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Electrophysiological and Neurochemical Considerations of Distinct Neuronal Populations in the Rat Pedunculopontine Nucleus and Their Responsiveness Following 6-Hydroxydopamine Lesions.

ABSTRACT: The pedunculopontine nucleus (PPN) is composed of a morphologically and neurochemically heterogeneous population of neurons, which is severely affected by Parkinson's disease (PD). However, the role of each subtype of neurons within the PPN in the pathophysiology of PD has not been completely elucidated. In this study, we present the discharge profiles of three classified subtypes of PPN neurons and their alterations after 6-hydroxydopamine (6-OHDA) lesion. Following 6-OHDA lesion, the spike timing of the Type II (GABAergic) and Type III (glutamatergic) neurons had phase-lock with the oscillations in the delta and beta band frequency range in the PPN, respectively. Morphological evidence has shown distinct alteration in three kinds of neurons after 6-OHDA lesion. These findings revealed that the changes in the firing characteristics of neurons in PPN in hemi-parkinsonism rats are closely associated with damaged neuronal morphology, which would make contributions to the divergence of dysfunctions in Parkinsonism.

SUBMITTER: Wang X

PROVIDER: S-EPMC6775246 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Electrophysiological and Neurochemical Considerations of Distinct Neuronal Populations in the Rat Pedunculopontine Nucleus and Their Responsiveness Following 6-Hydroxydopamine Lesions.

Wang Xuenan X Geng Xiwen X Li Min M Xie Jinlu J Chen Dadian D Han Hongyu H Meng Xiaoqian X Yao Xiaomeng X Zhang Haiyan H Gao Yunfeng Y Chang Hongli H Zhang Xiao X Wang Yanan Y Wang Min M

Frontiers in neuroscience 20190926

The pedunculopontine nucleus (PPN) is composed of a morphologically and neurochemically heterogeneous population of neurons, which is severely affected by Parkinson's disease (PD). However, the role of each subtype of neurons within the PPN in the pathophysiology of PD has not been completely elucidated. In this study, we present the discharge profiles of three classified subtypes of PPN neurons and their alterations after 6-hydroxydopamine (6-OHDA) lesion. Following 6-OHDA lesion, the spike tim ...[more]

PMID: 31616246

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Project description:BackgroundThe etiology of cervical dystonia is unknown. Cholinergic abnormalities have been identified in dystonia animal models and human imaging studies. Some animal models have cholinergic neuronal loss in the striatum and increased acetylcholinesterase activity in the pedunculopontine nucleus.ObjectivesThe objective of this study was to determine the presence of cholinergic abnormalities in the putamen and pedunculopontine nucleus in cervical dystonia human brain donors.MethodsFormalin-fixed brain tissues were obtained from 8 cervical dystonia and 7 age-matched control brains (controls). Pedunculopontine nucleus was available in only 6 cervical dystonia and 5 controls. Neurodegeneration was evaluated pathologically in the putamen, pedunculopontine nucleus, and other regions. Cholinergic neurons were detected using choline acetyltransferase immunohistochemistry in the putamen and pedunculopontine nucleus. Putaminal cholinergic neurons were quantified. A total of 6 cervical dystonia patients and 6 age-matched healthy controls underwent diffusion tensor imaging to determine if there were white matter microstructural abnormalities around the pedunculopontine nucleus.ResultsDecreased or absent choline acetyltransferase staining was identified in all 6 pedunculopontine nucleus samples in cervical dystonia. In contrast, strong choline acetyltransferase staining was present in 4 of 5 pedunculopontine nucleus controls. There were no differences in pedunculopontine nucleus diffusion tensor imaging between cervical dystonia and healthy controls. There was no difference in numbers of putaminal cholinergic neurons between cervical dystonia and controls.ConclusionsOur findings suggest that pedunculopontine nucleus choline acetyltransferase deficiency represents a functional cholinergic deficit in cervical dystonia. Structural lesions and confounding neurodegenerative processes were excluded by absence of neuronal loss, gliosis, diffusion tensor imaging abnormalities, and beta-amyloid, tau, and alpha-synuclein pathologies. © 2018 International Parkinson and Movement Disorder Society.

Project description:Rats with lesions of the pedunculopontine tegmental nucleus (PPTg) reliably overconsume high concentration sucrose solution. This effect is thought to be indicative of response-perseveration or loss of behavioral control in conditions of high excitement. While these theories have anatomical and behavioral support, they have never been explicitly tested. Here, we used a contact lickometer to examine the microstructure of drinking behavior to gain insight into the behavioral changes during overconsumption. Rats received either excitotoxic (ibotenic acid) damage to all PPTg neuronal subpopulations or selective depletion of the cholinergic neuronal sub-population (diphtheria toxin-urotensin II (Dtx-UII) lesions). We offered rats a variety of pleasant, neutral and aversive tastants to assess the generalizability and specificity of the overconsumption effect. Ibotenic-lesioned rats consumed significantly more 20% sucrose than sham controls, and did so through licking significantly more times. However, the behavioral microstructure during overconsumption was unaffected by the lesion and showed no indications of response-perseveration. Furthermore, the overconsumption effect did not generalize to highly consumed saccharin. In contrast, while only consuming small amounts of quinine solution, ibotenic-lesioned rats had significantly more licks and bursts for this tastant. Selective depletion of cholinergic PPTg neurons had no effect on consumption of any tastant. We then assessed whether it is the salience of the solution which determines overconsumption by ibotenic-lesioned rats. While maintained on free-food, ibotenic-lesioned rats had normal consumption of sucrose and hypertonic saline. After mild food deprivation ibotenic PPTg-lesioned rats overconsumed 20% sucrose. Subsequently, after dietary-induced sodium deficiency, lesioned rats consumed significantly more saline than controls. These results establish that it is the salience of the solution which is the determining factor leading to overconsumption following excitotoxic PPTg lesion. They also find no support for response-perseveration contributing to this effect. Results are discussed in terms of altered dopamine (DA) and salience signaling.

Project description:The brainstem pedunculopontine nucleus has a likely, although unclear, role in gait control, and is a potential deep brain stimulation target for treating resistant gait disorders. These disorders are a major therapeutic challenge for the ageing population, especially in Parkinson's disease where gait and balance disorders can become resistant to both dopaminergic medication and subthalamic nucleus stimulation. Here, we present electrophysiological evidence that the pedunculopontine and subthalamic nuclei are involved in distinct aspects of gait using a locomotor imagery task in 14 patients with Parkinson's disease undergoing surgery for the implantation of pedunculopontine or subthalamic nuclei deep brain stimulation electrodes. We performed electrophysiological recordings in two phases, once during surgery, and again several days after surgery in a subset of patients. The majority of pedunculopontine nucleus neurons (57%) recorded intrasurgically exhibited changes in activity related to different task components, with 29% modulated during visual stimulation, 41% modulated during voluntary hand movement, and 49% modulated during imaginary gait. Pedunculopontine nucleus local field potentials recorded post-surgically were modulated in the beta and gamma bands during visual and motor events, and we observed alpha and beta band synchronization that was sustained for the duration of imaginary gait and spatially localized within the pedunculopontine nucleus. In contrast, significantly fewer subthalamic nucleus neurons (27%) recorded intrasurgically were modulated during the locomotor imagery, with most increasing or decreasing activity phasically during the hand movement that initiated or terminated imaginary gait. Our data support the hypothesis that the pedunculopontine nucleus influences gait control in manners extending beyond simply driving pattern generation. In contrast, the subthalamic nucleus seems to control movement execution that is not likely to be gait-specific. These data highlight the crucial role of these two nuclei in motor control and shed light on the complex functions of the lateral mesencephalus in humans.

Dataset Information

Electrophysiological and Neurochemical Considerations of Distinct Neuronal Populations in the Rat Pedunculopontine Nucleus and Their Responsiveness Following 6-Hydroxydopamine Lesions.

Publications

Electrophysiological and Neurochemical Considerations of Distinct Neuronal Populations in the Rat Pedunculopontine Nucleus and Their Responsiveness Following 6-Hydroxydopamine Lesions.

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