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¹ Department of Physiology, Faculty of Medicine, Kagoshima University, Kagoshima 890-8520, Japan
² Laboratoire de Neurobiologie Cellulaire et Moleculaire, CNRS, 91198 Grif-sur-Yvette, Cedex, France
³ Laboratory of Physiology, Senshu University, Kawasaki 214-8580, Japan

Address correspondence to T. Gotow, Department of Physiology, Faculty of Medicine, Kagoshima University, 8-35-1 Sakuragaoka, Kagoshima 890-8520, Japan. Fax: 81-99-275-5470; E-mail: tsukasa{at}m.kufm.kagoshima-u.ac.jp

Light-dependent K⁺ channels underlying a hyperpolarizing response of one extraocular (simple) photoreceptor, Ip-2 cell, in the marine mollusc Onchidium ganglion were examined using cell-attached and inside-out patch-clamp techniques. A previous report (Gotow, T., T. Nishi, and H. Kijima. 1994. Brain Res. 662:268–272) showed that a depolarizing response of the other simple photoreceptor, A-P-1 cell, results from closing of the light-dependent K⁺ channels that are activated by cGMP. In the cell-attached patch recordings of Ip-2 cells, external artificial seawater (ASW) was replaced with a modified ASW containing 150 mM K⁺ and 200 mM Mg²⁺ to suppress any synaptic input and to maintain the membrane potential constant. When Ip-2 cells were equilibrated with this modified ASW, the internal K⁺ concentration was estimated to be 260 mM. Light-dependent single-channels in the cell-attached patch on these cells were opened by light but scarcely by voltage. After confirming the light-dependent channel activity in the cell-attached patches, an application of cGMP to the excised inside-out patches newly activated a channel that disappeared on removal of cGMP. Open and closed time distributions of this cGMP-activated channel could be described by the sum of two exponents with time constants _o1, _o2 and _c1, _c2, respectively, similar to those of the light-dependent channel. In both the channels, _o1 and _o2 in ms ranges were similar to each other, although _c2 over tens of millisecond ranges was different. _o1, _o2, and the mean open time _o were both independent of light intensity, cGMP concentration, and voltage. In both channels, the open probability increased as the membrane was depolarized, without changing any of _o2 or _o. In both, the reversal potentials using 200- and 450-mM K⁺-filled pipettes were close to the K⁺ equilibrium potentials, suggesting that both the channels are primarily K⁺ selective. Both the mean values of the channel conductance were estimated to be the same at 62 and 91 pS in 200- and 450-mM K⁺ pipettes at nearly 0 mV, respectively. Combining these findings with those in the above former report, it is concluded that cGMP is a second messenger which opens the light-dependent K⁺ channel of Ip-2 to cause hyperpolarization, and that the channel is the same as that of A-P-1 closed by light.

Key Words: primitive vision • cGMP-gated K⁺ channels • phototransduction in vertebrates and invertebrates • guanylate cyclase activated by light

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