Elsevier

Neuroscience

Volume 165, Issue 4, 17 February 2010, Pages 1476-1489
Neuroscience

Sensory System
Research Paper
The role of transient receptor potential vanilloid-1 on neural responses to acids by the chorda tympani, glossopharyngeal and superior laryngeal nerves in mice

https://doi.org/10.1016/j.neuroscience.2009.11.051Get rights and content

Abstract

The transient receptor potential vanilloid-1 (TRPV1) receptor acts as a polymodal nociceptor activated by capsaicin, heat, and acid. TRPV1, which is expressed in sensory neurons innervating the oral cavity, is associated with an oral burning sensation in response to spicy food containing capsaicin. However, little is known about the involvement of TRPV1 in responses to acid stimuli in either the gustatory system or the general somatosensory innervation of the oropharynx. To test this possibility, we recorded electrophysiological responses to several acids (acetic acid, citric acid and HCl) and other taste stimuli from the mouse chorda tympani, glossopharyngeal and superior laryngeal nerves, and compared potential effects of iodo-resiniferatoxin (I-RTX), a potent TRPV1 antagonist, on chemical responses of the three nerves. The results indicated that in the chorda tympani nerve, I-RTX (1–100 nM) did not affect responses to acids, sucrose and quinine HCl, but reduced responses to NaCl (I-RTX at concentrations of 10 and 100 nM) and KCl and NH4Cl (100 nM). In contrast, in the glossopharyngeal nerve, I-RTX significantly suppressed responses to all acids and salts, but not to sucrose and quinine HCl. Responses to acetic acid were suppressed by I-RTX even at 0.1 nM concentration. The superior laryngeal nerve responded in a concentration-dependent manner to acetic acid, citric acid, HCl, KCl, NH4Cl and monosodium l-glutamate. The responses to acetic acid, but not to the other stimuli, were significantly inhibited by I-RTX. These results suggested that TRPV1 may be involved in the mechanism for responses to acids presented to the posterior oral cavity and larynx. This high degree of responsiveness to acetic acid may account for the oral burning sensation, known as a flavor characteristic of vinegar.

Section snippets

Experimental animals

All experimental procedures were performed in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and approved by the committee for Laboratory Animal Care and Use at Kyushu University (Fukuoka, Japan). Subjects were adult male and female C57BL/6NCrj mice (Charles River Japan, Tokyo, Japan), 8–20 weeks of age, ranging in weight from 20 to 32 g. Two or three mice were housed together in plastic cages and received ad libitum food pellets (MF; Oriental

Results

We first examined if RTX, a TRPV1 agonist, would be an effective stimulant for the CT, GL and SL nerves. As shown in Fig. 1, RTX, applied to the oral cavity and larynx elicited responses of the CT, GL and SL nerves in a concentration-dependent manner. The magnitude of relative responses to RTX was much smaller in the CT than in the GL and SL nerves. The RTX responses in all the three nerves were largely reduced by 1 nM I-RTX, an antagonist for TRPV1 (two-way repeated ANOVA P<0.01 for CT, P

Discussion

The present study demonstrated that responses of the GL and SL nerves to acids were clearly inhibited by low concentrations of I-RTX, a potent TRPV1 antagonist, whereas no such inhibition was evident in the CT nerve (Fig. 2, Fig. 3, Fig. 4). The data obtained from the CT nerve is consistent with previous studies showing no change in acid responses in the fungiform taste bud cells or in the CT nerve following treatment with agonists and antagonists for TRPV1 (Liu and Simon, 2001, Lyall et al.,

Conclusion

In summary, the present study examined whether or not TRPV1 would be involved in responses to acid stimuli, we recorded electrophysiological responses to several acids (acetic acid, citric acid and HCl) and other taste stimuli from the CT, GL and SL nerves in mice, and compared potential effects of I-RTX, a potent TRPV1 antagonist, on responses of the three nerves. We found that acid and salt responses were suppressed by I-RTX differentially between the three nerves. The results suggest the

Acknowledgments

We thank Dr. Thomas E. Finger for valuable suggestions on the manuscript. This research was supported in part by Grant-in-Aids 18077004 (Y.N.), 18109013 (Y.N.) for Scientific Research from Japan Society of Promotion of Science.

References (65)

  • I. Matsumoto et al.

    A comparative study of three cranial sensory ganglia projecting into the oral cavity: in situ hybridization analyses of neurotrophin receptors and thermosensitive cation channels

    Brain Res Mol Brain Res

    (2001)
  • Y. Ninomiya et al.

    Amiloride inhibition of responses of rat single chorda tympani fibers to chemical and electrical tongue stimulations

    Brain Res

    (1988)
  • Y. Ninomiya et al.

    Gustatory neural responses in preweanling mice

    Physiol Behav

    (1991)
  • Y. Ninomiya et al.

    Responses to umami substances in taste bud cells innervated by the chorda tympani and glossopharyngeal nerves

    J Nutr

    (2000)
  • M. Ohmoto et al.

    Genetic tracing of the gustatory and trigeminal neural pathways originating from T1R3-expressing taste receptor cells and solitary chemoreceptor cells

    Mol Cell Neurosci

    (2008)
  • T. Shingai et al.

    Response characteristics of three taste nerves in mice

    Brain Res

    (1985)
  • A. Szallasi et al.

    Resiniferatoxin, a phorbol-related diterpene, acts as an ultrapotent analog of capsaicin, the irritant constituent in red pepper

    Neuroscience

    (1989)
  • M. Tominaga et al.

    The cloned capsaicin receptor integrates multiple pain-producing stimuli

    Neuron

    (1998)
  • A. Varga et al.

    Effects of the novel TRPV1 receptor antagonist SB366791 in vitro and in vivo in the rat

    Neurosci Lett

    (2005)
  • Y. Zhang et al.

    Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways

    Cell

    (2003)
  • J.C. Boudreau et al.

    Single unit recordings from the geniculate ganglion of the facial nerve of the cat

    Exp Brain Res

    (1971)
  • J.C. Boudreau et al.

    Single unit recordings from the petrosal ganglion of the rat glossopharyngeal nerve

    Chem Sens Abstr

    (1985)
  • M.J. Caterina et al.

    The capsaicin receptor: a heat-activated ion channel in the pain pathway

    Nature

    (1997)
  • M.J. Caterina et al.

    Impaired nociception and pain sensation in mice lacking the capsaicin receptor

    Science

    (2000)
  • S. Damak et al.

    Detection of sweet and umami taste in the absence of taste receptor T1r3

    Science

    (2003)
  • J.A. DeSimone et al.

    Taste receptors in the gastrointestinal tract IIISalty and sour taste: sensing of sodium and protons by the tongue

    Am J Physiol Gastrointest Liver Physiol

    (2006)
  • J.D. Dickman et al.

    Response properties of fibers in the hamster superior laryngeal nerve

    Brain Res

    (1988)
  • T.E. Finger et al.

    ATP signaling is crucial for communication from taste buds to gustatory nerves

    Science

    (2005)
  • N.R. Gavva et al.

    AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties

    J Pharmacol Exp Ther

    (2005)
  • P. Hartwig et al.

    Flavor characteristics of lactic, malic, citric, and acetic acids at various pH levels

    J Food Sci

    (1995)
  • W. He et al.

    Umami taste responses are mediated by alpha-transducin and alpha-gustducin

    J Neurosci

    (2004)
  • G.L. Heck et al.

    Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway

    Science

    (1984)
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