalamus to the entorhinal cortex, which transmits information for estimations of head direction; (3) the pathway via the nucleus reticularis pontis oralis, the supramammillary nucleus and the medial septum to the hippocampus, which transmits information supporting hippocampal theta rhythm and memory; and (4) a possible pathway via the cerebellum, and the ventral lateral nucleus of the thalamus (perhaps to the parietal cortex), which transmits information for spatial learning. Finally a new pathway is hypothesized via the basal ganglia, potentially involved in spatial learning and spatial memory. From these pathways, progressively emerges the anatomical network of vestibular cognition.
Self-consciousness is the remarkable human experience of being a subject: the “I”. Self-consciousness is typically bound to a body, and particularly to the spatial dimensions of the body, as well as to its location and displacement in the gravitational field. Because the vestibular system encodes head position and movement in three-dimensional space, vestibular cortical processing likely contributes to spatial aspects of bodily self-consciousness. We review here recent data showing vestibular effects on first-person perspective (the feeling from where “I” experience the world) and self-location (the feeling where “I” am located in space). We compare these findings to data showing vestibular effects on mental spatial transformation, self-motion perception, and body representation showing vestibular contributions to various spatial representations of the body with respect to the external world. Finally, we discuss the role for four posterior brain regions that process vestibular and other multisensory signals to encode spatial aspects of bodily self-consciousness: temporoparietal junction, parietoinsular vestibular cortex, ventral intraparietal region, and medial superior temporal region. We propose that vestibular processing in these cortical regions is critical in linking multisensory signals from the body (personal and peripersonal space) with external (extrapersonal) space. Therefore, the vestibular system plays a critical role for neural representations of spatial aspects of bodily self-consciousness.