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Changes of the biophysical properties of voltage-gated Na+ currents during maturation of the sodium-taste cells in rat fungiform papillae

Taste cells are a heterogeneous population of sensory receptors that undergoes a continuous turnover. Different chemo-sensitive cell lines rely on action potentials to release the neurotransmitter onto nerve endings. The electrical excitability is due to the presence of a tetrodotoxin-sensitive, voltage-gated sodium current (INa) similar to that found in neurons. Since the biophysical properties of INa change during neuronal development, we wondered whether the same also occurred in taste cells. Here, we used the patch-clamp recording technique to study INa in sodium sensing cells of rat fungiform papillae. We identified these cells by exploiting the known blocking effect of amiloride on ENaC, the sodium (salt) receptor. Then, based on the amplitude of INa and a morphological analysis, we subdivided sodium cells into two broad developmental groups, namely immature and mature cells. We found that: the voltage dependence of activation and inactivation changed in the transition from immature to mature state (depolarizing shift); the membrane capacitance significantly decreased in mature cells, enhancing the density of INa; a persistent sodium current, absent in immature cells, appeared in mature cells. mRNA expression analysis of the α-subunits of voltage-gated sodium channels in fungiform taste buds supported the electrophysiological data. As a whole, our findings provide evidence for a noticeable change in membrane excitability during development, which is consistent with the key role played by electrical signaling in the release of neurotransmitter by mature sodium cells. Key Points Summary Taste cells are sensory receptors that undergo continuous turnover while they detect food chemicals and communicate with afferent nerve fibers. The voltage-gated sodium current (INa) is a key ion current for generating action potentials in fully differentiated and chemo-sensitive taste cells, which use electrical signaling to release neurotransmitters. Here we report that in rat taste cells involved in salt detection, the properties of INa, such as voltage dependence of activation and inactivation, undergo significant changes during the transition from immature to mature state. Our results help understand how taste cells gain electrical excitability during turnover, a property critical to operate as chemical detectors that relay sensory information to nerve fibers.