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The Journal of Neuroscience, July 16, 2003, 23(15):6200-6208

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Muscarine-Induced Increase in Frequency of Spontaneous EPSCs in Purkinje Cells in the Vestibulo-Cerebellum of the Rat

Yukihiro Takayasu,^1,2,3 Masae Iino,^1,3 Nobuhiko Furuya,² and Seiji Ozawa^1,3

Departments of ¹Physiology and ²Otolaryngology, Gunma University School of Medicine, Maebashi, Gunma, 371-8511, Japan, and ³Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 322-0012, Japan

Cholinergic projections are relatively sparse in the cerebellum compared with other parts of the brain. However, some mossy fibers in the vestibulo-cerebellum are known to be cholinergic. To clarify the functional roles of cholinergic mossy fibers in the vestibulo-cerebellum, we investigated the effects of acetylcholine (ACh) on the membrane electrical properties of both granule cells and Purkinje cells in slices of the cerebellar vermis of the rat using whole-cell patch-clamp techniques. The bath application of ACh induced a marked increase in the frequency of spontaneous EPSCs (sEPSCs) in Purkinje cells specifically in the vestibulo-cerebellum. This effect of ACh was mimicked by muscarine but not by nicotine. It was abolished by application of either tetrodotoxin or the antagonist of AMPA receptors, indicating that the ACh-induced enhancement of sEPSCs occurred indirectly via the activation of neurons sending glutamatergic projections to Purkinje cells. In 15% of granule cells tested in the vestibulo-cerebellum, muscarine elicited membrane depolarization accompanied by a decrease in membrane conductance and increased the neuronal excitability. The muscarine-induced depolarization of granule cells in the vestibulo-cerebellum was attributable to the inhibition of standing-outward K⁺ currents (IK_SO) most likely via the activation of muscarinic M₃ receptors. Taken together, these results indicate that ACh increases the firing frequency of granule cells by inhibiting IK_SO, which in turn increases the frequency of sEPSCs in Purkinje cells in the rat vestibulo-cerebellum.

Key words: acetylcholine; vestibulo-cerebellum; Purkinje cell; granule cell; sEPSCs; muscarinic receptor; potassium current

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Received Feb. 3, 2003; revised May. 6, 2003; accepted May. 13, 2003.

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