Vestibular agnosia in traumatic brain injury and its link to imbalance

Abstract

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.

Sensitized rotatory motion perception and increased susceptibility to motion sickness in vestibular migraine: A cross‐sectional study

“…rior longitudinal fasciculus) is linked to disturbed vestibular perceptual and VOR thresholds[23]. This is of interest, as in cross-sectional comparison we did not find changes of the VOR threshold, but the increased excitability of brain stem structures may be supported by the inverse correlation between the VOR threshold and the intensity of migraine headache, which may indicate the interactive relation between cortex and brain stem.Sensitized motion perception following vestibular provocation was detected irrespective of other sensory input.…”

“…Patients with VM showed a decreased threshold for rotatory motion perception and a pronounced susceptibility for motion sickness during and after rotation compared to HC, whereas there was no difference at the basic VOR level between the groups. Decreased altered self-motion perception [22,23].…”

“…Vestibular (perceptual) thresholds in VM have been investigated several times [10,20,21]. Seemungal et al reported a technique to measure simultaneous VOR and vestibular perceptual thresholds in healthy participants for the first time in 2004, which recently was applied in acute traumatic brain injury patients and demonstrated altered self‐motion perception [22,23].…”

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

“…We recently showed that in acute TBI patients with imbalance, objective laboratory-obtained measures of VA correlate with impaired brain structural integrity in the white matter (identified using diffusion tensor imaging -DTI) in the right inferior longitudinal fasciculus (ILF) (Calzolari et al, 2021). This DTI analysis thus identified the overlap in imbalance and VA, however the neural correlates distinct to VA were not identified since a whole brain correlation with VA scores did not reach significance.…”

“…CC-BY 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted December 7, 2021. ; https://doi.org/10.1101/2021.12.03.471139 doi: bioRxiv preprint since we previously showed that VA was linked to imbalance via damage to the right inferior longitudinal fasciculus (ILF) (Calzolari et al, 2021) and ILF connects higher order visual cortices to the temporal regions (Latini et al, 2017;Panesar et al, 2018), we probed the cortical regions mapped by right ILF using lingual gyrus as seed, which is often linked to motion-and illusion-perception (Cha & Chakrapani, 2015;Della-Justina et al, 2014;Kahane et al, 2003;Roberts et al, 2017). To assess our predictions, we evaluated functional connectivity via resting state fMRI (rsfMRI) in both grey and white matter brain networks.…”