Structural and Functional Neuroplasticity Following Bilateral Vestibular Loss: A Longitudinal [18F]-UCB-H/[18F]-FDG Dual Tracer Rat Study

Abstract

Neuronal lesions trigger mechanisms of structural and functional neuroplasticity, which can support recovery. However, the temporal and spatial appearance of structure-function changes and their interrelation remain unclear. The current study aimed to directly compare serial whole-brain in vivo measurements of functional plasticity (by [18F]-FDG-PET) and structural synaptic plasticity (by [18F]-UCB-H-PET) before and after bilateral labyrinthectomy in rats and investigate the effect of locomotor training. Complex structure-function changes were found after bilateral labyrinthectomy: in brainstem-cerebellar circuits, regional cerebral glucose metabolism (rCGM) decreased early, followed by reduced synaptic density. In the thalamus, increased [18F]-UCB-H binding preceded a higher rCGM uptake. In frontal-basal ganglia loops, an increase in synaptic density was paralleled by a decrease in rCGM. In the group with locomotor training, thalamic rCGM and [18F]-UCB-H binding increased following bilateral labyrinthectomy compared to the no training group. Rats with training had relatively fewer body rotations. In conclusion, combined [18F]-FDG/[18F]-UCB-H dual tracer imaging reveals that adaptive neuroplasticity after bilateral vestibular loss is not a uniform process but is composed of complex spatial and temporal patterns of structure-function coupling in networks for vestibular, multisensory, and motor control, which can be modulated by early physical training.

Recent developments in the understanding of the interactions between the vestibular system, memory, the hippocampus, and the striatum

“…Although the details are still to be elucidated, it is becoming clear that the pedunculopontine tegmental nucleus, which is known to project to the striatum, is also connected to the vestibular nucleus; furthermore, it is evident that PD is associated with major changes in cholinergic pathways involving the vestibular system. The study by Antons et al (48) reinforces previous evidence that vestibular loss is associated with major functional changes in the striatum. Evidence continues to be reported that GVS can modulate the symptoms of PD (23).…”

“…Antons et al (48) undertook a large longitudinal dual tracer study in rats following BVL, using positron emission tomography with computer tomography to measure functional and structural plasticity throughout the brain at 1, 3, 5, 7, and 9 weeks post-lesion. They found significant decreases in glucose metabolism in both the left and right striatum, coupled with increases in synaptic density.…”