Causal mapping of self-motion networks in the human brain

Abstract

Although functional neuroimaging studies using caloric and galvanic vestibular stimulation have identified a distributed cortical network involved in human vestibular processing, including the posterior insula, parietal operculum, temporo-parietal junction, cingulate and frontal areas, the causal contribution of specific brain regions to vestibular self-motion perception remains poorly understood. Invasive electrical brain stimulation (EBS) during stereoelectroencephalography (SEEG) offers a unique opportunity to causally map the cortical networks underlying vestibular self-motion perception in humans. Here, we retrospectively analyzed EBS-induced vestibular percepts in 354 patients with drug-resistant epilepsy undergoing SEEG. A total of 19,708 stimulations (11,004 at 50 Hz and 8,704 at 1 Hz) yielded 3,015 clinical responses. Vestibular self-motion illusions were defined as sensations of vertigo, dizziness, whole-body rotation, or translation occurring without corresponding physical movement. Stimulation sites were assigned to the seven large-scale functional networks of the Schaefer-Yeo atlas to characterize the network organization of vestibular self-motion perception. Vestibular self-motion sensations were elicited in 46 patients during 86 EBS delivered outside epileptogenic and lesional regions. Percepts ranged from nonspecific vertigo and dizziness (54.7%) to more explicit rotational (30.2%) and translational (15.1%) self-motion illusions. Vestibular responses were most commonly evoked by stimulation of the insula, medial temporal regions, cingulate cortex, inferior frontal gyrus, and premotor cortices. Network-level mapping using the Schaefer-Yeo atlas revealed a non-uniform distribution of vestibular sites across large-scale functional networks, with the highest representation within the salience/ventral attention, visual, and dorsal attention networks. Together, these findings provide causal evidence that vestibular self-motion perception emerges from activity within a distributed cortical network involved in attentional control and multisensory processing. Beyond advancing our understanding of human vestibular processing, these findings may have clinical relevance for disorders involving altered self-motion perception, including vestibular epilepsy and functional neurological disorders.