Chem. Senses 26: 1203-1210,
2001
© Oxford University Press 2001
Effects of Amiloride on Gustatory Neural Responses to Salts in the Frog
Department of Oral Physiology, School of Dentistry, Iwate Medical University, Iwate 020-8505, Japan 1 Department of Oral Physiology, Okayama University Dental School, Okayama 700-8525, Japan
Correspondence to be sent to: Yasuyuki Kitada, Department of Oral Physiology, School of Dentistry, Iwate Medical University, Iwate 020-8505, Japan. e-mail: ykita{at}iwate-med.ac.jp
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Abstract |
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In frogs, the glossopharyngeal nerve (GL) innervates taste receptors on almost the entire tongue. The mandibular branch (MBF) and palatine branch (PN) of the facial nerve innervate taste receptors on a very small area at the base of the tongue and on the palate, respectively. In the present study, effects of amiloride, an epithelial sodium channel blocker, on the tonic responses of the GL, MBF and PN in frogs to NaCl, LiCl, KCl and CaCl2 were investigated. In three nerves, amiloride at 0.5 mM, a relatively high concentration, did not affect the responses to 0.15 (concentration just above threshold)-0.5 M NaCl, 0.5 M LiCl and 0.3 M KCl, whereas it almost completely inhibited the response to 1.0 mM CaCl2. Amiloride may exert an inhibitory action on the response to CaCl2 by a competitive antagonism between Ca2+ and a monovalent cation of amiloride, because the response to Ca2+ is competitively inhibited by other cations such as Na+ and Mg2+. The lack of inhibitory effect of amiloride on the responses in the GL, MBF and PN to NaCl suggests that amiloride-sensitive sodium channels in the apical membrane of taste receptor cells are not involved in sodium taste transduction in frogs.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In mammals, taste receptors on the anterior two-thirds and the posterior one-third of the tongue are innervated by the chorda tympani nerve (CT) and the glossopharyngeal nerve (GL), respectively. Taste receptors on the soft palate and in the naso-incisor ducts are innervated by the greater superficial petrosal nerve (GSP). The CT and the GSP are branches of the facial nerve. It has been demonstrated that amiloride, an epithelial sodium channel blocker, partially reduces the neural responses of the rat CT (Lindemann, 1996
;
Stewart et al., 1997)
and GSP (Harada et al.,
1997; Sollars and Hill,
1998) to NaCl, but it does not affect the NaCl response of the GL
in rats (Formaker and Hill,
1991; Kitada et al.,
1998) and mice (Ninomiya
et al., 1991). These findings suggest that sodium taste
processing involves both amiloride-sensitive and amiloride-insensitive
transduction pathways. In frogs, unlike mammals, taste receptors on almost the
entire tongue are innervated by the GL. When compared with those in the
mammalian gustatory nerves, studies of amiloride-sensitive and
amiloride-insensitive transduction pathways in the frog gustatory nerves are
relatively few. Some investigators have reported that amiloride partially
inhibited the responses of the frog GL to salts
(Yoshii et al., 1986;
Herness, 1987). However, in
their studies a single concentration (0.1 mM) of amiloride was tested, but the
affinity of amiloride for inhibition was not quantitatively studied. Other
investigators have reported opposing results—that amiloride had no
effect on the response to NaCl (Okada
et al., 1991). In their experiments only a single
concentration was chosen for stimulation. No systematic studies have been done
so far. Therefore, the effect of amiloride on neural responses of the frog to
salts remains unclear.
In the present study, we investigated the effects of amiloride on the
responses of the frog GL to a variety of salts (NaCl, LiCl, KCl and
CaCl2). In frogs, the mandibular branch of the facial nerve (MBF)
innervates taste receptors on a very small area at the base of the tongue
(Gaupp, 1899;
Nomura and Suzuki, 1989) and
the palatine nerve (PN), a branch of the facial nerve, innervates taste
receptors on the palate (Gaupp,
1899; Pumphrey,
1935). Since in the rodent facial nerve NaCl responses are
inhibited by amiloride (Lindemann,
1996; Stewart et al.,
1997), we also investigated the effects of amiloride on the
responses of the MBF and of the PN to NaCl, LiCl, KCl and CaCl2 in
frogs.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Neurophysiological recording
Bullfrogs (Rana catesbeiana), weighing 200-400 g, were anesthetized with urethane (3 g/kg body wt). Each animal was put in the supine position and the tongue was pulled out from the mouth and fixed on the plate of an experimental chamber with pins. The hypoglossal nerve was transected bilaterally to prevent tongue movements. The GL or the MBF on one side was dissected free from the surrounding connective tissues and cut centrally. For recording the neural activities of the PN, the mandibles were removed from animals and the PN on one side was exposed from the ventral side by slitting the mucous membrane of the palate. The PN was cut near its entrance to the skull.
The nerve was placed on a silver recording electrode. Multifiber neural activity was differentially recorded in reference to a stainless-steel needle electrode placed in nearby tissue. The activities were displayed on an oscilloscope and passed through an integrator with a time constant of 0.5 s. The integrated neural activity was then displayed on a rectilinear pen recorder for analyses of response magnitudes.
Stimulation
The experiments were performed at 20-25°C. Since the frog GL response
is sensitive to water and the water response is inhibited by low
concentrations of NaCl (Zotterman,
1949), 0.05 M NaCl solution was used as an adapting solution.
Taste receptors on the tongue were adapted with 0.05 M NaCl for at least 5 min
before each stimulation. Stimulating solutions of 0.1-0.5 M NaCl, 0.1-0.5 M
LiCl, 0.1-0.3 M KCl and 0.1-1.0 mM CaCl2 were prepared with
distilled water. Stimulating solutions were applied to the surface of the
tongue at a flow rate of 20 ml/min for 30 s. To study the effect of amiloride,
the adapting solution (0.05 M NaCl) containing 0.05-0.5 mM amiloride
hydrochloride (Sigma) was flowed over the tongue for 1 min prior to each test
and then the stimulating solution containing 0.05-0.5 mM amiloride was applied
to the tongue. Stimulation of the palate was similar to that of the
tongue.
Data analysis
The height of the pen recorder deflection at 25 s after stimulus
application was used as the measure of response. In frogs, the phasic portion
of the response is variable and depends on the adapting condition of taste
receptors on the tongue as well as on concentration of salt stimuli, while the
tonic response is practically independent of the adapting condition
(Kashiwagura et al.,
1976). The response magnitudes were normalized relative to the
magnitude of the response to 0.5 M NaCl, 0.5 M LiCl, 0.3 M KCl and 1.0 mM
CaCl2 for NaCl, LiCl, KCl and CaCl2 stimulations,
respectively.
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Results |
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The GL responses
One GL innervates taste receptors on most of the tongue of the ipsilateral side (Figure 1A). The concentration of NaCl at threshold was 0.1-0.15 M when taste receptors on the tongue were adapted to 0.05 M NaCl. Amiloride at 0.1 mM did not affect the response of the GL to 0.15-0.5 M NaCl (data not shown). Thus, 0.5 mM, a relatively high concentration, of amiloride was used in the following experiments for NaCl stimulations. Figure 1B shows the integrated responses of the GL to NaCl stimulation with and without 0.5 mM amiloride. The adapting solution containing 0.5 mM amiloride elicited a phasic response, indicating that amiloride itself is stimulatory in the GL responses. The responses to NaCl over the concentration range 0.15-0.5 M were unaffected by 0.5 mM amiloride. Figure 1C shows concentration—response curves for NaCl with and without 0.5 mM amiloride. Amiloride at 0.5 mM had no effect on the responses to NaCl stimulations at all concentrations tested.
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The effects of amiloride on the responses of the GL to LiCl, KCl and
CaCl2 were examined. The concentration of LiCl or KCl at threshold
was 
0.1 M. CaCl2 is a very effective stimulus for eliciting
impulses from the frog GL (Zotterman,
1949; Kusano and Sato,
1957; Nomura and Sakada,
1965; Kitada,
1978; Kitada and Shimada,
1980). The concentration of CaCl2 at threshold was
reported to be <0.01 mM and the maximum response was obtained at 1 mM
CaCl2 (Kitada,
1978). In the present study, 0.5 M LiCl, 0.3 M KCl and 1 mM
CaCl2 were employed as stimulating solutions. The reasons for
choosing these concentrations are that the stable responses to the salts were
obtained in these concentrations. Figure
2A shows the integrated responses to three salts. The responses to
0.5 M LiCl and 0.3 M KCl were not affected by the presence of 0.5 mM
amiloride, but the response to 1.0 mM CaCl2 was almost completely
inhibited by 0.5 mM amiloride. Effects of amiloride on salt responses are
summarized in 4-6 preparations (Figure
2B). No reduction in magnitudes of responses to 0.5 M LiCl and 0.3
M KCl was seen with 0.5 mM amiloride, whereas amiloride at 0.5 mM strongly
inhibited the response to 1.0 mM CaCl2.
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Figure 3 shows the amiloride inhibition curves of CaCl2 responses at two concentrations. Reducing the concentration of CaCl2 from 1.0 to 0.1 mM shifted the curve to a low concentration range of amiloride, suggesting that the amiloride inhibition is due to competitive antagonism between Ca2+ ions and amiloride.
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The MBF and PN responses
Figure 4A illustrates the small innervation area of the frog MBF. Application of 0.5 M NaCl solution to the innervation area of the tongue elicited impulses from the MBF. The concentration of NaCl at threshold was 0.1-0.15 M. Figure 4B,C shows integrated responses to NaCl and the concentration—response curves for NaCl with and without 0.5 mM amiloride, respectively. It is evident that amiloride did not affect the responses to NaCl stimulation. Effects of 0.5 mM amiloride on the responses to 0.5 M LiCl, 0.3 M KCl and 1.0 mM CaCl2 in the MBF were similar to those in the GL (Figure 5). Amiloride at 0.5 mM did not affect the responses to 0.5 M LiCl and 0.3 M KCl, but it eliminated the responses to 1.0 mM CaCl2 (Figure 5).
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The frog PNs are responsive to salts
(Pumphrey, 1935). As shown in
Figure 6A, one PN innervates
the taste receptors on the palate of the ipsilateral side. The concentration
of NaCl at threshold was 0.1-0.15 M. Integrated responses of the PN to NaCl at
0.15, 0.2, 0.3 and 0.5 M are shown in
Figure 6B. Effects of amiloride
on the responses to NaCl in the PN were similar to those in the GL and MBF. As
shown in Figure 6B,C, amiloride
at 0.5 mM did not affect the responses to NaCl stimulations at all
concentrations tested. Effects of 0.5 mM amiloride on the responses to 0.5 M
LiCl and 0.3 M KCl were also examined. No reduction in the responses to 0.5 M
LiCl and 0.3 M KCl were seen with 0.5 mM amiloride
(Figure 7). The responses to
1.0 mM CaCl2 were eliminated by 0.5 mM amiloride
(Figure 7).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In frogs, amiloride-sensitive sodium channels (ASSCs) were found in isolated taste cells by patch clamp recording (Avenet and Lindemann, 1988
).
The presence of ASSCs in taste cells suggests that the influx of
Na+ ions through ASSCs directly depolarizes the taste cells,
eventually leading to the release of neurotransmitters onto taste afferent
nerve terminals. Therefore, the frog GL response has been thought to be
sensitive to amiloride. In the present study, we used 0.5 mM amiloride that is
sufficient to block the influx of Na+ ions through ASSCs
(Lindemann, 1996;
Miyamoto et al.,
2000). We investigated the effects of amiloride on the responses
to NaCl not only in the frog GL, but also in the MBF and PN (branches of the
facial nerve). Our results show that amiloride does not affect the responses
to NaCl in these nerves. The findings suggest that ASSCs in apical membrane of
taste cells are not involved in salt taste transduction in frogs and that an
amiloride-insensitive sodium pathway is the main contributor to salt taste
transduction.
The distribution of ASSCs in taste buds isolated from the oral cavity has
been investigated in rats (Doolin and
Gilbertson, 1996; Gilbertson
and Fontenot, 1998), hamsters
(Gilbertson and Fontenot, 1998)
and mice (Miyamoto et al.,
1999) by patch clamp recording. In rats, ASCCs were found in
roughly two-thirds of fungiform taste receptor cells, in one-third of foliate
taste receptor cells and in one-third of palate taste receptor cells
(Doolin and Gilbertson, 1996;
Gilbertson and Fontenot, 1998).
Fungiform and palate taste receptor cells and a part of foliate taste receptor
cells are innervated by the facial nerve. On the other hand, no ASSCs were
found in the circumvallate taste receptor cells which are innervated by the GL
(Doolin and Gilbertson, 1996).
The pattern of the distribution of ASSCs in the oral cavity of rats suggests
that the occurrence of ASSCs in the rat taste cells is linked with innervation
by the facial nerve. In contrast, in frog taste cells ASSCs seem not to be
linked with innervation by the facial nerve. That is, ASSCs were found in
>50% of taste cells innervated by the GL
(Avenet and Lindemann, 1988).
Interestingly, in hamsters ASSCs were found in 68.4% of circumvallate taste
receptor cells (Gilbertson and Fontenot,
1998). Hence, the distribution of ASSCs may not simply be linked
with innervation by branches of the facial nerve.
For the amiloride-insensitive sodium pathway, Ye et al.
(Ye et al., 1993)
proposed a model in which a flow of Na+ ions through tight
junctions between taste cells stimulates the submucosal membrane of taste
cells. The present results showed that the frog GL lacks amiloride
sensitivity. Miyamoto et al.
(Miyamoto et al.,
1989) reported that amiloride had no effect on the receptor
potentials of taste cells induced by lingual application of NaCl solution in
intracellular recordings in anesthetized frogs, suggesting that ASSCs are not
present in the apical membrane of frog taste cells, but leaving a possibility
that ASSCs exist in the vasolateral membrane of the cells. If this is the
case, paracellular transport of Na+ ions through tight junctions
may contribute to sodium taste transduction in frogs. However, a large
molecule of amiloride impermeable to the tight junctions cannot block the
inflow of sodium ions through the submucosal ASSCs in taste cells. Therefore,
this transduction pathway in the frog taste cells is amiloride-insensitive.
There may be another amiloride-insensitive pathway. That is, Doolin and
Gilbertson (Doolin and Gilbertson,
1996) reported that Na+ influx independent of ASSCs is
important for apical and/or basolateral routes of Na+ entry into
taste cells of the rat circumvallate taste buds. Thus, we cannot rule out the
possibility that amiloride-insensitive Na+ currents in frog taste
cells are responsible for the amiloride-insensitive component of neural
responses to NaCl.
In the rat CT, responses to LiCl are partially inhibited by amiloride, as
well as responses to NaCl (Brand et
al., 1985). Although responses of the rat CT to KCl are not
affected by amiloride (Brand et
al., 1985), ASSCs in frog taste cells are somewhat permeable
to K+ ions (Avenet and
Lindemann, 1988). Therefore, it is important to examine effects of
the responses to LiCl and KCl in the frog GL, MBF and PN. Our results showed
that amiloride does not affect the responses of the three gustatory nerves to
LiCl and KCl. The results suggest that ASSCs in the apical membrane of taste
cells are not responsible for the responses to LiCl and KCl in the frog
gustatory nerves.
Among the salts tested to date, Ca salts act as the most effective stimulus
in the frog GL response (Zotterman,
1949; Kusano and Sato,
1957; Nomura and Sakada,
1965; Kitada,
1978). In the present study, amiloride at 0.5 mM almost completely
inhibited the response to 1.0 mM CaCl2. It has been reported that
amiloride blocks the low threshold (T) Ca2+ channel in mouse
neuroblastoma and chick dorsal root ganglion neurons
(Tang et al., 1988).
However, the effect of amiloride on the response to 1.0 mM CaCl2 in
the frog gustatory nerve requires much higher concentrations (amiloride
concentration of half-maximal inhibition 
0.2 mM) than the blockade of the
low threshold Ca2+ channel (amiloride concentration of half-maximal
inhibition = 0.032 mM) (Tang et
al., 1988). There is no evidence for the presence of
Ca2+ channel in frog taste cells so far
(Avenet and Lindemann, 1987;
Miyamoto et al.,
1991). It appears that the Ca2+ channel, as with that
found in mouse neuroblastoma and chick dorsal root ganglion neurons, is not
responsible for the response of the frog gustatory nerve to
CaCl2.
Kitada (Kitada, 1984,
1986) has found that low
concentrations of pronase E inhibit the response to CaCl2, but do
not inhibit the response to NaCl and suggests that the calcium-receptor sites
responsible for the response to Ca2+ may be a protein that is
distinct from the sodium-receptor sites responsible for the response to
Na+. Kitada (Kitada,
1978) found that all cations tested (Na+,
K+, NH4+, choline+,
Mg2+, Ni2+, Co2+, Mn2+,
La3+) inhibited the response to CaCl2. The inhibition of
the response to Ca2+ by other cations is due to competition between
Ca2+ and other cations for the same calcium-receptor sites
(Kitada and Shimada, 1980).
Therefore, the affinity of calcium-receptor sites for cations is not
chemically specific, but charge-specific. Amiloride exists primarily as a
monovalent cation with a positive charge in solution
(Benos, 1982). Since the
semilogarithmic concentration—inhibition curve of amiloride was shifted
to the left as CaCl2 was decreased
(Figure 3), it is probable that
amiloride inhibited the response to CaCl2 in a competitive manner.
Relatively high concentrations of amiloride (>0.1 mM) were required to
inhibit the response to 1.0 mM CaCl2
(Figure 3). It appears that
amiloride does not act as a pharmacological agent, but simply acts as a
cation. Complete inhibition of the response to CaCl2 by amiloride
suggests that calcium-receptor sites responsible for the response to
CaCl2 may reside in the apical membrane of frog taste cells.
In the mudpuppy, it has been reported that amiloride failed to inhibit the
responses to NaCl in the GL (McPheeters
and Roper, 1985). Since the present results showed that the
responses of the frog gustatory nerves (GL, MBF and PN) to NaCl were not
affected by amiloride, it is likely that ASSCs in the apical membrane are not
associated with salt taste transduction in amphibians. Since the responses to
NaCl in the mammalian facial nerve are sensitive to amiloride, the salt taste
transduction mechanism in the frog facial nerve is different from that in the
mammalian facial nerve.
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Acknowledgments |
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This work was supported by grants-in-aid for High Performance Biomedical Materials Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan.
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Accepted August 17, 2001
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