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The Journal of Neuroscience, March 10, 2004, 24(10):2440-2448; doi:10.1523/JNEUROSCI.0783-03.2004

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Behavioral/Systems/Cognitive
Oscillating Purkinje Neuron Activity Causing Involuntary Eye Movement in a Mutant Mouse Deficient in the Glutamate Receptor 2 Subunit

Takashi Yoshida,^1,2 * Akira Katoh,^1,2 * Gen Ohtsuki,^1,2 Masayoshi Mishina,^2,3 and Tomoo Hirano^1,2

¹Department of Biophysics, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan, ² Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Saitama 332-0012, Japan, and ³Department of Molecular Neurobiology and Pharmacology, School of Medicine, University of Tokyo, and Solution Oriented Research for Science and Technology, Tokyo 113-0033, Japan

How failures in regulation of synaptic transmission in the mammalian CNS affect neuronal activity and disturb motor coordination is addressed. The mutant mouse deficient in the glutamate receptor 2 subunit, specifically expressed in cerebellar Purkinje neurons, has defects in synaptic regulations such as synaptic plasticity, stabilization, and elimination of synaptic connections and shows failures in motor coordination and learning. In this study, the cause of motor discoordination of the 2 mutant mouse was analyzed by comparing its motor control ability with those of the wild-type mouse and the lurcher mutant mouse, which loses all Purkinje neurons, the sole output neurons in the cerebellar cortex. Unexpectedly, the 2 mutant mouse showed severer motor discoordination than the lurcher mouse without any cerebellar cortical outputs. The 2 mutant mouse showed involuntary spontaneous eye movement with characteristic 10 Hz oscillation, which disappeared by ablation of the cerebellar flocculus, suggesting that the 2 mutant cerebellar cortex outputs an abnormal signal. In vivo extracellular recordings of neuronal activity revealed that Purkinje neurons tended to fire clustered action potentials and complex spikes at 10 Hz in the 2 mutant mouse. A whole-cell patch-clamp recording from Purkinje neurons in cerebellar slices indicated that the clustered action potentials could be induced by climbing fiber activation. Taken together, our results suggest that the 2 subunit deficiency produces the oscillating activity in Purkinje neurons by enhancing climbing fiber inputs, causing surplus movement and affecting motor control worse than no signal at all.

Key words: Purkinje cell; motor control; glutamate receptor; knock-out mouse; oscillation; eye movement; 2 subunit; climbing fiber

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Received March 17, 2003; revised December 11, 2003; accepted January 13, 2004.

This article has been cited by other articles:

				M. Beraneck, J. L. McKee, M. Aleisa, and K. E. Cullen Asymmetric Recovery in Cerebellar-Deficient Mice Following Unilateral Labyrinthectomy J Neurophysiol, August 1, 2008; 100(2): 945 - 958. [Abstract] [Full Text] [PDF]

				N. Wada, Y. Kishimoto, D. Watanabe, M. Kano, T. Hirano, K. Funabiki, and S. Nakanishi Conditioned eyeblink learning is formed and stored without cerebellar granule cell transmission PNAS, October 16, 2007; 104(42): 16690 - 16695. [Abstract] [Full Text] [PDF]

				G. Ohtsuki, S.-y. Kawaguchi, M. Mishina, and T. Hirano Enhanced Inhibitory Synaptic Transmission in the Cerebellar Molecular Layer of the GluR{delta}2 Knock-Out Mouse J. Neurosci., December 1, 2004; 24(48): 10900 - 10907. [Abstract] [Full Text] [PDF]

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