Intercellular signaling in Necturus taste buds: chemical excitation of receptor cells elicits responses in basal cells.

Abstract

1. Taste cells in intact taste buds in slices of Necturus lingual epithelium were impaled with microelectrodes for intracellular recording. Two types of cells were investigated: taste receptor cells and basal cells. 2. Impaling cells in the apical end of taste buds resulted in intracellular records from taste receptor cells. Applying short pulses (100- to 200-ms duration) of 140 mM KCl solution to the apical pore elicited receptor potentials in the taste receptor cells. 3. Impaling cells in the base of the taste bud resulted in intracellular records from taste receptor cells and basal cells. KCl applied to the taste pore elicited responses in the basal region that varied greatly in both magnitude and time of onset. The latency of these responses (time of onset compared with the onset of the receptor potential) ranged from 0 to hundreds of milliseconds. 4. Impaled cells were identified by injecting Lucifer yellow after recording KCl responses for 21 cells. KCl responses recorded from identified basal cells all had latencies of greater than 75 ms. KCl responses from identified receptor cells all had latencies of less than 75 ms. 5. One explanation for the long latency of KCl responses recorded in basal cells is that the responses represent postsynaptic potentials. In agreement with this interpretation, long-latency responses, but not short-latency responses, were reversibly reduced by the Ca antagonist Cd (1 mM, 10- to 20-min bath exposure). 6. Long-latency responses also differed from short-latency responses in their voltage dependence. Short-latency responses had the same voltage dependence as apically recorded receptor potentials, increasing with hyperpolarization from resting potential with an extrapolated reversal potential near 0 mV. Long-latency responses were much less dependent on voltage in this range. 7. We measured the spread of exogenously applied KCl with potassium-sensitive electrodes. Long-latency responses were not generated by diffusion of applied KCl to the basal region of the taste bud. A small transient increase in extracellular potassium occurred at the base of the taste bud after chemostimulation at the apical pore. This increase was due to depolarization-evoked release of potassium from taste cells and did not cause the long-latency responses in basal cells. 8. We conclude that short-latency (less than 75 ms) responses recorded from cells situated in the bases of taste buds are electrotonically conducted receptor potentials generated at the apical region. Long-latency (greater than 75 ms) responses are consistent with recording postsynaptic responses in basal cells.