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.
Highlights
The vestibular system is organized bilaterally with ascending and descending pathways; they cross three times in the brainstem and at least once in the hemispheres between vestibular cortex areas [1,2]
Relevant structures in the brainstem circuitry for processing vestibular information are the vestibular nuclei (VN) in the pontomedullary brainstem and an assembly of nuclei for eye-head integration in the midbrain tegmentum including the interstitial nucleus of Cajal (INC), the rostral interstitial nucleus of the medial longitudinal fasciculus, the oculomotor nucleus with paired and unpaired subnuclei, and the posterior commissure (PC)
Unilateral midbrain lesions of the INC typically manifest with ocular tilt reaction (OTR) [6,7]
Summary
The vestibular system is organized bilaterally with ascending and descending pathways; they cross three times in the brainstem and at least once in the hemispheres between vestibular cortex areas [1,2]. The two clinical vestibular syndromes, elicited at different levels of the brainstem, share certain signs and symptoms They differ, in the direction of tilts of the OTR, which is ipsiversive at the pontomedullary and typically contraversive at the mesencephalic level because of the pontine crossing of the graviceptive pathways [7]. A major structural difference between the VNs and the midbrain nuclei is that right and left VNs are anatomically clearly separated, whereas the paramedian midbrain nuclei seem to form a structural and presumably functionally connected neuronal assembly [8] These structures have tight reciprocal as well as commissural connections to their contralateral nuclei; some of them are excitatory, others inhibitory [9], ensuring in part the close vertical coupling of the two eyes and their stabilization
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