Anions modulate cation-induced responses of single units of the frog glossopharyngeal nerve

Fibers of the frog glossopharyngeal nerve that are sensitive to water stimulation also respond to Ca, Mg and Na salts. During stimulation with a salt, the cation and the anion are applied together and the anion could influence the response to the cation. We examined this interaction using single unit recordings at the level of fungiform papilla. Nerve impulses of large amplitude were recorded in response to the stimulation of adjacent papillae with increasing concentrations of various Ca, Mg and Na salts. For a given cation, the elicited spike frequency depended on the anion. For example, the responses of single fibers to Ca2+ concentrations above 0.1 mM were maximal with CaSO4 and minimal with Ca(SCN)2. The rank order of efficiency was CaSO4 > CaCl2 = CaBr2 = Ca(NO3)2 > Ca(SCN)2 for Ca2+ ions at 5 mM. The effects of these anions were reversed for Mg and Na salts, the rank orders being Mg(SCN)2 > Mg(NO3)2 > MgBr2 = MgCl2 > MgSO4, for Mg2+ ions at 200 mM, and NaSCN > NaI > NaNO3 > NaBr > NaCl >> NaF = Na2SO4, for Na+ ions at 500 mM. All these sequences correspond to the lyotropic rank order of the anions. In stimulation by a mixture of Ca and Na salts, which have different rank orders with respect to anions, either the response to Ca2+ ions or the response to Na+ ions could be eliminated as a result of mutual antagonism between Ca2+ and Na+ ions. In this case, the rank order of anions was dependent only on the cation that was able to exert a stimulatory effect in the mixture. Threshold concentrations for Ca, Mg and Na salts are influenced by cationic properties, but not by anionic properties. We hypothesize that anions can modulate the efficacy of cation transduction by binding to a membrane element that interacts with each of the three distinct receptors for Ca2+, Mg2+ and Na+ ions without altering the affinities of these receptors for the respective cations. The present results cannot be interpreted in terms of permeability of the apical membrane to anions and changes in surface potential on the apical membrane. The possibility is discussed that an anion-selective paracellular pathway between taste cells is responsible for the effect of anions on the cation-induced response.