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The Journal of Neuroscience, August 20, 2003, 23(20):7677-7684

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Motor Dysfunction and Altered Synaptic Transmission at the Parallel Fiber-Purkinje Cell Synapse in Mice Lacking Potassium Channels Kv3.1 and Kv3.3

Hiroshi Matsukawa,^1 * Alexander M. Wolf,^1 * Shinichi Matsushita,^1 * Rolf H. Joho,^1,2 and Thomas Knöpfel¹

¹Laboratory for Neuronal Circuit Dynamics, RIKEN Brain Science Institute, Wako, Japan 351-0198, and ²Center for Basic Neuroscience, The University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111

Micelacking both Kv3.1 and both Kv3.3 K⁺ channel alleles display severe motor deficits such as tremor, myoclonus, and ataxic gait. Micelacking one to three alleles at the Kv3.1 and Kv3.3 loci exhibit in an allele dose-dependent manner a modest degree of ataxia. Cerebellar granule cells coexpress Kv3.1 and Kv3.3 K⁺ channels and are therefore candidate neurons that might be involved in these behavioral deficits. Hence, we investigated the synaptic mechanisms of transmission in the parallel fiber-Purkinje cell system. Action potentials of parallel fibers were broader in mice lacking both Kv3.1 and both Kv3.3 alleles and in mice lacking both Kv3.1 and a single Kv3.3 allele compared with those of wild-type mice. The transmission of high-frequency trains of action potentials was only impaired at 200 Hz but not at 100 Hz in mice lacking both Kv3.1 and Kv3.3 genes. However, paired-pulse facilitation (PPF) at parallel fiber-Purkinje cell synapses was dramatically reduced in a gene dose-dependent manner in mice lacking Kv3.1 or Kv3.3 alleles. Normal PPF could be restored by reducing the extracellular Ca²⁺ concentration indicating that increased activity-dependent presynaptic Ca²⁺ influx, at least in part caused the altered PPF in mutant mice. Induction of metabotropic glutamate receptor-mediated EPSCs was facilitated, whereas longterm depression was not impaired but rather facilitated in Kv3.1/Kv3.3 double-knockout mice. These results demonstrate the importance of Kv3 potassium channels in regulating the dynamics of synaptic transmission at the parallel fiber-Purkinje cell synapse and suggest a correlation between short-term plasticity at the parallel fiber-Purkinje cell synapse and motor performance.

Key words: cerebellar cortex; parallel fibers; Kv channels; synaptic transmission; presynaptic mechanisms; action potential repolarization; voltage-sensitive dyes

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Received Jan. 8, 2003; revised Jun. 23, 2003; accepted Jun. 30, 2003.

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