Dopaminergic modulation of primary motor cortex: From cellular and synaptic mechanisms underlying motor learning to cognitive symptoms in Parkinson’s disease

Cousineau, Jérémy; Plateau, Valentin; Baufreton, Jérôme; Bon-Jégo, Morgane Le

doi:10.1016/j.nbd.2022.105674

Cited by 27 publications

(28 citation statements)

References 206 publications

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“…They are responsible for short intracortical inhibition of pyramidal neurons by synapsing on pyramidal axonal initial segments as well as their dendrites [ 63 ] and increase their axonal aborisation and myelination in response to increased activity [ 58 ]. Reduced effectiveness of short intracortical inhibition in the motor cortex is the most reliable abnormality identified in motor PD thought to be due to saturated activity of these neurons [ 17 , 23 ], with dopamine input modulating this inhibitory network [ 13 ]. An increase in cortical myelination could indicate increased arborization and activity of such motor cortex interneurons which would result in increased inhibition to and hypoactivity of their targeted pyramidal neurons, and also parallel an increase in NFL and the dendritic arbor of their targeted neurons.…”

Section: Discussionmentioning

confidence: 99%

Adaptive structural changes in the motor cortex and white matter in Parkinson’s disease

Zhou

Liu

et al. 2022

Acta Neuropathol

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Parkinson’s disease (PD) is a movement disorder characterized by the early loss of nigrostriatal dopaminergic pathways producing significant network changes impacting motor coordination. Recently three motor stages of PD have been proposed (a silent period when nigrostriatal loss begins, a prodromal motor period with subtle focal manifestations, and clinical PD) with evidence that motor cortex abnormalities occur to produce clinical PD[8]. We directly assess structural changes in the primary motor cortex and corticospinal tract using parallel analyses of longitudinal clinical and cross-sectional pathological cohorts thought to represent different stages of PD. 18F-FP-CIT positron emission tomography and subtle motor features identified patients with idiopathic rapid-eye-movement sleep behaviour disorder (n = 8) that developed prodromal motor signs of PD. Longitudinal diffusion tensor imaging before and after the development of prodromal motor PD showed higher fractional anisotropy in motor cortex and corticospinal tract compared to controls, indicating adaptive structural changes in motor networks in concert with nigrostriatal dopamine loss. Histological analyses of the white matter underlying the motor cortex showed progressive disorientation of axons with segmental replacement of neurofilaments with α-synuclein, enlargement of myelinating oligodendrocytes and increased density of their precursors. There was no loss of neurons in the motor cortex in early or late pathologically confirmed motor PD compared to controls, although there were early cortical increases in neuronal neurofilament light chain and myelin proteins in association with α-synuclein accumulation. Our results collectively provide evidence of a direct impact of PD on primary motor cortex and its output pathways that begins in the prodromal motor stage of PD with structural changes confirmed in early PD. These adaptive structural changes become considerable as the disease advances potentially contributing to motor PD.

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Section: Discussionmentioning

confidence: 99%

Adaptive structural changes in the motor cortex and white matter in Parkinson’s disease

Zhou

Liu

et al. 2022

Acta Neuropathol

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“…52 The frontal cortex has been associated with psychotic and cognitive symptoms of PD. 53,54 We assessed autophagy in those regions, as it is relevant to both the ECS and PD as explained in the introduction section. Autophagy process can be viewed as a double-edged sword according to its context-dependent cellular consequences: it is one of the traditional apoptotic processes inducing neuronal cell death, while its induction could promote neuroprotective action through increased clearance of neurotoxic materials.…”

Section: Discussionmentioning

confidence: 99%

Electroconvulsive Seizure Normalizes Motor Deficits and Induces Autophagy Signaling in the MPTP-Induced Parkinson Disease Mouse Model

Huh

Kang

et al. 2023

Psychiatry Investig

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Objective Electroconvulsive seizure (ECS) is a potent treatment modality for various neuropsychiatric diseases, including Parkinson disease (PD). Recent animal studies showed that repeated ECS activates autophagy signaling, the impairment of which is known to be involved in PD. However, the effectiveness of ECS on PD and its therapeutic mechanisms have not yet been investigated in detail.Methods Systemic injection of a neurotoxin 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride (MPTP), which destroys dopaminergic neurons in the substantia nigra compacta (SNc), in mice was utilized to induce an animal model of PD. Mice were treated with ECS 3 times per week for 2 weeks. Behavioral changes were measured with a rotarod test. Molecular changes related to autophagy signaling in midbrain including SNc, striatum, and prefrontal cortex were analyzed with immunohistochemistry and immunoblot analyses.Results Repeated ECS treatments normalized the motor deficits and the loss of dopamiergic neurons in SNc of the MPTP PD mouse model. In the mouse model, LC3-II, an autophagy marker, was increased in midbrain while decreased in prefrontal cortex, both of which were reversed by repeated ECS treatments. In the prefrontal cortex, ECS-induced LC3-II increase was accompanied with AMP-activated protein kinase (AMPK)-Unc-51-like kinase 1-Beclin1 pathway activation and inhibition of mamalian target of rapamycin signaling which promotes autophagy initiation.Conclusion The findings revealed the therapeutic effects of repeated ECS treatments on PD, which could be attributed to the neuroprotective effect of ECS mediated by AMPK-autophagy signaling.

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“…46 Its mechanism may involve the establishment of new synapses 47 and dopaminergic projections from midbrain to M1. 42 On the flip side, the experimentally supplied water bolus's temperature below body temperature 42,48 and its difference in viscosity with saliva 49 may have also enhanced sensory-motor association to activate M1. 43 However, as we did not find significant sensory cortical activation in water swallowing, it is not clear which region of M1 integrates the sensory information afferent to it.…”

Section: Discussionmentioning

confidence: 99%

Brain functional activity of swallowing: A meta‐analysis of functional magnetic resonance imaging

Huang

Yan

Lin

et al. 2022

J of Oral Rehabilitation

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Background: Swallowing is one of the most important activities in our life and serves the dual roles of nutritional intake and eating enjoyment. Objective:The study aimed to conduct a meta-analysis to investigate the brain activity of swallowing.Methods: Studies of swallowing using functional magnetic resonance imaging were reviewed in PubMed, Web of Science, China National Knowledge Infrastructure (CNKI), Chinese Science and Technology Periodical Database (VIP) and Wan Fang before 30 November 2021. Two authors analysed the studies for eligibility criteria. The final inclusion of studies was decided by consensus. An activation likelihood estimation (ALE) meta-analysis of these studies was performed with GingerALE, including 16 studies.Results: For swallowing, clusters with high activation likelihood were found in the bilateral insula, bilateral pre-central gyrus, bilateral post-central gyrus, left transverse temporal gyrus, right medial front gyrus, bilateral inferior frontal gyrus and bilateral cingulate gyrus. For water swallowing, clusters with high activation likelihood were found in the bilateral inferior frontal gyrus and the left pre-central gyrus. For saliva swallowing, clusters with high activation likelihood were found in the bilateral cingulate gyrus, bilateral pre-central gyrus, left post-central gyrus and left transverse gyrus. Conclusion:This meta-analysis reflects that swallowing is regulated by both sensory and motor cortex, and saliva swallowing activates more brain areas than water swallowing, which would promote our knowledge of swallowing and provide some direction for clinical and other research.

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Dopaminergic modulation of primary motor cortex: From cellular and synaptic mechanisms underlying motor learning to cognitive symptoms in Parkinson’s disease

Cited by 27 publications

References 206 publications

Adaptive structural changes in the motor cortex and white matter in Parkinson’s disease

Adaptive structural changes in the motor cortex and white matter in Parkinson’s disease

Electroconvulsive Seizure Normalizes Motor Deficits and Induces Autophagy Signaling in the MPTP-Induced Parkinson Disease Mouse Model

Brain functional activity of swallowing: A meta‐analysis of functional magnetic resonance imaging

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