Functional Plasticity after Unilateral Vestibular Midbrain Infarction in Human Positron Emission Tomography

Abstract

The aim of the study was to uncover mechanisms of central compensation of vestibular function at brainstem, cerebellar, and cortical levels in patients with acute unilateral midbrain infarctions presenting with an acute vestibular tone imbalance. Eight out of 17 patients with unilateral midbrain infarctions were selected on the basis of signs of a vestibular tone imbalance, e.g., graviceptive (tilts of perceived verticality) and oculomotor dysfunction (skew deviation, ocular torsion) in F18-fluordeoxyglucose (FDG)-PET at two time points: A) in the acute stage, and B) after recovery 6 months later. Lesion-behavior mapping analyses with MRI verified the exact structural lesion sites. Group subtraction analyses and comparisons with healthy controls were performed with Statistic Parametric Mapping for the PET data. A comparison of PET A of acute-stage patients with that of healthy controls showed increases in glucose metabolism in the cerebellum, motion-sensitive visual cortex areas, and inferior temporal lobe, but none in vestibular cortex areas. At the supratentorial level bilateral signal decreases dominated in the thalamus, frontal eye fields, and anterior cingulum. These decreases persisted after clinical recovery in contrast to the increases. The transient activations can be attributed to ocular motor and postural recovery (cerebellum) and sensory substitution of vestibular function for motion perception (visual cortex). The persisting deactivation in the thalamic nuclei and frontal eye fields allows alternative functional interpretations of the thalamic nuclei: either a disconnection of ascending sensory input occurs or there is a functional mismatch between expected and actual vestibular activity. Our data support the view that both thalami operate separately for each hemisphere but receive vestibular input from ipsilateral and contralateral midbrain integration centers. Normally they have gatekeeper functions for multisensory input to the cortex and automatic motor output to subserve balance and locomotion, as well as sensorimotor integration.

Why acute unilateral vestibular midbrain lesions rarely manifest with rotational vertigo: a clinical and modelling approach to head direction cell function

“…The following functions were assessed: clinical head impulse test, rapid and smooth pursuit eye movements, gaze and ocular motor nerve function, spontaneous-, optokinetic- and gaze-evoked nystagmus, spontaneous deviation from normal head upright position, and signs of graviceptive (otolith/vertical semicircular canal) dysfunction. It was also checked for a vestibular tone imbalance in the roll plane, i.e., the components of an ocular tilt reaction (OTR) such as head tilt, skew deviation, ocular torsion, and perception of subjective visual vertical (SVV) [ 17 , 38 ]. Fundus photography was performed with a laser ophthalmoscope to determine ocular torsion.…”

“…In all 8 patients the strokes caused a sustained instability of stance and gait with skew torsion of the eyes. Only one patient reported an initially transient rotatory vertigo, two a swaying vertigo, and five no vertigo/dizziness at all (modified from [ 17 ]). EW Edinger–Westphal nucleus, icp nucleus intracapsularis, IIIpr nucleus oculomotorius principalis …”

“…The clinical manifestation of more cranial unilateral vestibular lesions in the meso-diencephalic brainstem and the vestibular cortex differs. In a small case study of eight patients with acute unilateral lesions of the midbrain, only one patient initially had rotational vertigo and two, swaying vertigo [ 17 ] (Fig. 1 b).…”

Global multisensory reorganization after vestibular brain stem stroke

“…Bense and colleagues found signal decreases in visual cortex in pontomedullary infarcts and decreases in the premotor cortex in both pontomedullary and pontomesencephalic infarcts with functional imaging. 25,26 However, structural plasticity, that is, an increase of GMV and WMV in the cortical multisensory vestibular areas following unilateral brain stem infarcts has not been demonstrated before. Apart from the inherent differences in these two methods, we used a thorough state-of-theart preprocessing and analysis algorithm that allows subtle changes in GMV to be detected and is corrected for type 1 errors (TFCE with FWE correction for multiple comparisons) which could additionally explain the differences between ours and the former studies.…”

“…[20][21][22] Central compensation in central vestibular lesions has only been investigated in a few studies using PET and functional MRI. [23][24][25][26] The current study used voxel-based morphometry (VBM) to evaluate changes in gray matter volume (GMV) and white matter volume (WMV) over time in 24 patients with acute unilateral brain stem infarcts presenting with vestibular or ocular motor deficits, compared to the baseline (acute phase). 27 A group of healthy age-and gendermatched participants (HC) served as a control group.…”