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

Hadi, Zaeem; Mahmud, Mohammad; Pondeca, Yuscah; Calzolari, Elena; Chepisheva, Mariya; Smith, Rebecca; Rust, Heiko; Sharp, David J.; Seemungal, Barry

doi:10.1016/j.jns.2022.120458

Cited by 8 publications

(10 citation statements)

References 65 publications

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“…7 More convincing however, is that TBI patients with imbalance had worse damage to the genu of the corpus callosum than TBI patients with normal balance. 7 These findings are congruent with that of our longitudinal fMRI data (supplementary) and with our previous studies, 7,22 and buttresses the notion that interhemispheric disconnection in TBI leads to vestibular dysfunction with imbalance and vestibular agnosia.…”

Section: Discussionsupporting

confidence: 90%

“…Regarding underlying brain mechanisms, our structural (white and grey matter) brain imaging found that vestibular recovery was mediated primarily by recovery of posterior corpus callosal structural integrity, mediating sensory signalling, and motor and premotor cortical regions, mediating efferent signalling. These data thus support the notion that vestibular cortical circuits mediating the vestibular signals of head motion are highly distributed, 7,22,38–41 with recovery of interhemispheric sensori-motor signalling being critical for post-TBI recovery of vestibular-mediated balance and perception.…”

Section: Discussionsupporting

confidence: 80%

“…Acutely, our patient cohort were categorized into vestibular agnosia (VA+) or no vestibular agnosia (VA-) by comparison with healthy controls’ vestibular perceptual thresholds (mean: 0.76 °/s 2 ; SD: 0.42) using k-means clustering, which resulted in 1.99 °/s 2 or above acceleration threshold on either side (right or left sided rotations) being classified as vestibular agnosia. 22…”

Section: Methodsmentioning

confidence: 99%

“…As such, this report provides new longitudinal data relevant to recovery of vestibular mediated balance and perception, in a cohort we previously reported only acute data. 7,22,23…”

Section: Introductionmentioning

confidence: 99%

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

Hadi,

Mahmud,

Calzolari

et al. 2024

Preprint

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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° /s versus controls 1.78° /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° /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.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionsupporting

confidence: 80%

Section: Methodsmentioning

confidence: 99%

“…As such, this report provides new longitudinal data relevant to recovery of vestibular mediated balance and perception, in a cohort we previously reported only acute data. 7,22,23…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Hadi,

Mahmud,

Calzolari

et al. 2024

Preprint

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“…These questions remain unanswered however, as there are no prospective, blinded, and controlled studies that have assessed the mechanisms and incidence of dizziness in patients with severe cervical radiculopathy and their progress, following surgical intervention. For example, in healthy subjects, although measures of vestibular-perceptual and VOR thresholds to self-motion overlap in magnitude [53], perceptual thresholds are generally greater than VOR thresholds, but this perceptuo-reflex disparity is hugely amplified in patients with a brain dysfunction who manifest 'vestibular agnosia' [5,54] (in vestibular agnosia, significant peripheral vestibular activation may not be accompanied by a vertigo sensation). Anecdotally, cardiologists expert in syncope do not recognise seeing patients with carotid sinus syndrome with neck pain, although this could arise from referral bias or because cardiologists do not ask, or ponder, about neck pain.…”

Section: The Somatosensory Input Hypothesismentioning

confidence: 99%

The Bárány Society position on ‘Cervical Dizziness’

Seemungal

Agrawal

Bisdorff

et al. 2022

VES

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This paper describes the Bárány Society Classification OverSight Committee (COSC) position on Cervical Dizziness sometimes referred to as Cervical Vertigo. This involved an initial review by a group of experts across a broad range of fields, and then subsequent review by the Bárány Society COSC. Based upon the so far published literature, the Bárány Society COSC takes the view that the evidence supporting a mechanistic link between an illusory sensation of self-motion (spinning or otherwise) and neck pathology and/or symptoms of neck pain - either by affecting the cervical vertebra, soft tissue structures or cervical nerve roots - is lacking. When a combined head and neck movement triggers an illusory sensation of spinning, there is either an underlying common vestibular condition such as migraine or BPPV or less commonly a central vestibular condition including, when acute in onset, dangerous conditions such as a dissection of the vertebral artery with posterior circulation stroke and, exceedingly rarely, a vertebral artery compression syndrome. The Committee notes however, that migraine, including vestibular migraine, is by far, the commonest cause for the combination of neck pain and vestibular symptoms. The committee notes that since head movement aggravates symptoms in almost any vestibular condition, the common finding of increased neck muscle tension in vestibular patients, may be linked as both cause and effect, to reduced head movements. Additionally, there are theoretical mechanisms, which have never been explored, whereby cervical pain may promote vaso-vagal, cardio-inhibitory reflexes and hence by presyncopal mechanisms, elicit transient disorientation and/or imbalance. The committee accepts that further research is required to answer the question as to whether those rare cases in which neck muscle spasm is associated with a vague sense of spatial disorientation and/or imbalance, is indeed linked to impaired neck proprioception. Future studies should ideally be placebo controlled and double-blinded where possible, with strict inclusion and exclusion criteria that aim for high specificity at the cost of sensitivity. To facilitate further studies in “cervical dizziness/vertigo”, we provide a narrative view of the important confounds investigators should consider when designing controlled mechanistic and therapeutic studies. Hence, currently, the Bárány COSC, refrains from proposing any preliminary diagnostic criteria for clinical use outside a research study. This position may change as new research evidence is provided.

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Illusions of Self‐Motion during Magnetic Resonance‐Guided Focused Ultrasound Thalamotomy for Tremor

Ciocca,

Jameel,

Yousif

et al. 2024

Annals of Neurology

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ObjectiveBrain networks mediating vestibular perception of self‐motion overlap with those mediating balance. A systematic mapping of vestibular perceptual pathways in the thalamus may reveal new brain modulation targets for improving balance in neurological conditions.MethodsHere, we systematically report how magnetic resonance‐guided focused ultrasound surgery of the nucleus ventralis intermedius of the thalamus commonly evokes transient patient‐reported illusions of self‐motion. In 46 consecutive patients, we linked the descriptions of self‐motion to sonication power and 3‐dimensional (3D) coordinates of sonication targets. Target coordinates were normalized using a standard atlas, and a 3D model of the nucleus ventralis intermedius and adjacent structures was created to link sonication target to the illusion.ResultsA total of 63% of patients reported illusions of self‐motion, which were more likely with increased sonication power and with targets located more inferiorly along the rostrocaudal axis. Higher power and more inferiorly targeted sonications increased the likelihood of experiencing illusions of self‐motion by 4 and 2 times, respectively (odds ratios = 4.03 for power, 2.098 for location).InterpretationThe phenomenon of magnetic vestibular stimulation is the most plausible explanation for these illusions of self‐motion. Temporary unilateral modulation of vestibular pathways (via magnetic resonance‐guided focused ultrasound) unveils the central adaptation to the magnetic field‐induced peripheral vestibular bias, leading to an explicable illusion of motion. Consequently, systematic mapping of vestibular perceptual pathways via magnetic resonance‐guided focused ultrasound may reveal new intracerebral targets for improving balance in neurological conditions. ANN NEUROL 2024

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

Cited by 8 publications

References 65 publications

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

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

The Bárány Society position on ‘Cervical Dizziness’

Illusions of Self‐Motion during Magnetic Resonance‐Guided Focused Ultrasound Thalamotomy for Tremor

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