Characteristics of Biphasic Slow Depolarizing and Slow Hyperpolarizing Potential in Frog Taste Cell Induced by Parasympathetic Efferent Stimulation

Abstract

When the velocity of capillary blood flow in the frog tongue declined to an intermediate range of 0.2-0.7 mm/s, the glossopharyngeal nerve stimulation induced a biphasic slow depolarizing and slow hyperpolarizing potential (HP) in taste cells. The objective of this work was to examine the generative mechanisms of the biphasic slow potentials. The biphasic slow response was always preceded by a slow depolarizing potential (DP) component and followed by a slow HP component. Intravenous injection of tubocurarine completely blocked the biphasic slow responses, suggesting that both components of the biphasic slow potentials are evoked by the parasympathetic nerve (PSN) fibers. Membrane conductance of taste cells increased during slow DPs and decreased during slow HPs. The reversal potential of either component of a biphasic slow response was the almost same value of -12 mV. An antagonist, L-703,606, for neurotransmitter substance P neurokinin(1) receptor completely blocked both components of the biphasic slow responses. An antagonist, flufenamic acid, for nonselective cation channels on the taste cell membrane completely blocked the biphasic slow responses. These results suggest that PSN-induced biphasic slow responses are postsynaptically elicited in taste cells by releasing substance P at the PSN axon terminals. It is concluded that the slow DP component may be generated by opening one type of nonselective cation channel on taste cells and that the slow HP component may be generated by closing the other type of nonselective cation channel. We discussed that a second messenger inositol 1,4,5-trisphosphate might be related to a slow DP component and another second messenger diacylglycerol might be related to a slow HP component.

Efferent Fibers Innervate Gustatory and Mechanosensitive Afferent Fibers in Frog Fungiform Papillae

“…The time course (45 s) of slow external synaptic potentials recorded from whole afferent fiber terminals in a fungiform papilla using a suction electrode is similar to that of slow depolarizing synaptic potentials in frog taste cells elicited by stimulation of parasympathetic efferent fibers in blood circulation-declined frog (Sato et al 2007a(Sato et al , 2007b. Probably, similar intracellular Ca 2+ -activated nonselective cation channels might be involved in generation of slow negative synaptic potential in afferent endings of the papillae.…”

“…The possibility that frog taste cells are innervated by efferent fibers was clarified in 2002 by recording slow postsynaptic potentials from taste cells (Sato et al 2002). When lingual circulation is normal, only slow hyperpolarizing postsynaptic potential regarded as slow IPSP is recorded by parasympathetic efferent stimulation at 30 Hz (Sato et al 2005(Sato et al , 2007b. Synaptic substance released from the terminals of parasympathetic efferent fibers is supposed to be substance P because slow hyperpolarizing postsynaptic potentials are blocked by L-703,606 (Sato et al 2004).…”

“…Before start of experiments atropine (a blocker of muscarinic acetylcholine [Ach] receptor) was intravenously injected at 1 mg/kg to completely block the large physicochemical junction potential generated between secreted saliva and lingual fluid when the GPN was strongly stimulated (Sato et al 2000). All experiments were carried out during normal blood circulation for 4 h of the tongue (Sato et al 2002(Sato et al , 2007b. The room temperature of laboratory was kept at 22-25 °C.…”

“…All the drugs were purchased from Sigma-Aldrich Co.. Stock solutions of tubocurarine and flufenamic acid were prepared with ethanol. Stock solution of L-703,606 oxalate was prepared with methanol (Sato et al 2004(Sato et al , 2005(Sato et al , 2007a(Sato et al , 2007b. These stock solutions were dissolved in Frog Ringer solution to make dilute drug solutions.…”

“…The receptor potentials in frog taste cells induced by gustatory stimuli are inhibited or enhanced by efferent stimulation (Sato et al 2005, Sato, Nishishita, Mineda, et al 2007. Slow depolarizing postsynaptic potentials are elicited in frog taste cells when lingual blood circulation declines (Sato et al 2007a(Sato et al , 2007b.…”