Vestibular dysfunction, causing dizziness and imbalance, is a common yet poorly understood feature in patients with TBI. Damage to the inner ear, nerve, brainstem, cerebellum and cerebral hemispheres may all affect vestibular functioning, hence, a multi-level assessment—from reflex to perception—is required. In a previous report, postural instability was the commonest neurological feature in ambulating acute patients with TBI. During ward assessment, we also frequently observe a loss of vertigo sensation in patients with acute TBI, common inner ear conditions and a related vigorous vestibular-ocular reflex nystagmus, suggesting a ‘vestibular agnosia’. Patients with vestibular agnosia were also more unbalanced; however, the link between vestibular agnosia and imbalance was confounded by the presence of inner ear conditions. We investigated the brain mechanisms of imbalance in acute TBI, its link with vestibular agnosia, and potential clinical impact, by prospective laboratory assessment of vestibular function, from reflex to perception, in patients with preserved peripheral vestibular function. Assessment included: vestibular reflex function, vestibular perception by participants’ report of their passive yaw rotations in the dark, objective balance via posturography, subjective symptoms via questionnaires, and structural neuroimaging. We prospectively screened 918 acute admissions, assessed 146 and recruited 37. Compared to 37 matched controls, patients showed elevated vestibular-perceptual thresholds (patients 12.92°/s versus 3.87°/s) but normal vestibular-ocular reflex thresholds (patients 2.52°/s versus 1.78°/s). Patients with elevated vestibular-perceptual thresholds [3 standard deviations (SD) above controls’ average], were designated as having vestibular agnosia, and displayed worse posturography than non-vestibular-agnosia patients, despite no difference in vestibular symptom scores. Only in patients with impaired postural control (3 SD above controls’ mean), whole brain diffusion tensor voxel-wise analysis showed elevated mean diffusivity (and trend lower fractional anisotropy) in the inferior longitudinal fasciculus in the right temporal lobe that correlated with vestibular agnosia severity. Thus, impaired balance and vestibular agnosia are co-localized to the inferior longitudinal fasciculus in the right temporal lobe. Finally, a clinical audit showed a sevenfold reduction in clinician recognition of a common peripheral vestibular condition (benign paroxysmal positional vertigo) in acute patients with clinically apparent vestibular agnosia. That vestibular agnosia patients show worse balance, but without increased dizziness symptoms, explains why clinicians may miss treatable vestibular diagnoses in these patients. In conclusion, vestibular agnosia mediates imbalance in traumatic brain injury both directly via white matter tract damage in the right temporal lobe, and indirectly via reduced clinical recognition of common, treatable vestibular diagnoses.
Background While extensive research has been advancing our understanding of the spatial and postural decline in healthy elderly (HE) and Alzheimer’s disease (AD), much less is known about how the vestibular system contributes to the spatial and postural processing in these two populations. This is especially relevant during turning movements in the dark, such as while walking in our garden or at home at night, where the vestibular signal becomes central. As the prevention of falls and disorientation are of serious concern for the medical service, more vestibular-driven knowledge is necessary to decrease the burden for HE and AD patients with vestibular disabilities. Overview of the article The review briefly presents the current “non-vestibular based” knowledge (i.e. knowledge based on research that does not mention the “vestibular system” as a contributor or does not investigate its effects) about spatial navigation and postural control during normal healthy ageing and AD pathology. Then, it concentrates on the critical sense of the vestibular system and explores the current expertise about the aspects of spatial orientation and postural control from a vestibular system point of view. The norm is set by first looking at how healthy elderly change with age with respect to their vestibular-guided navigation and balance, followed by the AD patients and the difficulties they experience in maintaining their balance or during navigation. Conclusion Vestibular spatial and vestibular postural deficits present a considerable disadvantage and are felt not only on a physical but also on a psychological level by all those affected. Still, there is a clear need for more (central) vestibular-driven spatial and postural knowledge in healthy and pathological ageing, which can better facilitate our understanding of the aetiology of these dysfunctions. A possible change can start with the more frequent implementation of the “vestibular system examination/rehabilitation/therapy” in the clinic, which can then lead to an improvement of future prognostication and disease outcome for the patients.
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.
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