The human brain networks mediating the vestibular sensation of self-motion

Abstract

Activation of the peripheral vestibular apparatus simultaneously elicits a reflex vestibular nystagmus and the vestibular perception of self-motion (vestibular-motion perception) or vertigo. In a newly characterised condition called Vestibular Agnosia found in conditions with disrupted brain network connectivity, e.g. traumatic brain injury (TBI) or neurodegeneration (Parkinson's Disease), the link between vestibular reflex and perception is uncoupled, such that, peripheral vestibular activation elicits a vestibular ocular reflex nystagmus but without vertigo. Using structural brain imaging in acute traumatic brain injury, we recently linked vestibular agnosia to postural imbalance via disrupted right temporal white-matter circuits (inferior longitudinal fasciculus), however no white-matter tracts were specifically linked to vestibular agnosia. Given the relative difficulty in localizing the neuroanatomical correlates of vestibular-motion perception, and compatible with current theories of human consciousness (viz. the Global Neuronal Workspace Theory), we postulate that vestibular-motion perception (vertigo) is mediated by the coordinated interplay between fronto-parietal circuits linked to whole-brain broadcasting of the vestibular signal of self-motion. We thus used resting state functional MRI (rsfMRI) to map functional brain networks and hence test our postulate of an anterior-posterior cortical network mediating vestibular agnosia. Whole-brain rsfMRI was acquired from 39 prospectively recruited acute TBI patients (and 37 matched controls) with preserved peripheral and reflex vestibular function, along with self-motion perceptual thresholds during passive yaw rotations in the dark, and posturography. Following quality control of the brain imaging, 25 TBI patients' images were analyzed. We classified 11 TBI patients with vestibular agnosia and 14 without vestibular agnosia based on laboratory testing of self-motion perception. Using independent component analysis, we found altered functional connectivity within posterior (right superior longitudinal fasciculus) and anterior networks (left rostral prefrontal cortex) in vestibular agnosia. Regions of interest analyses showed both inter-hemispheric and intra-hemispheric (left anterior-posterior) network disruption in vestibular agnosia. Assessing the brain regions linked via right inferior longitudinal fasciculus, a tract linked to vestibular agnosia in unbalanced patients (but now controlled for postural imbalance), seed-based analyses showed altered connectivity between higher order visual cortices involved in motion perception and mid-temporal regions. In conclusion, vestibular agnosia in our patient group is mediated by multiple brain network dysfunction, involving primarily left frontal and bilateral posterior networks. Understanding the brain mechanisms of vestibular agnosia provide both an insight into the physiological mechanisms of vestibular perception as well as an opportunity to diagnose and monitor vestibular cognitive deficits in brain disease such as TBI and neurodegeneration linked to imbalance and spatial disorientation.

A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys

“…On the other hand, the larger gains and phase leads of the irregular afferents are required to drive robust postural responses since vestibulo-spinal pathways must account for the higher inertia of the body relative to the eye [ 27 , 42 ]. Furthermore, irregular afferents likely also make important contributions to ascending pathways that convey vestibular information to cortical brain circuits mediating self-motion perception ([ 43 ]; also reviewed in [ 14 ]). Interestingly, a recent imaging study in humans reported that these cortical circuits overlap with those mediating postural control [ 44 ].…”