Stimulation of Bitterness by Capsaicin and Menthol: Differences Between Lingual Areas Innervated by the Glossopharyngeal and Chorda Tympani Nerves

B. G. Green
2003 Chemical Senses  
Capsaicin is viewed as a purely chemesthetic stimulus that selectively stimulates the somatosensory system. Here we show that when applied to small areas of the tongue, capsaicin can produce a bitter taste as well as sensory irritation. In experiment 1, individuals were screened for the ability to perceive bitterness from capsaicin on the circumvallate papillae. Fifteen of 25 subjects who reported at least weak bitterness rated the intensity of taste, irritation and coolness produced by 100-320
more » ... µM capsaicin and 100-320 mM menthol applied via cotton swabs to the tip (fungiform region), the posterior edge (foliate region), and the dorsal posterior surface (circumvallate region) of the tongue. Sucrose, citric acid, sodium chloride and quinine hydrochloride were applied to the same areas to assess tastes responsiveness. On average, capsaicin and menthol produced 'moderate' bitterness (and no other significant taste qualities) in the circumvallate region, and weaker bitterness on the side and tip of the tongue. Sensory irritation from capsaicin was rated significantly higher at the tongue tip, whereas menthol coolness was rated higher in the circumvallate region. In experiment 2 we applied sucrose and quinine hydrochloride together with capsaicin to investigate the effects other taste stimuli might have on capsaicin's reported bitterness. As expected, adding quinine produced stronger bitterness in the circumvallate and fungiform regions, and adding sucrose significantly reduced the bitterness of capsaicin in the circumvallate region. Overall, the results suggest that capsaicin and menthol are capable of stimulating a subset of taste neurons that respond to bitter substances, perhaps via receptor-gated ion channels like those recently found in capsaicin-and menthol-sensitive trigeminal ganglion neurons, and that the glossopharyngeal nerve may contain more such neurons than the chorda tympani nerve. That some people fail to perceive bitterness from capsaicin further implies that the incidence of capsaicin-sensitive taste neurons varies across people as well as between gustatory nerves. T2Rs function as bitter taste receptors. Cell, 100, 703-711. Cliff , M.A. and Green, B.G. (1994) Sensory irritation and coolness produced by menthol: evidence for selective desensitization of irritation. Physiol. Behav., 56, 1021-1029. Cliff, M.A. and Green, B.G. (1996) Sensitization and desensitization to menthol and capsaicin in the oral cavity: interactions and individual differences. Physiol. Behav., 59, 487-494. Stimulation of Bitterness by Capsaicin and Menthol 53 Collings, V.B. (1974) Human taste response as a function of locus of stimulation on the tongue and soft palate. Percept. Psychophys., 16, 169-174. Cowart, B.J. (1987) Oral chemical irritation: does it reduce perceived taste intensity? Chem. Senses, 12, 467-479. Cowart, B.J. (1998) The addition of CO2 to traditional taste solutions alters taste quality. Chem. Senses, 23, 397-402. Dessirier, J.M., O'Mahony, M. and Carstens, E. (1997) Oral irritant effects of nicotine: psychophysical evidence for decreased sensation following repeated application and lack of cross-desensitization to capsaicin. Chem. Senses, 22, 483-492. Dessirier, J.M., Nguyen, N., Sieffermann, J.M. Carstens, E. and O'Mahony, M. (1999) Oral irritant properties of piperine and nicotine: psychophysical evidence for asymmetrical desensitization effects. Chem. Senses, 24, 405-413. Dessirier, J.M., Simons, C.T., Sudo, M., Sudo, S. and Carstens, E. (2000) Sensitization, desensitization and stimulus-induced recovery of trigeminal neuronal responses to oral capsaicin and nicotine. The oral sensation of carbonated water: cross-desensitization by capsaicin and potentiation by amiloride. Chem. Senses, 26, 639-643. Dessirier, J.M., O'Mahony, M. and Carstens, E. (2001b) Oral irritant properties of menthol: sensitizing and desensitizing effects of repeated application and cross-desensitization to nicotine. Physiol. Behav., 73, 25-36. Karrer, T. and Bartoshuk, L. (1991) Capsaicin desensitization and recovery on the human tongue. Physiol. Behav., 49, 757-764. Karrer, T. and Bartoshuk, L. (1995) Effects of capsaicin desensitization on taste in humans. Physiol. Behav., 57, 421-429. Katz, D.B., Simon, S.A. and Nicolelis, M.A. (2002) Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J. Neurosci., 22, 1850-1857. Kawamura, Y. and Adachi, A. (1967) Electrophysiological analysis of taste effectiveness of soda water and CO2 gas. In Hayashi, T. (ed.), Olfaction and Taste II. Pergamon, New York, pp. 431-437. Komai, M., Bryant, B., Takeda, T., Suzuki, H. and Kimura, S. (1994) The effect of carbonic anhydrase inhibitor, MK-927, on the response of the chorda tympani nerve to carbonated water. In Kurikara, K., Suzuki, N. and Ogawa, H. (eds), Olfaction and Taste XI. Springer, Tokyo, pp. 92-99. Kinnman, E. and Aldskogius, H. (1991) The role of substance P and calcitonin gene-related peptide containing nerve fibers in maintaining fungiform taste buds in the rat after a chronic chorda tympani nerve injury. Exp. Neurol., 113, 85-91. Koyama, N. and Kurihara, K. (1972) Mechanism of bitter taste reception: interaction of bitter compounds with monolayers of lipids from bovine circumvallate papillae. Biochim. Biophys. Acta, 288, 22-26. Kroeze, J.H. (1980) Masking in two-and three-component taste mixtures. In Van der Starre, H. (ed.), Olfaction and Taste VII. IRL Press, London, pp. 435-448. Kumar, R., Pratt, J.A. and Stolerman, I.P. (1983) Characteristics of conditioned taste aversion produced by nicotine in rats. Br. J. Pharmacol., 79, 245-253. 54 B.G. Green and M.T. Schullery
doi:10.1093/chemse/28.1.45 pmid:12502523 fatcat:nrag32mhifcsjkgfjxzvzps6zq