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The Journal of Neuroscience, February 18, 2004, 24(7):1734-1743; doi:10.1523/JNEUROSCI.4208-03.2004

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Development/Plasticity/Repair
P/Q-Type Ca²⁺ Channel 1A Regulates Synaptic Competition on Developing Cerebellar Purkinje Cells

Taisuke Miyazaki,^1 * Kouichi Hashimoto,^2 * Hee-Sup Shin,³ Masanobu Kano,² and Masahiko Watanabe¹

¹Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan, ²Department of Cellular Neurophysiology, Graduate School of Medical Science, Kanazawa University, Takara-machi, Kanazawa 920-8640, Japan, and ³National Creative Research Initiative Center for Calcium and Learning, Korea Institute of Science and Technology, Seongbuk-ku, Seoul 136-791, Korea

Synapse formation depends critically on the competition among inputs of multiple sources to individual neurons. Cerebellar Purkinje cells have highly organized synaptic wiring from two distinct sources of excitatory afferents. Single climbing fibers innervate proximal dendrites of Purkinje cells, whereas numerous parallel fibers converge on their distal dendrites. Here, we demonstrate that the P/Q-type Ca²⁺ channel 1A, a major Ca²⁺ channel subtype in Purkinje cells, is crucial for this organized synapse formation. In the 1A knock-out mouse, many ectopic spines were protruded from proximal dendrites and somata of Purkinje cells. Innervation territory of parallel fibers was expanded proximally to innervate the ectopic spines, whereas that of climbing fibers was regressed to the basal portion of proximal dendrites and somata. Furthermore, multiple climbing fibers consisting of a strong climbing fiber and one or a few weaker climbing fibers, persisted in the majority of Purkinje cells and were cowired to the same somata, proximal dendrites, or both. Therefore, the lack of 1A results in the persistence of parallel fibers and surplus climbing fibers, which should normally be expelled from the compartment innervated by the main climbing fiber. These results suggest that a P/Q-type Ca²⁺ channel 1A fuels heterosynaptic competition between climbing fibers and parallel fibers and also fuels homosynaptic competition among multiple climbing fibers. This molecular function facilitates the distal extension of climbing fiber innervation along the dendritic tree of the Purkinje cell and also establishes climbing fiber monoinnervation of individual Purkinje cells.

Key words: cerebellum; Purkinje cell; climbing fiber; parallel fiber; P/Q-type calcium channel; 1A subunit; development; synapse formation

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Received Sep 13, 2003; revised December 9, 2003; accepted December 10, 2003.

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