Depression of Gustatory Receptor Potential in Frog Taste Cell by Parasympathetic Nerve-Induced Slow Hyperpolarizing Potential

Abstract

Parasympathetic nerve (PSN) innervates taste cells of the frog taste disk, and electrical stimulation of PSN elicited a slow hyperpolarizing potential (HP) in taste cells. Here we report that gustatory receptor potentials in frog taste cells are depressed by PSN-induced slow HPs. When PSN was stimulated at 30 Hz during generation of taste cell responses, the large amplitude of depolarizing receptor potential for 1 M NaCl and 1 mM acetic acid was depressed by approximately 40% by slow HPs, but the small amplitude of the depolarizing receptor potential for 10 mM quinine-HCl (Q-HCl) and 1 M sucrose was completely depressed by slow HPs and furthermore changed to the hyperpolarizing direction. The duration of the depolarizing receptor potentials depressed by slow HPs prolonged with increasing period of PSN stimulation. As tastant-induced depolarizing receptor potentials were increased, the amplitude of PSN-induced slow HPs inhibiting the receptor potentials gradually decreased. The mean reversal potentials of the slow HPs were approximately -1 mV under NaCl and acetic acid stimulations, but approximately -14 mV under Q-HCl and sucrose stimulations. This implies that when a slow HP was evoked on the same amplitude of depolarizing receptor potentials, the depression of the NaCl and acetic acid responses in taste cells was larger than that of Q-HCl and sucrose responses. It is concluded that slow HP-induced depression of gustatory depolarizing receptor potentials derives from the interaction between gustatory receptor current and slow hyperpolarizing current in frog taste cells and that the interaction is stronger for NaCl and acetic acid stimulations than for Q-HCl and sucrose stimulations.

Effect of Gap Junction Blocker β-Glycyrrhetinic Acid on Taste Disk Cells in Frog

“…As revealed in the previous investigation (Sato et al 2007), the vertical penetration of a microelectrode across the taste disk induced three step-potential changes (arrows in Fig. 1).…”

“…The cell bodies of taste disk cells in the central area of the disk are arranged at three layers: Ia cell bodies at the superficial layer, Ib cell bodies at the upper part of intermediate layer and cell bodies of Ic/II/III cells at the lower part of intermediate layer (Richiter et al 1988;Witt 1993;Osculati and Sbarbati 1995). The criteria for identification of Ia cell, Ib cell and II/III cell in intracellular recordings from taste disks were the same as described previously (Sato et al 2007). In brief, the cell types were identified by three significantly different resting membrane potentials.…”

Interaction Between Gustatory Depolarizing Receptor Potential and Efferent-Induced Slow Depolarizing Synaptic Potential in Frog Taste Cell

“…All experiments were carried out in accordance with the Guidance of Animal Experimentation in Nagasaki University. The methods of making preparation, electrical recording from taste cells, electrical stimulation of GPN and chemical stimulation of taste cells were the same as previously mentioned (Sato et al 2002(Sato et al , 2004(Sato et al , 2005(Sato et al , 2007a. In brief, intracellular recordings from taste cells in the taste disks of fungiform papillae were made with a 3 M KCl filled-microelectrode.…”

“…The fungiform papillae used were located at the apical and middle portions of the tongue. The microelectrode was put at the surface of the central area of taste disk and advanced into the lower portion of intermediate layer (Osculati and Sbarbati 1995) by monitoring appearance of three step-potential changes of the membrane potentials in taste disk cells (Sato et al 2007a). Both GPNs were separated free from the connective tissues, cut centrally and immersed into mineral oil.…”

“…Under normal blood circulation in the tongue, all gustatory depolarizing receptor potentials (GDRPs) in frog taste cells evoked by four basic taste stimuli are depressed by adding PSN-induced slow HSPs (Sato et al 2007a). Thus suppression is due to an inhibition of depolarizing receptor currents across the apical receptive membrane by slow hyperpolarizing synaptic currents across the proximal subsynaptic membrane of taste cells.…”