Cellular and Molecular Neurobiology

, Volume 38, Issue 4, pp 883–890 | Cite as

Enhancement of Gustatory Neural Responses by Parasympathetic Nerve in the Frog

  • Toshihide Sato
  • Yukio Okada
Original Research


The autonomic nervous system affects the gustatory responses in animals. Frog glossopharyngeal nerve (GPN) contains the parasympathetic nerve. We checked the effects of electrical stimulation (ES) of the parasympathetic nerves on the gustatory neural responses. The gustatory neural impulses of the GPNs were recorded using bipolar AgCl wires under normal blood circulation and integrated with a time constant of 1 s. Electrical stimuli were applied to the proximal side of the GPN with a pair of AgCl wires. The parasympathetic nerves of the GPN were strongly stimulated for 10 s with 6 V at 30 Hz before taste stimulation. The integrated neural responses to 0.5 M NaCl, 2.5 mM CaCl2, water, and 1 M sucrose were enhanced to 130–140% of the controls. On the other hand, the responses for 1 mM Q-HCl and 0.3 mM acetic acid were not changed by the preceding applied ES. After hexamethonium (a blocker of nicotinic ACh receptor) was intravenously injected, ES of the parasympathetic nerve did not modulate the responses for all six taste stimuli. The mechanism for enhancement of the gustatory neural responses is discussed.


Bullfrog Gustatory neural response Parasympathetic nerve Glossopharyngeal nerve Electrical stimulation Neural modulation 



This work was supported by school running expense from Nagasaki University.

Compliance with Ethical Standards

Conflict of interest

The authors do not have any conflict of interest.

Ethical Approval

All applicable institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.


  1. Akaike N, Noma A, Sato M (1976) Electrical responses of frog taste cells to chemical stimuli. J Physiol 254:87–107CrossRefPubMedPubMedCentralGoogle Scholar
  2. Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martin JD, Candenas ML (2004) Tachykinins and tachykinin receptors: structure and activity relationships. Curr Med Chem 11:2045–2081CrossRefPubMedGoogle Scholar
  3. Beppu N, Higure Y, Mashiyama K, Ohtubo Y, Kumazawa T, Yoshii K (2012) Hypertonicity augments bullfrog taste nerve response. Pflugers Arch-Eur J Physiol 463:845–851CrossRefGoogle Scholar
  4. Ekström J, Ekman R, Håkanson R, Sjögren S, Sundler F (1988a) Calcitonin gene-related peptide in rat salivary glands: neural localization, depletion upon nerve stimulation, and effects on salivation in relation to substance P. Neuroscience 26:935–945CrossRefGoogle Scholar
  5. Ekström J, Håkansson R, Månsson B, Tobin G (1988b) Tachykinin involvement in parasympathetic nerve-evoked salivation of the ferret. Br J Pharmacol 94:707–712CrossRefPubMedPubMedCentralGoogle Scholar
  6. Filin VA, Esakov AI (1968) Interaction between taste receptors. Bull Exp Biol Med 65:9–11CrossRefGoogle Scholar
  7. Hille B (2001) Ionic channels of excitable membranes, 3rd edn. Sinauer, SunderlandGoogle Scholar
  8. Jaber L, Zhao F, Kolli T, Herness S (2014) A physiologic role for serotonergic transmission in adult rat taste buds. PLoS ONE 9:e112152CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kim BJ, Chang IY, Choi S, Jun JY, Jeon J, Xu W, Kwon YK, Ren D, So I (2012) Involvement of Na+-leak channel in substance P-induced depolarization of pacemaking activity in interstitial cells of Cajal. Cell Physiol Biochem 29:501–510CrossRefPubMedPubMedCentralGoogle Scholar
  10. Kuramoto H (1988) An immunohistochemical study of cellular and nervous elements in the taste organ of the bullfrog, Rana catesbeiana. Arch Histol Cytol 51(2):205–221CrossRefPubMedGoogle Scholar
  11. Linley JE, Ooi L, Pettinger L, Kirton H, Boyle JP, Peers C, Gamper N (2012) Reactive oxygen species are second messengers of neurokinin signaling in peripheral sensory neurons. Proc Natl Acad Sci USA 24:E1578–E1586CrossRefGoogle Scholar
  12. Linster C, Fontanini A (2014) Functional neuromodulation of chemoreception in vertebrates. Curr Opin Neurobiol 29:82–87CrossRefPubMedGoogle Scholar
  13. Lytton WW (2002) From computer to brain, foundations of computational neuroscience. Springer, New YorkGoogle Scholar
  14. Miyamoto T, Okada Y, Sato T (1988) Ionic basis of receptor potential in frog taste cells induced by acid stimuli. J Physiol 405:699–711CrossRefPubMedPubMedCentralGoogle Scholar
  15. Miyamoto T, Okada Y, Sato T (1989) Ionic basis of salt-induced receptor potential in frog taste cells. Comp Biochem Physiol 94A:591–595Google Scholar
  16. Miyamoto T, Okada Y, Sato T (1993) Cationic and anionic channels of apical receptive membrane in a frog taste cell contribute to generation of salt-induced receptor potential. Comp Biochem Physiol 105A:489–493CrossRefGoogle Scholar
  17. Murayama N, Ishiko N (1985) Effect of antidromic stimulation of the glossopharyngeal nerve on afferent discharge occurring with and without sensory stimulation of the frog tongue. Neurosci Lett 60:95–99CrossRefPubMedGoogle Scholar
  18. Murayama N, Ishiko N (1986) Selective depressant action of antidromic impulses on gustatory nerve signals. J Gen Physiol 88:219–236CrossRefPubMedGoogle Scholar
  19. Okada Y, Miyamoto T, Sato T (1986) Contribution of the receptor and basolateral membranes to the resting potential of a frog taste cell. Jpn J Physiol 36:139–150CrossRefPubMedGoogle Scholar
  20. Okada Y, Miyamoto T, Sato T (1988) Ionic mechanism of generation of receptor potential in response to quinine in frog taste cell. Brain Res 450:295–302CrossRefPubMedGoogle Scholar
  21. Okada Y, Miyamoto T, Sato T (1992) The ionic basis of the receptor potential of frog taste cells induced by sugar stimuli. J Exp Biol 162:23–36PubMedGoogle Scholar
  22. Okada Y, Miyamoto T, Sato T (1993a) The ionic basis of the receptor potential of frog taste cells induced by water stimuli. J Exp Biol 174:1–17CrossRefPubMedGoogle Scholar
  23. Okada Y, Miyamoto T, Sato T (1993b) Contribution of proton transporter to acid-induced receptor potential in frog taste cells. Comp Biochem Physiol 105A:725–728Google Scholar
  24. Otsuka M, Yoshioka K (1993) Neurotransmitter functions of mammalian tachykinins. Physiol Rev 73:229–308CrossRefPubMedGoogle Scholar
  25. Sato T (1978) Off-response in frog taste nerve and cell after stimulation of the tongue with bitter solutions. Comp Biochem Physiol 61A:339–353CrossRefGoogle Scholar
  26. Sato T, Beidler LM (1975) Membrane resistance change of the frog taste cells in response to water and NaCl. J Gen Physiol 66:735–763CrossRefPubMedPubMedCentralGoogle Scholar
  27. Sato T, Okada Y, Miyamoto T (1995) Molecular mechanisms of gustatory transductions in frog taste cells. Prog Neurobiol 46:239–287CrossRefPubMedGoogle Scholar
  28. Sato T, Toda K, Miyamoto T, Okada Y (2000) The origin of slow potentials on tongue surface induced by glossopharyngeal efferent fiber stimulation. Chem Senses 25:583–589CrossRefPubMedGoogle Scholar
  29. Sato T, Miyamoto T, Okada Y (2002) Slow potentials in taste cells induced by frog glossopharyngeal nerve stimulation. Chem Senses 27:367–374CrossRefPubMedGoogle Scholar
  30. Sato T, Okada Y, Toda K (2004) Analysis of slow hyperpolarizing potentials in frog taste cells induced by glossopharyngeal nerve stimulation. Chem Senses 29:651–657CrossRefPubMedGoogle Scholar
  31. Sato T, Okada Y, Miyazaki T, Kato Y, Toda K (2005) Taste cell responses in the frog are modulated by parasympathetic efferent fibers. Chem Senses 30:761–769CrossRefPubMedGoogle Scholar
  32. Sato T, Nishishita K, Okada Y, Toda K (2007) Characteristics of biphasic slow depolarizing and slow hyperpolarizing potential in frog taste cell induced by parasympathetic efferent stimulation. Chem Senses 32:817–823CrossRefPubMedGoogle Scholar
  33. Sato T, Nishishita K, Okada Y, Toda K (2009) Interaction between gustatory depolarizing receptor potential and efferent-induced slow depolarizing synaptic potential in frog taste cell. Cell Mol Neurobiol 29:243–252CrossRefPubMedGoogle Scholar
  34. Sato T, Nishishita K, Okada Y, Toda K (2012) Efferent fibers innervate gustatory and mechanosensitive afferent fibers in frog fungiform papillae. Chem Senses 37:315–324CrossRefPubMedGoogle Scholar
  35. Steinhoff MS, von Mentzer B, Geppetti P, Pothoulakis C, Bunnett NW (2014) Tachykinins and their receptors: contributions to physiological control and the mechanisms of disease. Physiol Rev 94:265–301CrossRefPubMedPubMedCentralGoogle Scholar
  36. Tadokoro O, Ando H, Kawahara I, Asanuma N, Okumura M, Kitagawa J, Kondo E, Yagasaki H (2016) Distribution and origin of VIP-, SP-, and phospholipase Cβ2-immunoreactive nerves in the tongue of the bullfrog, Rana catesbeiana. Anat Record 299:929–942CrossRefGoogle Scholar
  37. Taglietti V (1969) Effects of antidromic impulses on frog taste receptors. Arch Sci Biol 53:226–234Google Scholar
  38. Yoshida R, Ohkuri T, Jyotaki M, Yasuo T, Horio N, Yasumatsu K, Sanematsu K, Shigemura N, Yamamoto T, Margolskee RF, Ninomiya Y (2010) Endocannabinoids selectively enhance sweet taste. Proc Natl Acad Sci USA 107:935–939CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Division of Integrative Sensory PhysiologyNagasaki University Graduate School of Biomedical SciencesNagasakiJapan
  2. 2.Nakanoto-machiJapan

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