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The Journal of Neuroscience, July 22, 2009, 29(29):9281-9291; doi:10.1523/JNEUROSCI.1865-09.2009

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Cellular/Molecular
Activation of Metabotropic Glutamate Receptors Induces Periodic Burst Firing and Concomitant Cytosolic Ca²⁺ Oscillations in Cerebellar Interneurons

Thibault Collin,^1,2 Romain Franconville,¹ Barbara E. Ehrlich,³ and Isabel Llano¹

¹Centre National de la Recherche Scientifique, Laboratoire de Physiologie Cérébrale, Université Paris Descartes, Paris 75006, France, ²Université Paris Diderot, Paris 75013, France, and ³Department of Pharmacology and Cellular and Molecular Physiology, Yale University, New Haven, Connecticut 06520

Correspondence should be addressed to Isabel Llano, Laboratoire de Physiologie Cérébrale, Université Paris Descartes, 45 rue des Saints Pères, Paris 75006, France. Email: isabel.llano{at}parisdescartes.fr

Little is known about the generation of slow rhythms in brain neuronal circuits. Nevertheless, a few studies, both from reconstituted systems and from hippocampal slices, indicate that activation of metabotropic glutamate receptors (mGluRs) could generate such rhythms. Here we show in rat cerebellar slices that after either release of glutamate by repetitive stimulation, or direct stimulation of type 1 mGluRs, molecular layer interneurons exhibit repetitive slow Ca²⁺ transients. By combining cell-attached patch-clamp recording with Ca²⁺ imaging, we show that the regular Ca²⁺ transients (mean frequency, 35 mHz induced by 2 µM quisqualate in the presence of ionotropic glutamate receptor blockers) are locked with bursts of action potentials. Nevertheless, the Ca²⁺ transients are not blocked by tetrodotoxin, indicating that firing is not necessary to entrain oscillations. The first Ca²⁺ transient within a train is different in several ways from subsequent transients. It is broader than the subsequent transients, displays a different phase relationship to associated spike bursts, and exhibits a distinct sensitivity to ionic and pharmacological manipulations. Whereas the first transient appears to involve entry of Ca²⁺ ions through transient receptor potential channel-like channels and secondarily activated L-type Ca²⁺ channels, subsequent transients rely mostly on an exchange of Ca²⁺ ions between the cytosol and D-myo-inositol-1,4,5-triphosphate-sensitive intracellular Ca²⁺ stores. The slow, highly regular oscillations observed in the present work are likely to drive pauses in postsynaptic Purkinje cells, and could play a role in coordinating slow oscillations involving the cerebello-olivar circuit loop.

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Received April 20, 2009; revised June 12, 2009; accepted June 17, 2009.

Correspondence should be addressed to Isabel Llano, Laboratoire de Physiologie Cérébrale, Université Paris Descartes, 45 rue des Saints Pères, Paris 75006, France. Email: isabel.llano{at}parisdescartes.fr

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