Improvement of Asymmetric Vestibulo-Ocular Reflex Responses Following Onset of Vestibular Neuritis Is Similar Across Canal Planes

Abstract

Background: We examined whether, after onset of acute unilateral vestibular neuritis (aUVN), initial disease effects, subsequent peripheral recovery and central compensation cause similar changes in vestibular ocular reflex (VOR) gains in all 3 semi-circular canal planes. Methods: 20 patients, mean age 56.5 years, with pathological lateral canal video head impulse test (vHIT) VOR gains due to aUVN, were subsequently examined with vHIT in all 3 canal planes on average 4.3 and 36.7 days (“5 weeks”) after aUVN onset. Results: Lateral and anterior deficit side (DS) average gains equaled 0.41 at aUVN onset. Non-deficit, normal, side (NS) gains were 0.88 and 0.81, respectively. Mean posterior DS gain was similar at onset, 0.43, provided only gains lower than 0.6 (lower limit of healthy controls) were considered. NS posterior mean gain at onset (0.68) was less ( p ≤ 0.0006) than lateral and anterior NS gains. After 5 weeks, DS lateral, anterior and posterior canal gains increased ( p ≤ 0.05), on average, to 0.65, 0.59, and 0.58, respectively. NS gains increased to 0.91, 0.87, and 0.76 ( p = 0.007), respectively. At 5 weeks deficit-lateral/normal-lateral canal plane gain asymmetries were significantly ( p < 0.0008) reduced from 36.9 to 19.4%, deficit-anterior/normal-posterior asymmetry decreased from 28.6 to 18.1%, while deficit-posterior/normal-anterior asymmetry changed from 29.7 to 21.4%, all to circa 20%. Roll plane asymmetries decreased slightly over 5 weeks (28.6–18.1%) but pitch plane asymmetries remained significantly less ( p = 0.001), not different from 0% regardless of initial DS posterior canal vHIT gain. Yaw plane asymmetry changes are identical to those of the lateral canals (36.7–19.4%). Conclusions: These results indicate that, at onset, aUVN of the superior vestibular nerve has a similar effect on lateral and anterior deficit DS VOR gains, and on posterior DS canal VOR gains if the inferior nerve was also affected at onset. The significant improvements to equal 5 week levels of DS gains and slightly greater posterior NS gain improvements, compared to lateral and anterior NS gains, yielding a common canal plane gain asymmetry of 20% at 5 weeks, suggest similar neural compensation mechanisms were active along VOR pathways. Unexpectantly, canal plane improvement was not replicated in pitch plane asymmetries.

Video Head Impulse Test (vHIT): Value of Gain and Refixation Saccades in Unilateral Vestibular Neuritis

“…The gain asymmetry decreased on the affected side, mainly in the affected AC/unaffected PC plane ( Table 2 ). However, Allum and Honegger [ 20 ] reported that the mean gain asymmetry change between onset and 5 weeks was greater ( p < 0.001) in the horizontal canal plane (from 36.9% to 19.4%) than in the other planes.…”

Case Report: Could Hennebert's Sign Be Evoked Despite Global Vestibular Impairment on Video Head Impulse Test? Considerations Upon Pathomechanisms Underlying Pressure-Induced Nystagmus due to Labyrinthine Fistula

“…On the other hand, PSC was the only hypoactive canal in the contralateral ear in all cases and the expected corrective saccades after head impulses were lacking in most cases, raising the possibility that our findings might be due to artifacts. Nevertheless, most healthy PSCs exhibited highly reduced VOR-gain values compared to ipsilateral SCs also in larger cohorts with unilateral vestibular loss ( 41 ). Moreover, the functional impairment for the PSC of the unaffected ear in the first two cases might reflect the greater effect of aging on PSC VOR-gain compared to the other SCs ( 42 ).…”

Acute unilateral vestibular neuritis contributes to alterations in vestibular function modulating circumvention around obstacles: A pilot study suggesting a role for vestibular signals in the spatial perception of orientation during circumvention

“…Either the planned approaching trajectory yaw velocity is set by patients with aUVL to a larger preprogrammed yaw velocity than that set by HCs to ensure a collision does not occur, or, the same velocity is set by the subjects with aUVL as set by HCs, but larger velocities result because the feedback vestibulo-spinal gain countering trunk rotation velocities is too strong, that is, destabilizing, or, third, a combination of the effects occur in patients with aUVL. For the vestibulospinal gain explanation to be valid, the equal effect of unilateral vestibular loss on yaw velocities for turning away from the deficit vs. the non-deficit side would be divergent from the clearly asymmetric responses seen in vestibulo-ocular reflexes (Halmagyi et al, 1990;Palla and Straumann, 2004;Allum and Honegger, 2020a). Vestibulo-spinal influences on trunk muscles are inhibitory.…”

“…Walking among crowds trying to avoid colliding with people is described by patients with vestibular disorder as vertigo-inducing. This is one particular situation where 45% of patients with chronic vestibular disorders, as reported by several clinical centers, noted difficulties with ( Whitney et al, 2016 ), presumably for three reasons: First, finely controlled trunk yaw angular rotations of the patients and linear distances to the obstacle are required to avoid bumping into someone ( Vallis and McFadyen, 2003 ; Olivier et al, 2013 ); second, the head and trunk rotate in phase ( Vallis and McFadyen, 2003 ), permitting easier use of the lateral semi-circular canal signals to control trunk velocities; third, compounding the first two reasons because the lateral vestibular semi-circular responses providing yaw control signals are more commonly affected by acute unilateral vestibular neuritis than the vertical canals ( Allum and Honegger, 2020a ).…”

“…These authors argued that moving the head and trunk segments together simplified the control task for the CNS and reduced the risk of unstable veering behavior. Restricting the degrees of freedom in the yaw plane would have a major advantage for “top-down” sensory integration: First, the peripheral vestibular sensory deficit caused by vestibular neuritis is predominant in the yaw plane ( Taylor et al, 2016 ; Allum and Honegger, 2020a ) and would presumably benefit from such a restriction and, second, allow top-down higher order compensation for the dynamic VOR imbalance via gaze control of the visual system ( Robins and Hollands, 2017 ). Also, the vestibular deficit could then presumably be more easily compensated for at the level of the brainstem mediated by higher cortical network structures involved in spatial orientation ( Lopez et al, 2012 ; Huang et al, 2015 ; Kaski et al, 2016 ), apart from brainstem circuits acting directly to compensate for VOR asymmetries.…”