Vestibular agnosia is linked to worse balance recovery in traumatic brain injury: a longitudinal behavioural and neuro-imaging study

Background and Objectives: Moderate-to-severe traumatic brain injury patients commonly manifest vestibular dysfunction with imbalance and dizziness. Importantly, falls in these patients are linked to long-term unemployment and increased mortality. There are however no objective acute-prospective longitudinal data of vestibular outcomes nor of the mechanisms predicting vestibular recovery. We previously showed that in acute traumatic brain injury, acute imbalance was linked to impaired vestibular perception of self-motion (i.e. vestibular agnosia) via right inferior longitudinal fasciculus disruption. This report importantly could not inform upon the predictors nor neural substrates of vestibular recovery, questions which we focus upon in this first acute-longitudinal study assessing objective vestibular recovery in traumatic brain injury, with detailed clinical, laboratory and neuroimaging measures. Methods: We screened 918 hospitalized traumatic brain injury patients, recruiting 39 acutely (18 - 65 age) with preserved peripheral vestibular function confirmed via vestibular ocular reflex testing (patients 2.52{degrees} /s versus controls 1.78{degrees} /s; P > 0.05) of which 34 patients (17 with vestibular agnosia) completed the follow-up testing. Common inner ear and migraine diagnoses were treated to resolution pre-testing. Vestibular perceptual thresholds were assessed via whole-body rotations in the dark on a computerized rotating chair. Using k-means clustering, vestibular perceptual thresholds of healthy controls and patients were compared resulting in 1.99{degrees} /s/s or above being classified as vestibular agnosia. Balance was assessed via force platform. Results: The change in vestibular perceptual thresholds and sway from acute to follow-up was linked (P < 0.05) and a logistic model indicated (P < 0.05) that those who had acute vestibular agnosia made worse recovery of vestibular mediated function (balance and vestibular perception) as compared to non-vestibular agnosia patients. Moreover, subjective symptoms of imbalance and dizziness (via "Dizziness Handicap Inventory") were not linked to objective vestibular recovery of balance and perception (P > 0.05). Neuroimaging findings indicated that the linked vestibular recovery (from vestibular agnosia and imbalance) was mediated by bihemispheric fronto-posterior circuits particularly frontal poles and splenium of corpus callosum. Conclusion: Acute vestibular agnosia predicts worse recovery of imbalance and linked recovery of vestibular agnosia and is mediated by partially overlapping, bi-hemispheric circuits. Since vestibular dysfunction may occur without vertigo complaint (from vestibular agnosia), clinical and research assessment of vestibular recovery should assess objective vestibular measures in addition to dizziness symptoms, which poorly track central vestibular recovery. Finally, our cohort was young and without medical co-morbidities, hence understanding the additional impacts of ageing and multimorbidity is required in vestibular recovery in traumatic brain injury cohorts.