Multimodal MRI of the reorganization of multisensory and sensorimotor networks in chronic bilateral vestibulopathy

Chronic bilateral vestibulopathy (BVP) occurs preferably in elderly patients presenting with postural imbalance and head movement induced oscillopsia. The condition is often incomplete with residual functions in both ears. Beyond the vestibular reflexive deficits, an impairment of spatial orientation and navigation has been described associated with an atrophy of the hippocampal formation. However, this finding was inconsistent in various studies on rodents and humans. In the current MRI study on 15 BVP patients and 15 healthy controls (HC) we combined analyses of whole brain voxel-based morphometry (VBM) and the resting state fMRI (rs-fMRI) on the widely distributed multisensory vestibular network and its connections to sensorimotor, cognitive, and emotional networks at rest. Major results were gray and white matter changes in conjunction with rs-fMRI changes: the left posterior insula, angular and supramarginal gyri, and left premotor cortex; as well as bilateral anterior hippocampal formation and adjacent amygdala; visual cortex V1 and V5; thalamus; prefrontal cortex; cerebellar hemispheres and uvula; and pyramidal tract. Thus, the overlap of structural (VBM) and rs-fMRI including various correlation analyses disclosed that a bilateral reduction of peripheral vestibular input affects multiple networks from the cerebellum up to the cortical hemispheres. A possible functional interpretation is that the observed specific alterations reflect compensation and substitution by other networks - handling perception, sensorimotor balance regulation, cognition, and emotions - due to deficits in one sensory system. This is consistent with anterior hippocampal atrophy's role in spatial memory deficits, as well as the involvement of the cerebellum, amygdala, and prefrontal cortex in emotional processes. It also aligns with the top-down regulation by the prefrontal cortex via the pyramidal tract for cognitive control of balance triggered by the perception of postural instability. Further, correlation analyses support this interpretation because most morphological changes were dependent on the duration of the condition.