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The Journal of Neuroscience, August 15, 2001, 21(16):5962-5972

Contribution of the Na-K-Cl Cotransporter on GABA_A Receptor-Mediated Presynaptic Depolarization in Excitatory Nerve Terminals

Il-Sung Jang, Hyo-Jin Jeong, and Norio Akaike

Cellular and System Physiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan

GABA_A receptor-mediated responses manifest as either hyperpolarization or depolarization according to the intracellular Cl concentration ([Cl]_i). Here, we report a novel functional interaction between the Na-K-Cl cotransporter (NKCC) and GABA_A receptor actions on glutamatergic presynaptic nerve terminals projecting to ventromedial hypothalamic (VMH) neurons. The activation of presynaptic GABA_A receptors depolarizes the presynaptic nerve terminals and facilitates spontaneous glutamate release by activating TTX-sensitive Na⁺ channels and high-threshold Ca²⁺ channels. This depolarizing action of GABA was caused by an outwardly directed Cl driving force for GABA_A receptors; that is, the [Cl]_i of glutamatergic nerve terminals was higher than that predicted for a passive distribution. The higher [Cl]_i was generated by bumetanide-sensitive NKCCs and was responsible for the GABA-induced presynaptic depolarization. Thus, GABA_A receptor-mediated modulation of spontaneous glutamatergic transmission may contribute to the development and regulation of VMH function as well as to the excitability of VMH neurons themselves.

Key words: sEPSCs; presynaptic GABA_A receptors; intraterminal Cl concentration; NKCC; mechanical dissociation; VMH; GABA-induced depolarization

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21165962-11$05.00/0

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