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Open AccessArticle

A Subset of Purposeless Oral Movements Triggered by Dopaminergic Agonists Is Modulated by 5-HT2C Receptors in Rats: Implication of the Subthalamic Nucleus

1
Centre National de la Recherche Scientifique (Unité Mixte de Recherche 5287), 146 Rue Léo Saignat, 33076 Bordeaux CEDEX, France
2
Centre National de la Recherche Scientifique (Unité Mixte de Recherche 5293), 33076 Bordeaux CEDEX, France
3
Neuronal and Neuroendocrine Differentiation and Communication Laboratory, Institute for Research and Innovation in Biomedicine of Normandy (IRIB), Normandie Univ, UNIROUEN, INSERM, U1239, CHU Rouen, 76000 Rouen, France
4
Department of Medical Biochemistry, Rouen University Hospital, 76000 Rouen, France
5
Institut de Recherche Servier, Center for Therapeutic Innovation in Neuropsychiatry, Croissy/Seine, 78290 Paris, France
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2020, 21(22), 8509; https://doi.org/10.3390/ijms21228509
Received: 18 October 2020 / Revised: 4 November 2020 / Accepted: 5 November 2020 / Published: 12 November 2020
Dopaminergic medication for Parkinson’s disease is associated with troubling dystonia and dyskinesia and, in rodents, dopaminergic agonists likewise induce a variety of orofacial motor responses, certain of which are mimicked by serotonin2C (5-HT2C) receptor agonists. However, the neural substrates underlying these communalities and their interrelationship remain unclear. In Sprague-Dawley rats, the dopaminergic agonist, apomorphine (0.03–0.3 mg/kg) and the preferential D2/3 receptor agonist quinpirole (0.2–0.5 mg/kg), induced purposeless oral movements (chewing, jaw tremor, tongue darting). The 5-HT2C receptor antagonist 5-methyl-1-[[2-[(2-methyl-3-pyridyl)oxyl]-5-pyridyl]carbamoyl]-6-trifluoromethylindone (SB 243213) (1 mg/kg) reduced the oral responses elicited by specific doses of both agonists (0.1 mg/kg apomorphine; 0.5 mg/kg quinpirole). After having confirmed that the oral bouts induced by quinpirole 0.5 mg/kg were blocked by another 5-HT2C antagonist (6-chloro-5-methyl-1-[6-(2-methylpiridin-3-yloxy)pyridine-3-yl carbamoyl] indoline (SB 242084), 1 mg/kg), we mapped the changes in neuronal activity in numerous sub-territories of the basal ganglia using c-Fos expression. We found a marked increase of c-Fos expression in the subthalamic nucleus (STN) in combining quinpirole (0.5 mg/kg) with either SB 243213 or SB 242084. In a parallel set of electrophysiological experiments, the same combination of SB 243213/quinpirole produced an irregular pattern of discharge and an increase in the firing rate of STN neurons. Finally, it was shown that upon the electrical stimulation of the anterior cingulate cortex, quinpirole (0.5 mg/kg) increased the response of substantia nigra pars reticulata neurons corresponding to activation of the “hyperdirect” (cortico-subthalamonigral) pathway. This effect of quinpirole was abolished by the two 5-HT2C antagonists. Collectively, these results suggest that induction of orofacial motor responses by D2/3 receptor stimulation involves 5-HT2C receptor-mediated activation of the STN by recruitment of the hyperdirect (cortico-subthalamonigral) pathway. View Full-Text
Keywords: single cell extracellular recording; basal ganglia; c-fos; quinpirole; orofacial; electrical stimulation; substantia nigra pars reticulata; 5-HT2C antagonist; anterior cingulate cortex; compulsive disorder single cell extracellular recording; basal ganglia; c-fos; quinpirole; orofacial; electrical stimulation; substantia nigra pars reticulata; 5-HT2C antagonist; anterior cingulate cortex; compulsive disorder
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MDPI and ACS Style

Lagière, M.; Bosc, M.; Whitestone, S.; Benazzouz, A.; Chagraoui, A.; Millan, M.J.; De Deurwaerdère, P. A Subset of Purposeless Oral Movements Triggered by Dopaminergic Agonists Is Modulated by 5-HT2C Receptors in Rats: Implication of the Subthalamic Nucleus. Int. J. Mol. Sci. 2020, 21, 8509.

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