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The Journal of Neuroscience, June 28, 2006, 26(26):6997-7006; doi:10.1523/JNEUROSCI.5515-05.2006

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Cellular/Molecular
Glutamatergic Control of Microvascular Tone by Distinct GABA Neurons in the Cerebellum

Armelle Rancillac,¹ Jean Rossier,¹ Manon Guille,² Xin-Kang Tong,³ Hélène Geoffroy,¹ Christian Amatore,² Stéphane Arbault,² Edith Hamel,³ and Bruno Cauli¹

¹Laboratoire de Neurobiologie et Diversité Cellulaire, Centre National de la Recherche Scientifique (CNRS), Unité Mixte de Recherche (UMR) 7637, Ecole Supérieure de Physique et de Chimie Industrielles de la ville de Paris, and ²Laboratoire "Processus d’Activation Sélective par Transfert d’Energie Uni-électronique ou Radiatif," CNRS, UMR 8640, Université Pierre et Marie Curie, Ecole Normale Supérieure, 75005 Paris, France, and ³Laboratory of Cerebrovascular Research, Montreal Neurological Institute, McGill University, Montréal, Québec, Canada H3A 2B4

Correspondence should be addressed to Dr. Bruno Cauli, Neurobiologie et Diversité Cellulaire, Unité Mixte de Recherche 7637, 10 rue Vauquelin, 75005 Paris, France. Email: bruno.cauli{at}espci.fr

The tight coupling between increased neuronal activity and local cerebral blood flow, known as functional hyperemia, is essential for normal brain function. However, its cellular and molecular mechanisms remain poorly understood. In the cerebellum, functional hyperemia depends almost exclusively on nitric oxide (NO). Here, we investigated the role of different neuronal populations in the control of microvascular tone by in situ amperometric detection of NO and infrared videomicroscopy of microvessel movements in rat cerebellar slices. Bath application of an NO donor induced both NO flux and vasodilation. Surprisingly, endogenous release of NO elicited by glutamate was accompanied by vasoconstriction that was abolished by inhibition of Ca²⁺-phopholipase A2 and impaired by cyclooxygenase and thromboxane synthase inhibition and endothelin A receptor blockade, indicating a role for prostanoids and endothelin 1 in this response. Interestingly, direct stimulation of single endothelin 1-immunopositive Purkinje cells elicited constriction of neighboring microvessels. In contrast to glutamate, NMDA induced both NO flux and vasodilation that were abolished by treatment with a NO synthase inhibitor or with tetrodotoxin. These findings indicate that NO derived from neuronal origin is necessary for vasodilation induced by NMDA and, furthermore, that NO-producing interneurons mediate this vasomotor response. Correspondingly, electrophysiological stimulation of single nitrergic stellate cells by patch clamp was sufficient to release NO and dilate both intraparenchymal and upstream pial microvessels. These findings demonstrate that cerebellar stellate and Purkinje cells dilate and constrict, respectively, neighboring microvessels and highlight distinct roles for different neurons in neurovascular coupling.

Key words: stellate cells; Purkinje cells; NO; amperometry; patch clamp; sphincter

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Received July 28, 2005; revised April 14, 2006; accepted April 28, 2006.

Correspondence should be addressed to Dr. Bruno Cauli, Neurobiologie et Diversité Cellulaire, Unité Mixte de Recherche 7637, 10 rue Vauquelin, 75005 Paris, France. Email: bruno.cauli{at}espci.fr

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