The human vestibular cortex: functional anatomy, connectivity and the effect of vestibular disease

Abstract

AbstractArea OP2 in the posterior peri-sylvian cortex has been proposed to be the core human vestibular cortex. We defined the functional anatomy of OP2 using spatially constrained independent component analysis of functional MRI data from the Human Connectome Project. Ten distinct subregions were identified. Most subregions showed significant connectivity to other areas with vestibular function: the parietal opercula, the primary somatosensory cortex, the supracalcarine cortex, the left inferior parietal lobule and the anterior cingulate cortex. OP2 responses to vestibular and visual-motion were analysed in 17 controls and 17 right-sided unilateral vestibular lesion patients (vestibular neuritis) who had previously undergone caloric and optokinetic stimulation during functional MRI. In controls, a posterior part of right OP2 showed: (a) direction-selective responses to visual motion; and (b) activation during caloric stimulation that correlated positively with perceived self-motion, and negatively with visual dependence. Patients showed abnormal OP2 activity, with an absence of visual or caloric activation of the healthy ear and no correlations with dizziness or visual dependence – despite normal brainstem responses to caloric stimulation (slow-phase nystagmus velocity). A lateral part of right OP2 showed activity that correlated with chronic dizziness (situational vertigo) in patients. Our results define the functional anatomy of OP2 in health and disease. A posterior subregion of right OP2 shows strong functional connectivity to other vestibular regions and a visuo-vestibular profile that becomes profoundly disrupted after vestibular disease. In vestibular patients, a lateral subregion of right OP2 shows responses linked to the challenging long-term symptoms which define poorer clinical outcomes.Significance statementThe human cortical vestibular network is critical to higher vestibular functions such as the perception of self-motion, judgements about verticality (‘which way is up’), and adaptation following peripheral vestibular disease (e.g. vestibular neuritis). The functional organisation of this network has remained poorly understood. In this study, we define the functional anatomy of area OP2 - a core region within the human cortical vestibular network. We identify subregions of OP2 with strong connectivity to other cortical vestibular areas. We show specific subregions of right OP2 process vestibular and visual motion information in health and that such processing is disrupted following peripheral vestibular disease. Abnormal signal processing within OP2 may underpin chronic dizziness following peripheral vestibular disease.