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Electrotonic Coupling in the Anterior Pituitary of a Teleost Fish

Department of Animal Sciences (B.L.-S., C.L.B.) and Koret School of Veterinary Medicine, (C.L.B., M.J.G., I.A.F.) Faculty of Agricultural, Food, and Environmental Quality Sciences, The Hebrew University, Rehovot 76100, Israel

Address all correspondence and requests for reprints to: Dr. Berta Levavi-Sivan, Department of Animal Sciences, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University, P.O. Box 12, Rehovot 76100, Israel. E-mail: sivan{at}agri.huji.ac.il.

The anterior pituitary of teleost fish contains a variety of endocrine cells, which, under control from the hypothalamus, release trophic hormones and thereby play a major role in reproduction, social behavior, and growth. In fish, hypothalamic fibers directly innervate the pituitary. The hypothalamic hormones released from these fibers bind to membrane receptors on pituitary cells, triggering action potentials, a rise in cytosolic calcium, and exocytosis. It is unclear whether these activities are confined to the stimulated cell or propagate to adjacent cells. We addressed this issue using whole cell and perforated patch-clamp techniques in a novel, hypothalamo-pituitary slice preparation from the tilapia fish (Oreochromis niloticus). Pituitary cells at rest generated occasional spontaneous spikes and sharp depolarizations of lower amplitude. The latter probably represented spikes in neighboring, electrotonically coupled cells. The presence of electrotonic communication, probably mediated by gap junctions, was also supported by the finding that Lucifer Yellow diffuses between cells. To quantify this connectivity, we performed simultaneous recording from pairs of adjacent cells. Thirty-three percent of the cells exhibited strong reciprocal coupling. Coupling coefficients ranged between 0.18 and 0.31, and coupling resistances ranged between 16 and 39 GOhm. The electrical junctions were effective low pass filters, attenuating action potentials much more than low frequency waveforms. We conclude that electrical activities of anterior pituitary cells in teleost fish are synchronized by coupling through gap junctions. Regulation of this coupling may play a critical role in determining complex patterns of pituitary hormone secretion.