Sequential [18F]FDG µPET whole-brain imaging of central vestibular compensation: a model of deafferentation-induced brain plasticity

Abstract

Unilateral inner ear damage is followed by a rapid behavioural recovery due to central vestibular compensation. In this study, we utilized serial [(18)F]Fluoro-deoxyglucose ([(18)F]FDG)-µPET imaging in the rat to visualize changes in brain glucose metabolism during behavioural recovery after surgical and chemical unilateral labyrinthectomy, to determine the extent and time-course of the involvement of different brain regions in vestibular compensation and test previously described hypotheses of underlying mechanisms. Systematic patterns of relative changes of glucose metabolism (rCGM) were observed during vestibular compensation. A significant asymmetry of rCGM appeared in the vestibular nuclei, vestibulocerebellum, thalamus, multisensory vestibular cortex, hippocampus and amygdala in the acute phase of vestibular imbalance (4 h). This was followed by early vestibular compensation over 1-2 days where rCGM re-balanced between the vestibular nuclei, thalami and temporoparietal cortices and bilateral rCGM increase appeared in the hippocampus and amygdala. Subsequently over 2-7 days, rCGM increased in the ipsilesional spinal trigeminal nucleus and later (7-9 days) rCGM increased in the vestibulocerebellum bilaterally and the hypothalamus and persisted in the hippocampus. These systematic dynamic rCGM patterns during vestibular compensation, were confirmed in a second rat model of chemical unilateral labyrinthectomy by serial [(18)F]FDG-µPET. These findings show that deafferentation-induced plasticity after unilateral labyrinthectomy involves early mechanisms of re-balancing predominantly in the brainstem vestibular nuclei but also in thalamo-cortical and limbic areas, and indicate the contribution of spinocerebellar sensory inputs and vestibulocerebellar adaptation at the later stages of behavioural recovery.

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

“…The tone imbalance recovers within weeks as a result of the so-called central vestibular compensation. Central compensation of vestibular tone imbalance elicited by acute unilateral peripheral vestibular failures has been extensively studied in animals [10–12] and humans [13–21]. So far central compensation of a unilateral central lesion of the VN has been documented in humans in a fluordeoxyglucose (FDG)-PET study on Wallenberg’s syndrome [22].…”

Histamine H1 Receptor Contributes to Vestibular Compensation

“…Y. Zhang et al, 2013;. Third, after unilateral labyrinthectomy (UL), elevated expression of H1 receptor in the MVN has been reported (Lacour and Tighilet, 2010;Zhou et al, 2013). Therefore, in the present study, using behavioral assessment combined with Western blot, retrograde tracing, immunostaining, and whole-cell patch-clamp recording, we determine the pathophysiological function of histamine H1 receptor in the vestibular compensation.…”

“…Whole-cell patch-clamp recordings were performed as previously described (J. Zhang et al, 2011;X. Y. Zhang et al, 2013;Zhuang et al, 2018a) on MVN neurons with borosilicate glass pipettes (3-5 M⍀). Pipettes were filled with (in mM): 140 K-methylsulfate, 7 KCl, 2 MgCl 2 , 10 HEPES, 0.1 EGTA, 4 Na 2 -ATP, 0.4 GTP-Tris, and 4% biocytin (Sigma-Aldrich), pH 7.25.…”

“…For intra-MVN microinjections, two stainless-steel guide tubes [length: 1.1 mm, outer diameter (o.d. ): 0.8 mm, inner diameter: 0.5 mm] were bilaterally implanted just above the MVN (A: Ϫ10.9 Ϯ 0.3, L: 1.3 Ϯ 0.2, and H: 3.8) according to the rat brain atlas (Paxinos and Watson, 2014) following stereotactic brain surgery as we described previously (J. Zhang et al, 2011;Wang et al, 2017;Zhuang et al, 2018b). The UL and behavioral assessment were conducted at least 3 d after implantation.…”

“…Negative geotaxis test. This test is considered as a diagnostic of vestibular function, reflex development, and motor skills (Altman and Sudarshan, 1975;J. Zhang et al, 2011).…”