Abstract
The present study in rats was conducted to identify brain regions affected by the interruption of vestibular transmission and to explore selected aspects of their functional connections. We analyzed, by positron emission tomography (PET), the regional cerebral glucose metabolism (rCGM) of cortical, and subcortical cerebral regions processing vestibular signals after an experimental lesion of the left laterodorsal thalamic nucleus, a relay station for vestibular input en route to the cortical circuitry. PET scans upon galvanic vestibular stimulation (GVS) were conducted in each animal prior to lesion and at post-lesion days (PLD) 1, 3, 7, and 20, and voxel-wise statistical analysis of rCGM at each PLD compared to pre-lesion status were performed. After lesion, augmented metabolic activation by GVS was detected in cerebellum, mainly contralateral, and in contralateral subcortical structures such as superior colliculus, while diminished activation was observed in ipsilateral visual, entorhinal, and somatosensory cortices, indicating compensatory processes in the non-affected sensory systems of the unlesioned side. The changes in rCGM observed after lesion resembled alterations observed in patients suffering from unilateral thalamic infarction and may be interpreted as brain plasticity mechanisms associated with vestibular compensation and substitution. The second set of experiments aimed at the connections between cortical and subcortical vestibular regions and their neurotransmitter systems. Neuronal tracers were injected in regions processing vestibular and somatosensory information. Injections into the anterior cingulate cortex (ACC) or the primary somatosensory cortex (S1) retrogradely labeled neuronal somata in ventral posteromedial (VPM), posterolateral (VPL), ventrolateral (VL), posterior (Po), and laterodorsal nucleus, dorsomedial part (LDDM), locus coeruleus, and contralateral S1 area. Injections into the parafascicular nucleus (PaF), VPM/VPL, or LDDM anterogradely labeled terminal fields in S1, ACC, insular cortex, hippocampal CA1 region, and amygdala. Immunohistochemistry showed tracer-labeled terminal fields contacting cortical neurons expressing the μ-opioid receptor. Antibodies to tyrosine hydroxylase, serotonin, substance P, or neuronal nitric oxide-synthase did not label any of the traced structures. These findings provide evidence for opioidergic transmission in thalamo-cortical transduction.
Highlights
The bilateral central vestibular system provides an excellent paradigm to study mechanisms of brain plasticity, since it is able to compensate a certain loss of function by reorganizing its neurotransmission parameters (“vestibular compensation,” VC)
Our previous rat data showing that galvanic vestibular stimulation (GVS) activates regional cerebral glucose metabolism (rCGM) in distinct cortical and subcortical regions characterized those as part of a vestibular network
Our present data of a rat model with unilateral thalamic lesions demonstrate that GVS resulted in augmented activation of contralateral cerebellum and distinct subcortical structures such as superior colliculus as well as diminished activation of ipsilateral sensory cortical regions, showing a distinct pattern measured during 20 days post lesion
Summary
The bilateral central vestibular system provides an excellent paradigm to study mechanisms of brain plasticity, since it is able to compensate a certain loss of function by reorganizing its neurotransmission parameters (“vestibular compensation,” VC). Neuronal plasticity underlying VC include changes in the physiological properties of afferents in the end-organ, mediated through the efferent system, as well as changes in the function of the vestibulocerebellum and its projection to the brainstem vestibular nuclei [VN; [15,16,17]] These involve functional changes in neurotransmitter systems using G-aminobutyric acid (GABA), acetylcholine (ACh), glutamate and, in particular, dopamine, and their receptors [cf [18,19,20]]. These effects were observed in the VN, the target structure of the vestibular organ, in studies focusing on intact central processing structures and compensation following experimental labyrinthectomy in animal models [6, 14, 18,19,20,21,22,23,24,25] or in acquired peripheral lesions in patients [11, 13, 14, 26, 27]
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