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The Journal of Neuroscience, August 5, 2009, 29(31):9668-9682; doi:10.1523/JNEUROSCI.0362-09.2009

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Cellular/Molecular
Functional Coupling between mGluR1 and Ca_v3.1 T-Type Calcium Channels Contributes to Parallel Fiber-Induced Fast Calcium Signaling within Purkinje Cell Dendritic Spines

Michael E. Hildebrand,^1 * Philippe Isope,^2 * Taisuke Miyazaki,⁶ Toshitaka Nakaya,⁶ Esperanza Garcia,¹ Anne Feltz,² Toni Schneider,⁵ Jürgen Hescheler,⁵ Masanobu Kano,³ Kenji Sakimura,⁴ Masahiko Watanabe,⁶ Stéphane Dieudonné,² and Terrance P. Snutch¹

¹Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada, ²Laboratoire de Neurobiologie, Ecole Normale Supérieure, Centre National de la Recherche Scientifique, 75005 Paris, France, ³Department of Neurophysiology, Graduate School of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan, ⁴Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Niigata 951-8585, Japan, ⁵Institute of Neurophysiology and Center for Molecular Medicine Cologne, University of Cologne, D-50931 Cologne, Germany, and ⁶Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan

Correspondence should be addressed to Dr. Terrance P. Snutch, Michael Smith Laboratories, University of British Columbia, 2185 East Mall, Vancouver, BC V6T 1Z4, Canada. Email: snutch{at}msl.ubc.ca

T-type voltage-gated calcium channels are expressed in the dendrites of many neurons, although their functional interactions with postsynaptic receptors and contributions to synaptic signaling are not well understood. We combine electrophysiological and ultrafast two-photon calcium imaging to demonstrate that mGluR1 activation potentiates cerebellar Purkinje cell Ca_v3.1 T-type currents via a G-protein- and tyrosine-phosphatase-dependent pathway. Immunohistochemical and electron microscopic investigations on wild-type and Ca_v3.1 gene knock-out animals show that Ca_v3.1 T-type channels are preferentially expressed in Purkinje cell dendritic spines and colocalize with mGluR1s. We further demonstrate that parallel fiber stimulation induces fast subthreshold calcium signaling in dendritic spines and that the synaptic Ca_v3.1-mediated calcium transients are potentiated by mGluR1 selectively during bursts of excitatory parallel fiber inputs. Our data identify a new fast calcium signaling pathway in Purkinje cell dendritic spines triggered by short burst of parallel fiber inputs and mediated by T-type calcium channels and mGluR1s.

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Received Jan. 22, 2009; revised June 12, 2009; accepted June 17, 2009.

Correspondence should be addressed to Dr. Terrance P. Snutch, Michael Smith Laboratories, University of British Columbia, 2185 East Mall, Vancouver, BC V6T 1Z4, Canada. Email: snutch{at}msl.ubc.ca

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