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Journal of Experimental Biology 157,101-122 (1991)
Published by Company of Biologists 1991

Initiation and Modulation Of Action Potentials in Salivary Gland Cells of Haementer1A Ghilianii by Putative Transmitters and Cyclic Nucleotides

WERNER A. WUTTKE ¹ and MICHAEL S. BERRY ¹

¹ Biomedical and Physiological Research Group, School of Biological Sciences, University College of Swansea Singleton Park, Swansea SA2 8PP, Wales, UK

1. The giant salivary cells of Haementeria ghilianii are known to produce Ca²⁺-dependent action potentials and to release their secretory products in response to stimulation of the stomatogastric nerve. In this study, the electrophysiological effects of some putative transmitters were examined by perfusion of the gland and two promising candidates were selected for detailed analysis.

2. Acetylcholine (ACh) was the only substance tested which excited the gland cells. It produced a large, Na⁺-dependent depolarization that elicited 1–3 action potentials and desensitized to about 24% of its maximal value within 2 min.

3. Carbachol, tetramethylammonium and nicotine elicited similar responses to ACh, whereas choline and pilocarpine had negligible effects.

4. The ACh response was completely blocked by d-tubocurarine and strychnine, and was reduced by tetraethylammonium, hexamethonium and atropine. The receptors, therefore, cannot be clearly distinguished as nicotinic or muscarinic.

5. ACh did not elicit secretion, but this does not necessarily preclude it from acting as a neuroglandular transmitter.

6. 5-Hydroxytryptamine (5-HT) was the only transmitter candidate that elicited secretion, though it did not excite the gland cells.

7. 5-HT produced a subthreshold depolarization and an increase in input resistance. Action potentials, elicited by depolarizing pulses, were increased in amplitude and duration, and showed greatly reduced adaptation.

8. 5-HT potentiated the net inward current, evoked by subthreshold depolarizing pulses, by reducing outward K⁺ current. The inward current, carried by Ca²⁺, was not directly affected. In addition, 5-HT increased an inwardly rectifying current, carried by Na⁺ and K⁺. All the effects of 5-HT tended to increase cell excitability.

9. Salivary cell responses to 5-HT were reversibly antagonised by methysergide.

10. Responses to ACh or 5-HT were not mimicked by 3', 5'-cyclic guanosine monophosphate, which greatly reduced spike amplitude and excitability. The effects were specific to the 3', 5' form; 2', 3'-cyclic GMP had no effect. Cyclic GMP dramatically reduced the duration of action potentials that had been artificially prolonged by TEA⁺ or removal of external Ca2⁺.

11. Cyclic 3', 5'-adenosine monophosphate and its dibutyryl derivative had little effect on membrane properties. 8-Bromo-cyclic AMP, however, mimicked all the effects of 5-HT. It is thought that 5-HT may exert its actions via cyclic AMP.

12. The possible role of 5-HT in salivary secretion is discussed.

Key words: salivary gland, leech, Haementeria ghilianii, 5-hydroxytryptamine, acetylcholine, cyclic nucleotides, action potential

Accepted on January 3, 1991