Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study)

Bilateral vestibular failure (BVF) is a rare disorder of the labyrinth or the eighth cranial nerve which has various aetiologies. BVF patients suffer from unsteadiness of gait combined with blurred vision due to oscillopsia. Functional MRI (fMRI) in healthy subjects has shown that stimulation of the visual system induces an activation of the visual cortex and ocular motor areas bilaterally as well as simultaneous deactivations of multisensory vestibular cortex areas. Our question was whether the chronic absence of bilateral vestibular input (BVF) causes a plastic cortical reorganization of the above-described visual-vestibular interaction. We used fMRI to measure the differential effects of horizontal visual optokinetic stimulation (OKN) on activations and deactivations in 10 patients with BVF and compared their data directly to those of pairwise age- and sex-matched controls. We found that bilateral activation of the primary visual cortex (inferior and middle occipital gyri, Brodmann area BA 17, 18, 19), the motion-sensitive areas V5 in the middle and inferior temporal gyri (BA 37), and the frontal eye field (BA 8), the right paracentral and superior parietal lobule and the right fusiform and parahippocampal gyri was significantly stronger and the activation clusters were larger than that of the age-matched healthy controls. Small areas of BOLD signal decreases (deactivations), located primarily in the right posterior insula containing the parieto-insular vestibular cortex, were similar to those in the healthy controls. No other sensory brain areas showed unexpected activations or deactivations, e.g. the somatosensory or auditory cortex areas. Our finding of enhanced activations within the visual and ocular motor systems of BVF patients suggests that they might be correlated with an upregulation of visual sensitivity during tracking of visual motion patterns. Functionally, these enhanced activations are independent of optokinetic performance, since the mean slow-phase velocity of OKN in the BVF patients did not differ from that in normals. Although psychophysical and neurophysiological tests have provided various examples of how sensory loss in one modality leads to a substitutional increase of functional sensitivity in other modalities, this study presents the first evidence of visual substitution for vestibular loss by functional imaging.