Chemical Senses Vol. 29 No. 8 © Oxford University Press
2004; all rights reserved
Analysis of Slow Hyperpolarizing Potentials in Frog Taste Cells Induced by Glossopharyngeal Nerve Stimulation
Division of Integrative Sensory Physiology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan
Correspondence to be sent to: Toshihide Sato, Division of Integrative Sensory Physiology, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan. e-mail: toshi{at}net.nagasaki-u.ac.jptoshi@net.nagasaki-u.ac.jp
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Abstract |
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Electrical stimulation of the frog glossopharyngeal (GP) nerve evoked slow hyperpolarizing potentials (HPs) in taste cells. This study aimed to clarify whether slow HPs were postsynaptically induced in taste cells. The slow HPs were recorded intracellularly with a microelectrode. When Ca2+ concentration in the blood plasma was decreased to
0.5 mM, the amplitude of slow HPs reduced and their
latency lengthened. When the Ca2+ concentration was increased to 20
mM, the amplitude of slow HPs increased and their latency shortened. Addition of
Cd2+ to the plasma greatly reduced the amplitude of slow HPs and
lengthened their latency. These data suggest that the slow HPs are dependent on
presynaptic activities in the GP nerve terminals in the taste disk. Of various
antagonists injected intravenously for blocking receptors of neurotransmitter biogenic
amines and peptides, only antagonists for substance P blocked the slow HPs at 2–4
mg/kg body wt. Application of substance P of 2 mg/kg to the plasma induced
hyperpolarizing responses in taste cells, whose amplitude was the same as that of the
slow HPs induced by GP nerve stimulation. Application of a nonselective cation channel
antagonist, flufenamic acid, to the plasma blocked the slow HPs. These results suggest
that the slow HPs are generated by closing the nonselective cation channels in the
postsynaptic membrane of taste cells following possible release of substance P from the
GP nerve terminals in the taste disk.
Key words: flufenamic acid, frog taste cell, gustatory efferent synapse, slow hyperpolarizing potential, substance P
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Sensory hair cells in the auditory organ (Nakajima and Wang, 1974
), the vestibular organ (Hillman, 1969) and the lateral-line organ
(Hama, 1965) are innervated by both
afferent and efferent nerve fibers. The former convey sensory information from the
sensory cells and the latter control the sensitivity of the cells (Fex, 1962;
Llinás and Precht, 1969;
Furukawa, 1981). Afferent innervation
of gustatory receptor cells has extensively been studied morphologically and
physiologically (Murray, 1973;
Lindemann, 1996). Efferent
innervation of the gustatory receptor cells has been suggested by electron-microscopical
studies (Nomura et al.,
1975;
Yoshie et al., 1996;
Reutter et al., 1997).
Electrophysiological studies have suggested that receptor potentials in the frog taste
cells are modulated by the glossopharyngeal (GP) nerve stimulation (Sato et al., 2001). Our previous study (Sato et al., 2002) showed that slow
hyperpolarizing potentials (HPs) and slow depolarizing potentials (DPs) are elicited in
frog taste cells by GP nerve stimulation. The former are evoked under normal blood
circulation, but the latter are observed only when the blood circulation is lowered.
Either slow potentials are likely to be postsynaptic responses since they are accompanied
with a change of conductances in the taste cell membrane (Sato et al., 2002). Slow types of postsynaptic
potentials have been found in many neurons of autonomic and central nervous systems
(Nicholls, 1994;
Shepherd, 1994;
Ganong, 2003). These potentials play
important roles in modulating various functions such as cardiac output, hormone release,
thirst, etc. (Pocock and Richards,
1999). The objective of this study was to clarify whether slow HPs in frog taste cells evoked by the GP nerve stimulation are postsynaptic. We examined effects of (1) Ca2+ and Cd2+ and (2) neurotransmitter antagonists and agonists on GP nerve-induced slow HPs. The results suggest that the slow HPs are postsynaptically evoked in taste cells by substance P possibly released from the GP nerve terminals in the taste disk.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Preparation
Fifty-four bullfrogs (Rana catesbeiana) of 330–720 g were used in the experiments. All the experiments were performed in accordance with the Guidelines for Animal Experimentation of Nagasaki University. The animals were deeply anaesthetized by i.p. injection of a 50% urethane solution at a dose of 2–3 g/kg body wt. The hypoglossal nerves were bilaterally cut to remove lingual muscle contractions. The tongue of the animal placed in a supine position was pulled out from the mouth and pinned on a silicone rubber plate. Blood supply to the tongue through the lingual arteries and veins was carefully maintained. The whole GP nerves on both sides were separated out from connective tissues, cut centrally and immersed into mineral oil. All experiments were carried out at room temperature of 23–27°C.
Electrical recordings and stimulations
Intracellular recordings were made from taste cells in the taste disk of the fungiform
papillae with a 3 M KCl-filled microelectrode (35–75 M
). An indifferent
electrode of chlorided silver wire was inserted into the forelimb muscles. The criteria
for identifying successful intracellular recordings were the same as described previously
(Sato et al., 2002).
The membrane potentials of the taste cells were amplified with a microelectrode
amplifier (MEZ-8101; Nihon Kohden, Tokyo, Japan) and recorded on a pen recorder. The
input resistance of single taste cells was always measured with a bridge circuit housed
in the amplifier. When a slow HP was generated by GP nerve stimulation, the input
resistance of an impaled taste cell increased (Sato et al., 2002). When the input resistance did
not increase, the cell was regarded as of no innervation with the GP nerve fibers. The
distal side of the GP nerve transected was electrically stimulated with repetitive pulses
of 30 Hz for 5–10 s, which produced the maximal amplitude of summated slow
potentials in the taste cells (Sato et
al., 2002). The electrical pulses were 0.1 ms in duration and
15–30 V in strength for stimulating C-fibers.
Solutions and drugs
The tongue surface was adapted to a frog Ringer solution, which consisted of (mM) 115
NaCl, 2.5 KCl, 1.8 CaCl2 and 5 HEPES (pH 7.2). The synaptic region of taste
cells in the taste disks was perfused via capillary vessels by intravenously injecting a
Ringer solution containing pharmacological drugs to modulate synaptic transmission.
Capillary vessels were abundant underneath the taste disks of the fungiform papillae
(Jaeger and Hillman, 1976). Amount of
injected Ringer solution was 2 ml/kg body wt. Applied agents were EGTA, CaCl2
and CdCl2. Ca2+ concentration in the blood plasma was
decreased by injecting EGTA at a dose of 23.9 mg/kg and increased by injecting
CaCl2 at a dose of 116 mg/kg. Estimated low and high Ca2+
concentrations in the plasma were 0.5 and 20 mM, respectively, which were
calculated from an even distribution of injected EGTA and CaCl2 in the frog
plasma volume (4% of the body wt;
Thorson, 1964). Normal
Ca2+ concentration in the frog plasma is 2 mM (Wilson, 1979). CdCl2 was intravenously injected
at doses of 0.001–1 mg/kg. Estimated Cd2+ concentrations in the
plasma were in the range of 6 x 10–8– 6
x 10–5 M.
To search for neurotransmitters which are released from the axon terminals in the taste disks, 10 receptor antagonists were used: DL-propranolol hydrochloride, prazosin hydrocloride, metergoline, tropine 3,5-dichlorobenzoate, spiperone, (±)-SKF-83566 hydrochloride, calcitonin gene-related peptide (CGRP) fragment 8–37, vasoactive intestinal peptide (VIP) fragment 6–28, [D-Arg1, D-Trp7,9,Leu11] substance P acetate salt and oxalate salt. Substance P acetate salt was used as an agonist (NK1 agonist). All drugs were purchased from Sigma-Aldrich Co. (St Louis, MO). Stock solutions from prazosin hydrochloride, metergoline, spiperone, SKF-83566 hydrochloride and oxalate salt were prepared with ethanol. Stock solutions from tropine 3,5-dichlorobenzoate and CGRP fragment 8–37 were prepared with DMSO and 0.1% acetic acid, respectively. These solutions were kept at –20°C. Aliquots of stock solutions were added into the frog Ringer solution to obtain desired final concentrations when used for experiments. VIP fragment 6–28, [D-Arg1, D-Trp7,9, Leu11] substance P acetate salt, substance P acetate salt and propranolol hydrochloride were directly dissolved in the Ringer solution. To remove the junction potential generated between the fluid secreted from lingual salivary glands following GP nerve stimulation and the lingual surface fluid, atropine sulfate (Sigma-Aldrich) dissolved in the Ringer solution was applied i.v. To block nonselective cation channels in taste cell membranes, flufenamic acid (Sigma-Aldrich) stocked in ethanol was injected i.v. after diluting with the Ringer solution. Ringer solutions containing Cd2+, EGTA and excess Ca2+ were intravenously injected at a slow rate of 0.1 ml/min so as not to perturb the heart rate, but Ringer solutions containing the other drugs were injected at a rate of 0.1 ml/s.
Experimental procedure
Strong repetitive electrical stimulations of GP nerve produce a large slow potential
on the lingual surface and in taste cells, which is derived from the physicochemical
junction potential between a secreted saliva and a lingual surface solution (Sato et al., 2000). This junction
potential disturbs an analysis of slow HP responses elicited in taste cells. Therefore,
before the start of intracellular recordings from taste cells, atropine sulfate was
injected intravenously at a dose of 1 mg/kg to completely block the slow physicochemical
junction potential. The effect of this injection lasted for >7 h.
The electrical activities of frog taste disks show a variation from individual to individual and from season to season. Comparison between control and test responses was performed using the slow HPs obtained from the same individual. Control response data were collected from 10–30 taste cells for 90 min before a drug injection and test response data were collected from 10–30 taste cells for 90 min after a 30 min circulation of an injected drug.
Statistics
All data were expressed as means ± SEMs. The level of significance was set at P < 0.05 with a Student’s t-test.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Effect of Ca2+ concentration on slow HPs
Release of neurotransmitters from the presynaptic axon terminal is triggerd by
Ca2+ influx at the terminal and modulated by changing
Ca2+ concentrations at the terminal (Katz and Miledi, 1967). If slow HPs are postsynaptically
evoked in taste cells by GP nerve stimulation, they may be modulated by changing
Ca2+ concentration in presynaptic axon terminals of taste disks. To test
this, Ca2+ concentration in the taste disks was altered by changing the
amount of Ca2+ in the blood plasma. The slow HPs in taste cells induced
by GP nerve stimulation at 30 Hz were significantly lower in amplitude and longer in
latency at a low Ca2+ concentration (0.5 mM) than at the control
(2 mM) (P < 0.05, n = 12–20; Figure
1A, Ba, Ca). On the other hand, the
slow HPs were higher in amplitude and shorter in latency at a high Ca2+
concentration (20 mM) than at the control (P < 0.05, n =
15–20; Figure
1A, Bb, Cb).
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The amplitude and latency of postsynaptic potentials fluctuate during repetitive synaptic transmission (Katz and Miledi, 1965
). To observe such a phenomenon, slow HPs in single taste cells were
induced by stimulating GP nerve with train pulses (30 Hz for 5 s) at every minute for
7–16 min. Figure
2 shows fluctuation of amplitudes (A
and B) and latencies (A and C) of the slow HPs when Ca2+ concentrations
in the plasma were kept at the control and the low level. Either the amplitude or the
latency distributed broadly at the low Ca2+ concentration (data at the
high Ca2+ concentration not shown). To statistically compare the
distribution of amplitudes and latencies of the slow HPs obtained under the low (0.5
mM), the control (2 mM) and the high (20 mM Ca2+ concentrations
in the plasma, the mean amplitude and mean latency of the slow HPs in each taste cell
were respectively normalized as 100. Resultantly, means and SEMs of standard deviations
in amplitude of the slow HPs were 46 ± 3 (n = 8) in the low , 21
± 1 (n = 6) in the control and 10 ± 1
(n = 8) in the high Ca2+ concentration. On the
other hand, means and SEMs of standard deviations in latency of the slow HPs were 49
± 2 (n = 7) in the low, 18 ± 1 (n = 6) in
the control and 11 ± 1 (n = 9) in the high Ca2+
concentration There were significant differences between any pairs of the three standard
deviations in either amplitude or latency of the slow HPs (P < 0.05,
n = 6–9). Both the amplitude and the latency of the slow HPs in
taste cells more fluctuated as Ca2+ concentration decreased in GP nerve
terminals of the taste disk.
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Effect of Cd2+ on slow HPs
Cd2+ is a nonselective voltage-gated Ca2+ channel
blocker (Randall, 1998). We tested
effect of intravenously injected Cd2+ on the slow HPs in taste cells. The
amplitude of slow HPs was dose-dependently decreased by Cd2+ (Figure
3). When CdCl2 was injected
at a dose of 1 mg/kg, the amplitude became 18% of that without
Cd2+ (P < 0.01, n = 18–21). At a dose
of 1 mg/kg, the concentration of Cd2+ in the plasma was estimated to be
60 µM. The IC50 of CdCl2 for the slow HPs was at
0.013 mg/kg (0.8 µM Cd2+). The latency of slow HPs
significantly increased from 5.0 ± 1.2 s (n = 15) in the controls
to 10.8 ± 1.2 s (P < 0.05, n = 18 ) when
CdCl2 was injected at 1 mg/kg.
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Effect of neurotransmitter receptor antagonists on slow HPs
First, effects of receptor antagonists for biogenic amines on the slow HPs were
tested. Prazosin (a noradrenaline 
1 blocker), propranolol (a
noradrenaline ß blocker), metergoline (a blocker of serotonin 5HT1 and
5HT2 receptors), tropine 3,5-dichlorobenzoate (a selective blocker of
serotonin 5HT3 receptor), SKF-83566 (a selective blocker of dopamine
D1 receptor) and spiperone (a selective blocker of dopamine D2
receptor) were injected intravenously at 1 mg/kg body wt with no effects on the amplitude
of slow HPs (P > 0.1, n = 19–23; Figure
4A).
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Kuramoto (1988
) and
Kusakabe et al. (1996) found
nerve fibers containing VIP, CGRP and substance P in the frog taste disks. Therefore, we
tested receptor antagonists for these peptides. Injected drugs were VIP fragment
6–28 (a potent VIP receptor blocker), CGRP fragment 8–37 (a selective CGRP
receptor blocker), [D-Arg1, D-Trp7,9,
Leu11] substance P acetate salt (a substance P receptor NK1
blocker) and oxalate salt (a substance P receptor NK1 blocker). Both VIP and
CGRP receptor antagonists did not affect the slow HPs (P > 0.1, n
= 16–20). Two types of substance P receptor antagonist reduced the slow HPs
(Figure
4B). When oxalate salt was injected at
doses of 0.2–4 mg/kg, the drug dose-dependently reduced the slow HPs. Oxalate salt
of 4 mg/kg reduced the slow HPs by 99 ± 1% (P < 0.01,
n = 17–21) and [D-Arg1,
D-Trp7,9, Leu11] substance P acetate salt of 2
mg/kg reduced the slow HPs by 98 ± 2% (P < 0.01, n
= 18–22). Therefore, it is suggested that a neurotransmitter candidate in
generating the slow HPs in taste cells is substance P. Hyperpolarizing responses induced by substance P
Whether substance P elicits the slow HPs in taste cells was examined by i.v. injection at a dose of 2 mg/kg. Membrane potentials were recorded from many taste cells of a tongue before and after injection of substance P. A summary of recordings is illustrated in Figure 5. The resting membrane potential of taste cells was –32 ± 2 mV (n = 14) before the drug injection, but the membrane potential was increased to –43 ± 4 mV (n = 6) 30 min after the drug injection. The increased membrane potential, which was maintained for 25 min, resumed the resting membrane potential of –33 ± 2 mV (n = 10) 20 min after a substance P antagonist, oxalate salt, was injected at a dose of 2 mg/kg. The amplitude of hyperpolarizing responses in taste cells evoked by substance P of 2 mg/kg was –11 ± 1 mV (n = 31).
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On the other hand, the amplitude of slow HPs evoked by electrical stimulation of GP nerve was –12 ± 3 mV (n = 8) when the resting potential was in a range from –28 to –36 mV (–32 ± 2 mV, n = 8). There was no difference in amplitude between substance P-induced hyperpolarization and GP nerve-induced slow HPs (P > 0.1, n = 8–31). The hyperpolarizing responses induced during application of substance P at 2 mg/kg were observed in 50 of 64 taste cells (78%) tested. The slow HPs induced by GP nerve stimulation were observed in 452 of 525 taste cells (86%).
Effect of flufenamic acid on slow HPs
Our previous study (Sato et al.,
2002) showed that the reversal potential for slow HPs in taste cells evoked
by GP nerve stimulation is –13 mV and that the mechanism generating the slow HPs is
an inactivation of nonselective cation channels which are most permeable to
K+ and Na+. Flufenamic acid is a potent antagonist for
the nonselective cation channels (Hescheler and
Schultz, 1993). The slow HPs in taste cells were dose-dependently reduced by
flufenamic acid (Figure
6). Flufenamic acid of 5 mg/kg
completely inhibited the slow HPs (P < 0.01, n =
25–26), indicating that they are generated by flufenamic-acid-sensitive
nonselective cation channels at the taste cell membrane.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Sequential events of chemical synaptic transmission are as follows: (i) activation of voltage-gated Ca2+ channels at presynaptic axon terminal by a depolarization; (ii) release of a neurotransmitter from the presynaptic terminal; (iii) binding of the neurotransmitter to receptors at postsynaptic cell; and (iv) generation of a postsynaptic potential at the postsynaptic cell by direct or indirect opening or closing of ion channels (Shepherd, 1994
).
The present study suggested that the amplitude and latency of the slow HPs in frog
taste cells induced by the GP nerve stimulation were modulated by Ca2+
and Cd2+ in the nerve terminals of taste disk (Figures
1 and
3) and that the fluctuations of the
amplitudes and latencies of the slow HPs in taste cells were dependent on
Ca2+ concentration in the nerve terminals of taste disk (Figure
2). Proton-gated nonselective cation
channels of the apical receptive membrane in frog taste cells cause acid responses
(Miyamoto et al., 1988;
Okada et al., 1994;
Sato et al., 1995).
Sensitivity of these nonselective cation channels to Cd2+ is low and the
IC50 of Cd2+ for the acid responses in frog taste
cells is estimated to be 0.5 mM (Miyamoto
et al., 1988). On the other hand, the IC50 of
Cd2+ for the slow HPs in frog taste cells was as low as 0.8 µM.
Cd2+ is a potent blocker of voltage-gated Ca2+ channels
in various tissues and the IC50 for these channels is 1
µM (Randall, 1998), which is
almost the same as the IC50 for the slow HPs in frog taste cells.
In general, sensitivity to Cd2+ is much lower in nonselective cation
channels than in voltage-gated Ca2+ channels (Wallnöfer et al., 1989).
Therefore, Cd2+-dependent inhibition of slow HPs in taste cells may be
due to an inactivation of voltage-gated Ca2+ channels at presynaptic axon
terminals. Also, Ca2+-dependence of the amplitude and latency of slow HPs
may be due to a modulation of Ca2+ influxes through voltage-gated
Ca2+ channels at the presynaptic axon terminals.
Of antagonists tested for receptors of biogenic amines and peptides only antagonists
for substance P receptor completely blocked slow HPs in taste cells induced by GP nerve
stimulation (Figure
4). The presence of substance P has
been shown immunohistochemically at the nerve terminals of frog taste disk (Kuramoto, 1988;
Kusakabe et al., 1996).
Intravenous application of substance P at 2 mg/kg, whose concentration in the plasma is
estimated to be 28 µM, produced hyperpolarizing responses in taste cells. These
results suggest that a candidate of neurotransmitter released from the presynaptic axon
terminals in frog taste disk is substance P.
Our previous study (Sato et al.,
2002) indicated that GP nerve-induced slow HPs may be due to an inactivation
of nonselective cation channels permeable to K+ and Na+
in the frog taste cells. Nonselective cation channels of 30 pS permeable to
K+ and Na+ have been found in the basolateral membranes
of frog taste cells (Fujiyama et al.,
1993). The present work showed that flufenamic acid as a potent blocker of
the nonselective cation channel in the postsynaptic membrane of the taste cell suppressed
the generation of slow HPs in taste cells (Figure
6). Since flufenamic acid is
relatively insensitive to voltage-gated Ca2+ channels present in the
presynaptic axon terminals (Hescheler and Schultz,
1993), the slow HPs is thought to be suppressed by binding of flufenamic acid
to the nonselective cation channels in the taste cell membrane.
Substance P receptor, NK1, is coupled to G-protein, and the second
messengers of the intracellular transduction pathways following binding of substance P to
NK1 are IP3 and DAG (Otsuka
and Yoshioka, 1993;
Bloom, 1996;
Ganong, 2003). Since the membrane
conductance decreases while slow HPs are generated in frog taste cells by GP nerve
stimulation (Sato et al.,
2002), the slow HPs are probably generated by closing the
nonselective cation channels through an intracellular transduction cascade after
substance P binds to NH1 in the postsynaptic membrane of the taste cells.
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Accepted July 16, 2004
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T. Sato, Y. Okada, T. Miyazaki, Y. Kato, and K. Toda Taste Cell Responses in the Frog Are Modulated by Parasympathetic Efferent Nerve Fibers Chem Senses, November 1, 2005; 30(9): 761 - 769. [Abstract] [Full Text] [PDF]
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