Development of rat chorda tympani sodium responses:: Evidence for age-dependent changes in global amiloride-sensitive Na+ channel kinetics

In rat, chorda tympani nerve taste responses to Na+ salts increase between roughly 10 and 45 days of age to reach stable, mature magnitudes. Previous evidence from in vitro preparations and from taste nerve responses using Na+ channel blockers suggests that the physiological basis for this developmental increase in gustatory Na+ sensitivity is the progressive addition of functional, Na+ transduction elements (i.e., amiloride-sensitive Na+ channels) to the apical membranes of fungiform papilla taste receptor cells. To avoid potential confounding effects of pharmacological interventions and to permit quantification of aggregate Na+ channel behavior using a kinetic model, we obtained chorda tympani nerve responses to NaCl and sodium gluconate (NaGlu) during receptive field voltage clamp in rats aged from 12-14 to 60 days and older (60+ days). Significant, age-dependent increases in chorda tympani responses to these stimuli occurred as expected. Importantly, apical Na+ channel density, estimated from an apical Na+ channel kinetic model, increased monotonically with age. The maximum rate of Na+ response increase occurred between postnatal days 12-14 and 29-31. In addition, estimated Na+ channel affinity increased between 12-14 and 19-23 days of age, i.e., on a time course distinct from that of the maximum rate of Na+ response increase. Finally, estimates of the fraction of clamp voltage dropped across taste receptor apical membranes decreased between 19-23 and 29-31 days of age for NaCl but remained stable for NaGlu. The stimulus dependence of this change is consistent with a developmental increase in taste bud tight junctional Cl- ion permeability that lags behind the developmental increase in apical Na+ channel density. A significant, indirect anion influence on apical Na+ channel properties was present at all ages tested. This influence was evident in the higher apparent apical Na+ channel affinities obtained for NaCl relative to NaGlu. This stimulus-dependent modulation of apical Na+ channel apparent affinity relies on differences in the transepithelial potentials between NaCl and NaGlu. These originate from differences in paracellular anion permeability but act also on the driving force for Na+ through apical Na+ channels. Detection of such an influence on taste depends fundamentally on the preservation of taste bud polarity and on a direct measure of sensory function, such as the response of primary afferents.