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Analysis of whole-cell currents by patch clamp of guinea-pig myenteric neurones in intact ganglia

François Rugiero, Maurice Gola, Wolf A. A. Kunze *, Jean-Claude Reynaud, John B. Furness * and Nadine Clerc

Whole-cell patch-clamp recordings taken from guinea-pig duodenal myenteric neurones within intact ganglia were used to determine the properties of S and AH neurones. Major currents that determine the states of AH neurones were identified and quantified. S neurones had resting potentials of -47 ± 6 mV and input resistances (R_in) of 713 ± 49 M at voltages ranging from -90 to -40 mV. At more negative levels, activation of a time-independent, caesium-sensitive, inward-rectifier current (I_Kir) decreased R_in to 103 ± 10 M. AH neurones had resting potentials of -57 ± 4 mV and R_in was 502 ± 27 M. R_in fell to 194 ± 16 M upon hyperpolarization. This decrease was attributable mainly to the activation of a cationic h current, I_h, and to I_Kir. Resting potential and R_in exhibited a low sensitivity to changes in [K⁺]_o in both AH and S neurones. This indicates that both cells have a low background K⁺ permeability. The cationic current, I_h, contributed about 20 % to the resting conductance of AH neurones. It had a half-activation voltage of -72 ± 2 mV, and a voltage sensitivity of 8.2 ± 0.7 mV per e-fold change. I_h has relatively fast, voltage-dependent kinetics, with on and off time constants in the range of 50-350 ms. AH neurones had a previously undescribed, low threshold, slowly inactivating, sodium-dependent current that was poorly sensitive to TTX. In AH neurones, the post-action-potential slow hyperpolarizing current, I_AHP, displayed large variation from cell to cell. I_AHP appeared to be highly Ca²⁺ sensitive, since its activation with either membrane depolarization or caffeine (1 mM) was not prevented by perfusing the cell with 10 mM BAPTA. We determined the identity of the Ca²⁺ channels linked to I_AHP. Action potentials of AH neurones that were elongated by TEA (10 mM) were similarly shortened and I_AHP was suppressed with each of the three -conotoxins GVIA, MVIIA and MVIIC (0.3-0.5 µM), but not with -agatoxin IVA (0.2 µM). There was no additivity between the effects of the three conotoxins, which indicates the presence of N- but not of P/Q-type Ca²⁺ channels. A residual Ca²⁺ current, resistant to all toxins, but blocked by 0.5 mM Cd²⁺, could not generate I_AHP. This patch-clamp study, performed on intact ganglia, demonstrates that the AH neurones of the guinea-pig duodenum are under the control of four major currents, I_AHP, I_h, an N-type Ca²⁺ current and a slowly inactivating Na⁺ current.

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