Taste-mixture suppression: functional dissection of cellular and paracellular origins.

Abstract

1. Chorda tympani (CT) nerve responses were recorded during simultaneous current and voltage clamping of the lingual receptive-field epithelium to examine the role of field potential in taste mixture suppression between sodium gluconate (NaG) and potassium gluconate (KG). 2. Under zero current-clamp conditions, CT responses to 100 mM NaG were suppressed by 63% when presented in mixture with 250 mM KG. At this concentration, KG alone elicited no measurable neural activity, but produced a large submucosal-positive field potential. 3. When CT responses to 100 mM NaG were obtained with voltage clamp at the zero-current clamp field potential of the NaG/KG mixture, they were suppressed by only 30% relative to NaG responses under zero-current clamp. Similarly, CT responses to the mixture of NaG and KG measured while voltage was clamped at the field potential of NaG alone were slightly elevated, but not to the magnitude of zero-current clamp responses to NaG. Therefore field potential-mediated suppression of CT responses to NaG accounts for only a part of the total mixture suppression between NaG and KG. 4. Analysis of the voltage dependence of CT responses to NaG indicated that the moderate field potential increase (8.9 mV) caused by the presence of KG in the mixture equates to a 43% increase in the apparent Km for NaG, from 110 to 157 mM. Use of this effective Km obviated the effect of field potential on CT responses to the NaG/KG mixture and permitted kinetic analysis of K+ blockade of Na+ responses. These analyses suggested that K ions block Na+ movement through apical Na+ channels in a voltage-independent manner with an apparent Ko of 405 mM. Importantly, direct inhibition of Na+ transduction by K+ can account for the part of mixture suppression not mediated by field potential. 5. These experiments reveal that mixture suppression between NaG and KG is derived from two distinct sources. Field potential, triggered largely by the limited mobility of both K+ and Na+ through taste bud tight junctions, globally modulates Na+ transduction. In addition, at the level of the apical Na+ channel, K ions directly block movement of depolarizing Na+ across taste receptor apical membranes.