Voltage dependence of the rat chorda tympani response to Na+ salts: implications for the functional organization of taste receptor cells

Abstract

1. Voltage-clamp and current-clamp data were obtained from a circumscribed region of the anterior rat lingual epithelium while simultaneously monitoring the afferent, stimulus-evoked, neural response from the same receptive field. 2. Chorda tympani (CT) responses at constant Na(+)-salt concentration were enhanced by submucosa negative voltage clamp and suppressed by positive voltage clamp. The complete CT response profile, including the time course of adaptation, was not uniquely determined by NaCl concentration alone. The response could be reproduced at different NaCl concentrations by applying a compensating voltage. 3. The form of the concentration and voltage dependence of the CT response indicates that the complete stimulus energy is the Na+ electrochemical potential difference across receptor cell apical membranes, and not Na+ concentration alone. This is the underlying principal behind the equivalence of chemical and electric taste for Na+ salts. 4. CT responses to sodium gluconate (25 and 200 mM) and 25 mM NaCl produced amiloride-insensitive components (AIC) of low magnitude. NaCl at 200 mM produced a significantly larger AIC. The AIC was voltage-clamp independent. The relative magnitude of the AIC was positively correlated with the transepithelial conductance of each salt. This suggests that the large AIC for 200 mM NaCl results from its relatively high permeability through the paracellular pathway. 5. Analysis of the CT response under voltage clamp revealed two anion effects on Na(+)-salt taste, both of which act through the paracellular shunt. 1) Anions modify the transepithelial potential (TP) across tight junctions and thereby modulate the cell receptor potential. This anion effect can be eliminated by voltage clamping the TP. 2) Sufficiently mobile anions facilitate electroneutral diffusion of Na+ salts through tight junctions. This effect is observed especially when Cl- is the anion and when the stimulus concentration favors NaCl influx, allowing Na+ to stimulate receptor cells from the submucosal side. Because the submucosal intercellular spaces are nearly isopotential regions, this effect is insensitive to voltage clamp of the TP. The large AIC associated with this anion effect is due to the low permeability of amiloride.

Anion Size Does Not Compromise Sodium Recognition by Rats After Acute Sodium Depletion.

“…Together, these results suggest that rather than responding to sodium activation of the AS transduction pathway, the behavioral detectability of high NaGlu concentrations derives from some cue related to the gluconate anion or perhaps activation of the AI pathway due to leakage of sodium through tight junctions, or AI apical channels, as a result of the high Na ϩ concentration gradient. In summary, these data support Bernstein & Hennessy's (1987) conclusion that the AS sodium transduction pathway is necessary for sodium recognition in the rat, and furthermore strongly suggest that this pathway is also sufficient (see Elliot & Simon, 1990;Formaker & Hill, 1988;Ye et al, 1993). We have also extended previous studies of the effects of amiloride on salt appetite to show that the sodium specificity of the appetite is completely abolished when the AS pathway is blocked, coupled with a modest increase in appetitive behavior.…”

Signal transduction and information processing in mammalian taste buds

“…NaCl evokes a stronger saltiness than Na sulphate, for example. One explanation for this involves the ability of Na + to permeate deep into the taste bud by penetrating through the tight junction spaces at the apical tips of cells [48]. The apical tips of taste bud cells, as in all epithelial boundaries, are sealed by a junctional complex including the zonula occudens.…”

Taste discrimination between NaCl and KCl is disrupted by amiloride in inbred mice with amiloride-insensitive chorda tympani nerves

“…Thus, in contrast to the predictions based on CT recordings, discrimination in all four strains appeared to depend on the amiloride-sensitive transduction pathway, which, in the case of BALB/cByJ, 129P3/J, and DBA/2J (and perhaps C57BL/6 as well), may exist in taste buds innervated by nerves other than the CT. animal psychophysics; taste transduction; taste coding; C57BL/6; BALB/c; 129P3/J; DBA/2 THE TASTE OF SODIUM CHLORIDE appears to be transduced via at least two mechanisms, one which is selective for Na ϩ (and Li ϩ ) and is disrupted by the lingual application of the epithelial Na ϩ channel-blocker amiloride (e.g., Refs. 1,3,5,8,12,16,27, 39), and the other(s) which is amiloride-insensitive and cation nonselective (e.g., 12,17,20,22,30,[35][36][37]. In rats, electrophysiological recordings from the chorda tympani (CT) nerve have demonstrated that, when amiloride is applied to the lingual epithelium, the responsiveness of this nerve to sodium salts, but not to nonsodium salts, is markedly suppressed (e.g., Refs.…”