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 developme ntal increase in gustatory Na+ sensitivity is the progressive addition of f unctional, Na+ transduction elements (i.e., amiloride-sensitive Na+ channel s) to the apical membranes of fungiform papilla taste receptor cells. To av oid potential confounding effects of pharmacological interventions and to p ermit quantification of aggregate Na+ channel behavior using a kinetic mode l, 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 t ympani responses to these stimuli occurred as expected. Importantly, apical Na+ channel density, estimated from an apical Na+ channel kinetic model, i ncreased 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 increas e. Finally, estimates of the fraction of clamp voltage dropped across taste receptor apical membranes decreased between 19-23 and 29-31 days of age fo r NaCl but remained stable for NaGlu. The stimulus dependence of this chang e 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 evid ent 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 an ion permeability but act also on the driving force for Na+ through apical N a+ channels. Detection of such an influence on taste depends fundamentally on the preservation of taste bud polarity and on a direct measure of sensor y function, such as the response of primary afferents.