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The neural mechanisms of gustation: a distributed processing code

Nature Reviews Neuroscience volume 7, pages 890–901 (2006)Cite this article

Abstract

Whenever food is placed in the mouth, taste receptors are stimulated. Simultaneously, different types of sensory fibre that monitor several food attributes such as texture, temperature and odour are activated. Here, we evaluate taste and oral somatosensory peripheral transduction mechanisms as well as the multi-sensory integrative functions of the central pathways that support the complex sensations that we usually associate with gustation. On the basis of recent experimental data, we argue that these brain circuits make use of distributed ensemble codes that represent the sensory and post-ingestive properties of tastants.

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Figure 1: Schematic diagram of a taste bud, taste receptor cell and associated neurons.
Figure 2: Salt intake is explained by input from both gustatory and trigeminal nerves.
Figure 3: Anatomical overview of the central taste pathways.
Figure 4: Ensemble activity of OFC neurons discriminates and anticipates natural rewards.
Figure 5: Taste processing in the gustatory cortex is fast.
Figure 6: Functional MRI shows multimodal integration in the human taste cortex.
Figure 7: Coding of satiety states by neuronal ensembles in the rat forebrain.

References

  1. Marks, L. E. & Wheeler, M. E. Attention and the detectability of weak taste stimuli. Chem. Senses 23, 19–29 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Breslin, P. A. & Huang, L. Human taste: peripheral anatomy, taste transduction, and coding. Adv. Otorhinolaryngol. 63, 152–190 (2006).

    PubMed  Google Scholar 

  3. Desimone, J. A. & Lyall, V. Salty and sour taste: sensing of sodium and protons by the tongue. Am. J. Physiol. Gastrointest. Liver Physiol. 29 June 2006 (doi:10.1152/ajpgi.00235).

  4. Margolskee, R. F. Sensory systems: taste perception. Sci. STKE 290, tr20 (2005).

    Google Scholar 

  5. Roper, S. D. Cell communication in taste buds. Cell. Mol. Life Sci. 63, 1494–1500 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Scott, K. Taste recognition. Neuron 48, 455–464 (2005).

    Article  CAS  PubMed  Google Scholar 

  7. Smith, D. V. & St. John, S. J. Neural coding of gustatory information. Curr. Opin. Neurobiol. 9, 427–435 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. de Araujo, I. E. et al. Neural ensemble coding of satiety states. Neuron 51, 483–494 (2006).

    Article  CAS  PubMed  Google Scholar 

  9. Fontanini, A. & Katz, D. B. State-dependent modulation of time-varying gustatory responses. J. Neurophysiol. 23 Aug 2006 (doi:10.1152/jn.00804).

  10. Gutierrez, R., Carmena, J. M., Nicolelis, M. A. & Simon, S. A. Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J. Neurophysiol. 95, 119–133 (2006).

    Article  PubMed  Google Scholar 

  11. Stapleton, J. A., Lavine, M., Wolpert, R., Nicolelis, M. A. L. & Simon, S. A. Rapid taste responses in the gustatory cortex during licking. J. Neurosci. 26, 4126–4138 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Finger, T. E. & Simon, S. A. in The Neurobiology of Taste and Smell (eds Finger, T. E., Silver, W. L. & Restrepo, D.) 287–314 (Wiley-Liss, New York, 2002).

    Google Scholar 

  13. Scott, T. R. & Verhagen, J. V. Taste as a factor in the management of nutrition. Nutrition 16, 874–885 (2000).

    Article  CAS  PubMed  Google Scholar 

  14. Spector, A. C. & Travers, S. P. The representation of taste quality in the mammalian nervous system. Behav. Cogn. Neurosci. Rev. 4, 143–191 (2005).

    Article  PubMed  Google Scholar 

  15. Holland, V. F., Zampighi, G. A. & Simon, S. A. Morphology of fungiform papillae in canine lingual epithelium: location of intercellular junctions in the epithelium. J. Comp. Neurol. 279, 13–27 (1989).

    Article  CAS  PubMed  Google Scholar 

  16. Yang, J. & Roper, S. D. Dye-coupling in taste buds in the mudpuppy. J. Neurosci. 7, 3561–3565 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yoshii, K. Gap junctions among taste bud cells in mouse fungiform papillae. Chem. Senses 30, i35–i36 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Herness, S., Zhao, F. L., Kaya, N., Lu, S. G. & Cao, Y. Communication routes within the taste bud by neurotransmitters and neuropeptides. Chem. Senses 30, i37–i38 (2005).

    Article  CAS  PubMed  Google Scholar 

  19. Zhao, F. L. et al. Expression, physiological action, and coexpression patterns of neuropeptide Y in rat taste-bud cells. Proc. Natl Acad. Sci. USA 102, 11100–11105 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Danilova, V., Danilov, Y., Roberts, T. & Hellekant, G. Sense of taste of the common marmoset: recordings from the chorda tympani and glossopharyngeal nerves. J. Neurophys. 88, 579–594 (2002).

    Article  Google Scholar 

  21. Hanamori, T., Miller, I. J. Jr & Smith, D. V. Gustatory responsiveness of fibers in the hamster glossopharyngeal nerve. J. Neurophysiol. 60, 478–498 (1988).

    Article  CAS  PubMed  Google Scholar 

  22. Spector, A. C. Linking gustatory neurobiology to behavior in vertebrates. Neurosci. Biobehav. Rev. 391, 391–416 (2000).

    Article  Google Scholar 

  23. Travers, S. P. in Mechanisms of Taste Transduction (eds Simon, S. A. & Roper, S. D.) 339–395 (CRC, Boca Raton, 1993).

    Google Scholar 

  24. Finger, T. E. et al. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310, 1495–1499 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. Bigiani, A. R., Delay, R. J., Chaudhari, N., Kinnamon, S. C. & Roper, S. D. Responses to glutamate in rat taste cells. J. Neurophysiol. 77, 3048–3059 (1997).

    Article  CAS  PubMed  Google Scholar 

  26. Huang, Y. J. et al. Mouse taste buds use serotonin as a neurotransmitter. J. Neurosci. 25, 843–847 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ogura, T. Acetylcholine increases intracellular Ca2+ in taste cells via activation of muscarinic receptors. J. Neurophysiol. 87, 2643–2649 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Bradbury, J. Taste perception: cracking the code. PLoS Biol. 2, e64 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zhang, Y. et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293–301 (2003).

    Article  CAS  PubMed  Google Scholar 

  30. Adler, E. et al. A novel family of mammalian taste receptors. Cell 100, 693–702 (2000).

    Article  CAS  PubMed  Google Scholar 

  31. Chrandrashekar, J. et al. T2Rs function as bitter taste receptors. Cell 100, 703–711 (2000).

    Article  Google Scholar 

  32. Liu, D. & Liman, E. R. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc. Natl Acad. Sci. USA 100, 15160–15165 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Max, M. et al. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nature Genet. 28, 58–63 (2001).

    CAS  PubMed  Google Scholar 

  34. Montmayeur, J. P., Liberlis, S. D., Matsunami, H. & Buck, L. A candidate taste receptor gene near a sweet taste locus. Nature Neurosci. 4, 492–498 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Mueller, K. L. et al. The receptors and coding logic for bitter taste. Nature 434, 225–229 (2005).

    Article  CAS  PubMed  Google Scholar 

  36. Perez, C. A., Margolskee, R. F., Kinnamon, S. C. & Ogura, T. Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells. Cell Calcium 33, 541–549 (2003).

    Article  CAS  PubMed  Google Scholar 

  37. Zhao, G. Q. et al. The receptors for mammalian sweet and umami taste. Cell 115, 255–266 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Huang, A. L. et al. The cells and logic for mammalian sour taste detection. Nature 442, 934–938 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kellenberger, S. & Schild, L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735–767 (2002).

    Article  CAS  PubMed  Google Scholar 

  40. Nelson, G., Hoon, M. A., Chandrashekar, J., Ryba, N. J. P. & Zuker, C. S. Mammalian sweet taste receptors. Cell 106, 381–390 (2001).

    Article  CAS  PubMed  Google Scholar 

  41. Galindo-Cuspinera, V., Winnig, M., Bufe, B., Meyerhof, W. & Breslin, P. A. A TAS1R receptor-based explanation of sweet 'water-taste'. Nature 441, 354–357 (2006).

    Article  CAS  PubMed  Google Scholar 

  42. Nelson, G. et al. An amino-acid taste receptor. Nature 416, 199–202 (2002).

    Article  CAS  PubMed  Google Scholar 

  43. Rong, M. et al. Signal transduction of umami taste: insights from knockout mice. Chem. Senses 30, i33–i34 (2005).

    Article  CAS  PubMed  Google Scholar 

  44. Chaudhari, N. et al. The taste of monosodium glutamate: membrane receptors in taste buds. J. Neurosci. 16, 3817–3826 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Maruyama, Y., Pereira, E., Margolskee, R. F., Chaudhari, N. & Roper, S. D. Umami responses in mouse taste cells indicate more than one receptor. J. Neurosci. 26, 2227–2234 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Ming, D., Ninomiya, T. & Margolskee, R. F. Blocking taste receptor activation of gustducin inhibits gustatory responses to bitter compounds. Proc. Natl Acad. Sci. USA 96, 9903–9908 (2000).

    Article  Google Scholar 

  47. Parry, C. M., Erkner, A. & le Coutre, J. Divergence of T2R chemosensory receptor families in humans, bonobos, and chimpanzees. Proc. Natl Acad. Sci. USA 101, 14830–14834 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Nelson, T., Munger, S. & Boughter, J. Haplotypes at the Tas2r locus on distal chromosome 6 vary with quinine taste sensitivity in inbred mice. BMC Genet. 6, 32 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chandrashekar, J. et al. T2Rs function as bitter taste receptors. Cell 100, 703–711 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Bufe, B. et al. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr. Biol. 15, 322–327 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kim, U. K. & Drayna, D. Genetics of individual differences in bitter taste perception: lessons from the PTC gene. Clin. Genet. 67, 275–280 (2005).

    Article  CAS  PubMed  Google Scholar 

  52. Kretz, O., Barbry, P., Bock, R. & Lindemann, B. Differential expression of RNA and protein of the three pore-forming subunits of the amiloride-sensitive epithelial sodium channel in taste buds of the rat. J. Histochem. Cytochem. 47, 51–64 (1999).

    Article  CAS  PubMed  Google Scholar 

  53. Schiffman, S. S., Lockhead, E. & Maes, F. W. Amiloride reduces the taste intensity of Na+ and Li+ salts and sweeteners. Proc. Natl Acad. Sci. USA 80, 6136–6140 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. DeSimone, J. A. & Ferrell, F. Analysis of amiloride inhibition of chorda tympani taste response of rat to NaCl. Am. J. Physiol. Cell Physiol. 249, R52–R61 (1985).

    CAS  Google Scholar 

  55. Elliott, E. J. & Simon, S. A. The anion in salt taste: a possible role of tight junctions. Brain Res. 535, 9–17 (1990).

    Article  CAS  PubMed  Google Scholar 

  56. Ossebaard, C. A. & Smith, D. V. Effect of amiloride on the taste of NaCl, Na-gluconate and KCl in humans: implications for Na+ receptor mechanisms. Chem. Senses 20, 37–46 (1995).

    Article  CAS  PubMed  Google Scholar 

  57. Schiffman, S. S. Taste quality and neural coding: implications from psychophysics and neurophysiology. Physiol. Behav. 69, 147–159 (2000).

    Article  CAS  PubMed  Google Scholar 

  58. Stevens, D. A., Smith, R. F. & Lawless, H. T. Multidimensional scaling of ferrous sulfate and basic tastes. Physiol. Behav. 87, 272–279 (2006).

    Article  CAS  PubMed  Google Scholar 

  59. Lyall, V. et al. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J. Physiol. 558, 147–159 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lyall, V. et al. A novel vanilloid receptor-1 (VR-1) variant mammalian salt taste receptor. Chem. Senses 30, i42–i43 (2005).

    Article  CAS  PubMed  Google Scholar 

  61. Ishimaru, Y. et al. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc. Natl Acad. Sci. USA 103, 12569–12574 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. LopezJimenez, N. D. et al. Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J. Neurochem. 98, 68–77 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. Lyall, V. et al. Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction. Am. J. Physiol. Cell Physiol. 281, C1005–C1013 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. French, S. & Robinson, T. Fats and food intake. Curr. Opin. Clin. Nutr. Metab. Care 6, 629–634 (2003).

    Article  CAS  PubMed  Google Scholar 

  65. Kadohisa, M., Verhagen, J. V. & Rolls, E. T. The primate amygdala: neuronal representations of the viscosity, fat texture, temperature, grittiness and taste of foods. Neuroscience 132, 33–48 (2005).

    Article  CAS  PubMed  Google Scholar 

  66. Rolls, E. T. Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol. Behav. 85, 45–56 (2005).

    Article  CAS  PubMed  Google Scholar 

  67. Laugerette, F. et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115, 3177–3184 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kawai, T. & Fushiki, T. Importance of lipolysis in oral cavity for orosensory detection of fat. Am. J. Physiol 285, R447–R454 (2003).

    CAS  Google Scholar 

  69. Gilbertson, T. A., Fontenot, D. T., Liu, L., Zhang, H. & Monroe, W. T. Fatty acid modulation of K+ channels in taste receptor cells: gustatory cues for dietary fat. Am. J. Physiol. Cell Physiol. 272, C1203–C1210 (1997).

    Article  CAS  Google Scholar 

  70. Gilbertson, T. A., Liu, L., Kim, I., Burks, C. A. & Hansen, D. R. Fatty acid responses in taste cells from obesity-prone and -resistant rats. Physiol. Behav. 86, 681–690 (2005).

    Article  CAS  PubMed  Google Scholar 

  71. Lindemann, B. Sodium taste. Curr. Opin. Neph. Hypertens. 6, 425–429 (1997).

    Article  CAS  Google Scholar 

  72. Rajan, R., Clement, J. P. & Bhalla, U. S. Rats smell in stereo. Science 311, 667–670 (2006).

    Article  CAS  Google Scholar 

  73. Lu, S. G., Kaya, N. & Herness, M. S. Cholecystokinin increases intracellular calcium levels in rat posterior taste receptor cells. Chem. Senses 25, 685 (2000).

    Google Scholar 

  74. Zhao, F. L. & Herness, M. S. Physiological actions of cholecystokinin on rat taste receptor cells. Chem. Senses 26, 1065 (2001).

    Google Scholar 

  75. Cruz, A. & Green, B. G. Thermal stimulation of taste. Nature 403, 889–892 (2000).

    Article  CAS  PubMed  Google Scholar 

  76. Bartoshuck, L. M., Rennert, K., Rodin, J. & Stevens, J. C. Effects of temperature on the perceived sweetness of sucrose. Physiol. Behav. 28, 905–910 (2001).

    Article  Google Scholar 

  77. Talavera, K. et al. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438, 1022–1025 (2005).

    Article  CAS  PubMed  Google Scholar 

  78. Green, B. G. Sensory interactions between capsaicin and temperature. Chem. Senses 11, 371–382 (1986).

    Article  CAS  Google Scholar 

  79. Liu, L. & Simon, S. A. Capsaicin, acid and heat evoked currents in rat trigeminal ganglion neurons: evidence for functional VR1 receptors. Physiol. Behav 69, 363–378 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Patapoutaian, A. TRP channels and thermoreception. Chem. Senses 30, i193–i194 (2005).

    Article  CAS  Google Scholar 

  81. Halata, H. & Munger, B. L. The sensory innervation of primate facial skin 11 Vermilion boarder and mucosa of lip. Brain Res. Rev. 5, 81–107 (1983).

    Article  Google Scholar 

  82. Munger, B. L. in Mechanisms of Taste Transduction (eds Simon, S. A. & Roper, S. D.) 83–102 (CRC, Boca Raton, 1993).

    Google Scholar 

  83. Liu, L. & Simon, S. A. Capsaicin-induced currents with distinct desensitization and Ca+ dependence in rat trigeminal ganglion cells. J. Neurophysiol. 75, 1503–1514 (1996).

    Article  CAS  PubMed  Google Scholar 

  84. Wang, Y., Erickson, R. E. & Simon, S. A. Modulation of chorda tympani nerve activity by lingual nerve stimulation. J. Neurophysiol. 73, 1468–1483 (1995).

    Article  CAS  PubMed  Google Scholar 

  85. Chuang, H. H., Neuhausser, W. M. & Julius, D. The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43, 859–869 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Xu, H., Delling, M., Jun, J. C. & Clapham, D. E. Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nature Neurosci. 9, 628–635 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Carstens, E., Kuenzler, N. & Handwerker, K. O. Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to the oral or ocular mucosa. J. Neurophysiol. 80, 465–492 (1998).

    Article  CAS  PubMed  Google Scholar 

  88. Simons, C. T., Dressier, J. M., Carstens, M. I., O'Mahoney, M. & Carstens, E. Neurobiological and psychophysical mechanisms underlying the oral sensation produced by carbonated water. J. Neurosci. 15, 8134–8144 (1999).

    Article  Google Scholar 

  89. Wang, Y., Erickson, R. P. & Simon, S. A. Selectivity of lingual nerve fibers to chemical stimuli. J. Gen. Physiol. 101, 843–866 (1993).

    Article  CAS  PubMed  Google Scholar 

  90. Danilova, V. & Hellekant, G. Oral sensation of ethanol in a primate model III: responses in the lingual branch of the trigeminal nerve of Macaca mulatta. Alcohol 26, 3–16 (2002).

    Article  CAS  PubMed  Google Scholar 

  91. Bennick, A. Interaction of plant polyphenols with salivary proteins. Crit. Rev. Oral Bio. Med. 13, 184–196 (2002).

    Article  Google Scholar 

  92. Breslin, P. A. S., Gilmore, M. M., Beauchamp, G. K. & Green, B. G. Physiophysical evidence that oral astringency is a tactile sensation. Chem. Senses 18, 405–417 (1993).

    Article  CAS  Google Scholar 

  93. Kawamura, Y., Okamoto, J. & Funakoshi, M. A role of oral afferents in aversion to taste solutions. Physiol. Behav. 3, 537–542 (1968).

    Article  CAS  Google Scholar 

  94. Erickson, R. P. Stimulus coding in topographic and non-topographic afferent modalities. Psychol. Rev. 75, 447–465 (1968).

    Article  CAS  PubMed  Google Scholar 

  95. Frank, M. An analysis of hamster afferent taste nerve response functions. J. Gen. Physiol. 61, 588–618 (1973).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Pfaffman, C. The afferent code for sensory quality. Am. Psychol. 14, 226–232 (1959).

    Article  Google Scholar 

  97. Caicedo, A., Kim, K. N. & Roper, S. D. Individual mouse taste cells respond to multiple chemical stimuli. J. Physiol. 544, 501–509 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Gilbertson, T. A., Boughter, J. D., Zhang, H. & Smith, D. V. Distribution of gustatory sensitivities in rat taste cells: whole-cell responses to apical chemical stimulation. J. Neurosci. 27, 4931–4941 (2001).

    Article  Google Scholar 

  99. Boudreau, J. C. et al. Neurophysiology of geniculate ganglion (facial nerve) taste systems: species comparisons. Chem. Senses 10, 89–127 (1985).

    Article  Google Scholar 

  100. Frank, M. F. Taste responsive neurons of the glossopharnygeal nerve of the rat. J. Neurophysiol. 65, 1452–1462 (1991).

    Article  CAS  PubMed  Google Scholar 

  101. Frank, M. F., Bieber, S. L. & Smith, D. V. The organization of taste sensibilities in hamster chorda tympani nerve fibers. J. Gen. Physiol. 91, 861–896 (1988).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Danilova, V. & Hellekant, G. Sense of taste in a new world monkey, the common marmoset. II. Link between behavior and nerve activity. J. Neurophys. 92, 1067–1076 (2004).

    Article  Google Scholar 

  103. Hellekant, G., Ninomiya, T. & Danilova, V. Taste in chimpanzees. III: Labeled-line coding in sweet taste. Physiol. Behav. 65, 191–200 (1998).

    Article  CAS  PubMed  Google Scholar 

  104. Grill, H. J. & Norgren, R. Chronically decerebrate rats demonstrate satiation but not bait shyness. Science 201, 267–269 (1978).

    Article  CAS  PubMed  Google Scholar 

  105. Jones, L. M., Fontanini, A. & Katz, D. B. Gustatory processing: a dynamic systems approach. Curr. Opin. Neurobiol. 16, 420–428 (2006).

    Article  CAS  PubMed  Google Scholar 

  106. Hamilton, R. B. & Norgren, R. Central projections of gustatory nerves in the rat. J. Comp. Neurol. 222, 560–577 (1984).

    Article  CAS  PubMed  Google Scholar 

  107. Boucher, Y., Simons, C. T., Faurion, A., Azerad, J. & Carstens, E. Trigeminal modulation of gustatory neurons in the nucleus of the solitary tract. Brain Res. 973, 265–274 (2003).

    Article  CAS  PubMed  Google Scholar 

  108. van Buskirk, R. L. & Erickson, R. P. Responses in the rostral medulla to electrical stimulation of an intranasal trigeminal nerve convergence of oral and nasal inputs. Neurosci. Lett. 5, 312–326 (2003).

    Google Scholar 

  109. Travagli, R. A., Hermann, G. E., Browning, K. N. & Rogers, R. C. Brainstem circuits regulating gastric function. Annu. Rev. Physiol. 68, 279–305 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Zhang, X., Fogel, R. & Renehan, W. E. Relationships between the morphology and function of gastric- and intestine-sensitive neurons in the nucleus of the solitary tract. J. Comp. Neurol. 363, 37–52 (1995).

    Article  CAS  PubMed  Google Scholar 

  111. Berthoud, H. R., Earle, T., Zheng, H., Patterson, L. M. & Phifer, C. Food-related gastrointestinal signals activate caudal brainstem neurons expressing both NMDA and AMPA receptors. Brain Res. 915, 143–154 (2001).

    Article  CAS  PubMed  Google Scholar 

  112. Glenn, J. F. & Erickson, R. P. Gastric modulation of gustatory afferent activity. Physiol. Behav. 16, 561–568 (1976).

    Article  Google Scholar 

  113. Simons, C. T., Boucher, Y., Iodi-Carstens, M. & Carstens, E. Nicotine suppression of gustatory responses of neurons in the nucleus of the solitary tract. J. Neurophys. 96, 1877–1886 (2006).

    Article  CAS  Google Scholar 

  114. Norgren, R. & Grill, H. J. in The Physiological Mechanisms of Motivation (ed. Pfaff, D. W.) 99–131 (Springer, New York, 1982).

    Book  Google Scholar 

  115. Cunningham, E. T. Jr & Sawchenko, P. E. Dorsal medullary pathways subserving oromotor reflexes in the rat: implications for the central neural control of swallowing. J. Comp. Neurol. 417, 448–466 (2000).

    Article  PubMed  Google Scholar 

  116. Travers, J. B., Dinardo, L. A. & Karimnamazi, H. Motor and Premotor Mechanisms of Licking. Neurosci. Biobehav. Rev. 21, 631–647 (1997).

    Article  CAS  PubMed  Google Scholar 

  117. Travers, S. P. & Norgren, R. Organization of orosensory responses in the nucleus of the solitary tract of rat. J. Neurophysiol. 73, 2144–2162 (1995).

    Article  CAS  PubMed  Google Scholar 

  118. Sugita, M. & Shiba, Y. Genetic tracing shows segregation of taste circuitries for bitter and sweet. Science 309, 781–785 (2005).

    Article  CAS  PubMed  Google Scholar 

  119. Scott, T. R., Yaxley, S., Sienkiewicz, Z. J. & Rolls, E. T. Taste responses in the nucleus tractus solitarius of the behaving monkey. J. Neurophysiol. 55, 182–200 (1986).

    Article  CAS  PubMed  Google Scholar 

  120. Lemon, C. H. & Smith, D. V. Neural representation of bitter taste in the nucleus of the solitary tract. J. Neurophysiol. 94, 3719–3729 (2005).

    Article  CAS  PubMed  Google Scholar 

  121. Lemon, C. H. & Smith, D. V. Influence of response variability on the coding performance of central gustatory neurons. J. Neurosci. 26, 7433–7443 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Di Lorenzo, P. M., Halloak, R. M. & Kennedy, D. P. Temporal coding of sensation: mimicking taste quality with electrical stimulation of the brain. Behav. Neurosci. 117, 1423–1433 (2003).

    Article  PubMed  Google Scholar 

  123. van der Kooy, D., Koda, L. Y., McGinty, J. F., Gerfen, C. R. & Bloom, F. E. The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. J. Comp. Neurol. 224, 1–24 (1984).

    Article  CAS  PubMed  Google Scholar 

  124. Whitehead, M. C., Bergula, A. & Holliday, K. Forebrain projections to the rostral nucleus of the solitary tract in the hamster. J. Comp. Neurol. 422, 429–447 (2000).

    Article  CAS  PubMed  Google Scholar 

  125. Di Lorenzo, P. M. & Monroe, S. Corticofugal influence on taste responses in the nucleus of the solitary tract in the rat. J. Neurophysiol. 74, 258–272 (1995).

    Article  CAS  PubMed  Google Scholar 

  126. Smith, D. V., Li, C. S. & Cho, Y. K. Forebrain modulation of brainstem gustatory processing. Chem. Senses 30, i176–i177 (2005).

    Article  PubMed  Google Scholar 

  127. Tokita, K., Karadi, Z., Shimura, T. & Yamamoto, T. Centrifugal inputs modulate taste aversion learning associated parabrachial neuronal activities. J. Neurophysiol. 92, 265–279 (2004).

    Article  PubMed  Google Scholar 

  128. Li, C. S., Cho, Y. K. & Smith, D. V. Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. J. Neurophysiol. 93, 1183–1196 (2005).

    Article  PubMed  Google Scholar 

  129. Lundy, R. F. Jr & Norgren, R. Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J. Neurophysiol. 91, 1143–1157 (2004).

    Article  PubMed  Google Scholar 

  130. Di Lorenzo, P. M. Corticofugal influence on taste responses in the parabrachial pons of the rat. Brain Res. 530, 73–84 (1990).

    Article  CAS  PubMed  Google Scholar 

  131. Erickson, R. P. A neural metric. Neurosci. Behav. Rev. 10, 377–386 (1986).

    Article  CAS  Google Scholar 

  132. Katz, D. B., Nicolelis, M. A. & Simon, S. A. Gustatory processing is dynamic and distributed. Curr. Opin. Neurobiol. 12, 448–454 (2002).

    Article  CAS  PubMed  Google Scholar 

  133. Kadohisa, M., Rolls, E. T. & Verhagen, J. V. Neuronal representations of stimuli in the mouth: the primate insular taste cortex, orbitofrontal cortex and amygdala. Chem. Senses 30, 401–419 (2005).

    Article  PubMed  Google Scholar 

  134. Hanamori, T., Kunitake, T., Kato, K. & Kannan, H. Responses of neurons in the insular cortex to gustatory, visceral and nociceptive stimuli in rats. J. Neurophysiol. 79, 2535–2545 (1998).

    Article  CAS  PubMed  Google Scholar 

  135. Hanamori, T., Kunitake, T., Kato, K. & Kannan, H. Neurons in the posterior insular cortex are responsive to gustatory stimulation of the pharyngolarnyx, baroreceptors and chemoreceptor stimulation and tail pinch in rats. Brain Res. 785, 97–106 (1999).

    Article  Google Scholar 

  136. Katz, D. B., Simon, S. A. & Nicolelis, M. A. Taste-specific neuronal ensembles in the gustatory cortex of awake rats. J. Neurosci. 22, 1850–1857 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Halpern, B. P. & Tapper, D. N. Taste stimuli: quality coding time. Science 171, 1256–1258 (1971).

    Article  CAS  PubMed  Google Scholar 

  138. Katz, D. B., Simon, S. A. & Nicolelis, M. A. Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J. Neurosci. 21, 4478–4489 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Ogawa, H. & Wang, X. D. Neurons in the cortical taste area receive nociceptive inputs from the whole body as well as the oral cavity in the rat. Neurosci. Lett. 322, 87–90 (2002).

    Article  CAS  PubMed  Google Scholar 

  140. Yamamoto, T., Yuyama, N. & Kawamura, Y. Cortical neurons responding to tactile, thermal and taste stimulations of the rat tongue. Brain Res. 221, 411–415 (1981).

    Article  Google Scholar 

  141. Dalton, P., Doolittle, N., Nagata, H. & Breslin, P. A. S. The merging of the senses: integration of subthreshold taste and smell. Nature Neurosci. 3, 431–432 (2000).

    Article  CAS  PubMed  Google Scholar 

  142. Todrank, J. & Bartoshuk, L. M. A taste illusion: taste sensation localized by touch. Physiol. Behav. 50, 1027–1031 (1991).

    Article  CAS  PubMed  Google Scholar 

  143. Ito, S. & Ogawa, H. Neural activity in fronto-opercular cortex of macaque monkeys during tasting and mastication. Jpn J. Physiol. 44, 141–156 (1994).

    Article  CAS  PubMed  Google Scholar 

  144. Scott, T. R., Yaxley, S., Sienkiewicz, Z. J. & Rolls, E. T. Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. J. Neurophysiol. 56, 876–890 (1986).

    Article  CAS  PubMed  Google Scholar 

  145. de Araujo, I. E. & Rolls, E. T. Representation in the human brain of food texture and oral fat. J. Neurosci. 24, 3086–3093 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Zald, D. H. & Pardo, J. V. Cortical activation induced by intraoral stimulation with water in humans. Chem. Senses 25, 267–276 (2000).

    Article  CAS  PubMed  Google Scholar 

  147. Rolls, E. T., Critchley, H. D., Browning, A. S., Hernadi, A. & Lenard, L. Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J. Neurosci. 19, 1532–1540 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Verhagen, J. V., Rolls, E. T. & Kadohisa, M. Neurons in the primate orbitofrontal cortex respond to fat texture independently of viscosity. J. Neurophys. 90, 1514–1525 (2003).

    Article  Google Scholar 

  149. Franks, K. M. & Isaacson, J. S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49, 357–363 (2006).

    Article  CAS  PubMed  Google Scholar 

  150. Sewards, T. V. & Sewards, M. A. Cortical association areas in the gustatory system. Neurosci. Biobehav. Rev. 25, 395–407 (2001).

    Article  CAS  PubMed  Google Scholar 

  151. Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M. & Evans, A. C. Flavor processing: more than the sum of its parts. Neuroreport 8, 3913–3917 (1997).

    Article  CAS  PubMed  Google Scholar 

  152. de Araujo, I. E., Rolls, E. T., Kringelbach, M. L., McGlone, F. & Phillips, N. Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur. J. Neurosci. 18, 2059–2068 (2003).

    Article  PubMed  Google Scholar 

  153. Small, D. M. et al. Experience-dependent neural integration of taste and smell in the human brain. J. Neurophysiol. 92, 1892–1903 (2004).

    Article  PubMed  Google Scholar 

  154. Mickley, G. A. et al. Dynamic processing of taste aversion extinction in the brain. Brain Res. 1016, 79–89 (2004).

    Article  CAS  PubMed  Google Scholar 

  155. Garcia, J., Kimeldorf, D. J. & Koelling, R. A. Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122, 157–158 (1955).

    CAS  PubMed  Google Scholar 

  156. Sclafani, A. Post-ingestive positive controls of ingestive behavior. Appetite 36, 79–83 (2001).

    Article  CAS  PubMed  Google Scholar 

  157. Rolls, E. T., Murzi, E., Yaxley, S., Thorpe, S. J. & Simpson, S. J. Sensory-specific satiety: food-specific reduction in responsiveness of ventral forebrain neurons after feeding in the monkey. Brain Res. 368, 79–86 (1986).

    Article  CAS  PubMed  Google Scholar 

  158. Rolls, E. T., Sienkiewicz, Z. J. & Yaxley, S. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur. J. Neurosci. 1, 53–60 (1989).

    Article  PubMed  Google Scholar 

  159. O'Doherty, J., Rolls, E. T., Francis, S., Bowtell, R. & McGlone, F. Representation of pleasant and aversive taste in the human brain. J. Neurophys. 85, 1315–1321 (2001).

    Article  CAS  Google Scholar 

  160. Small, D. M., Zatorre, R. J., Dagher, A., Evans, A. C. & Jones-Gotman, M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 124 1720–1733 (2001).

    Article  CAS  PubMed  Google Scholar 

  161. Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107 (2004).

    Article  CAS  Google Scholar 

  162. O'Doherty, J. et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 399–403 (2000).

    Article  CAS  PubMed  Google Scholar 

  163. de Araujo, I. E., Kringelbach, M. L., Rolls, E. T. & McGlone, F. Human cortical responses to water in the mouth, and the effects of thirst. J. Neurophysiol. 90, 1865–1876 (2003).

    Article  PubMed  Google Scholar 

  164. Bermudez-Rattoni, F. Molecular mechanisms of taste-recognition memory. Nature Rev. Neurosci. 5, 209–217 (2004).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported in part by grants from the National Institutes of Health, from Philip Morris Inc. USA and Philip Morris International.

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Authors and Affiliations

  1. Departments of Neurobiology and Anesthesiology,

    Sidney A. Simon

  2. Duke University, Durham, 27710, North Carolina, USA

    Sidney A. Simon

  3. Department of Neurobiology and the Center for Neuroengineering,

    Ivan E. de Araujo

  4. Duke University, Durham, 27710, North Carolina, USA

    Ivan E. de Araujo

  5. Department of Neurobiology,

    Ranier Gutierrez

  6. Duke University, Durham, 27710, North Carolina, USA

    Ranier Gutierrez

  7. the Departments of Neurobiology, Biomedical Engineering and Psychological and Brain Science, Duke University, Durham, 27710, North Carolina, USA

    Miguel A. L. Nicolelis

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  1. Sidney A. Simon
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  4. Miguel A. L. Nicolelis
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Glossary

Amiloride

A potassium-sparing diuretic that inhibits epithelial sodium channels (ENaCs) in the kidney and in taste receptor cells.

Carbonic anhydrase

Family of zinc-containing enzymes that catalyse the rapid interconversion of carbon dioxide and water into protons and bicarbonate ions.

Cholecystokinin

(CCK). A peptide hormone secreted from the mucosal epithelial cells in the small intestine (duodenum) that causes the release of digestive enzymes from the pancreas. Peripheral and central administration of CCK reduces appetite.

Chorda tympani nerve

Branch of cranial nerve VII that innervates the front two-thirds of the tongue and carries taste information to the brain.

Conditioned taste aversion

(CTA). This is a one-trial form of learning that occurs when a palatable tastant becomes aversive after pairing with gastric malaise.

ENaC/Deg

Epithelial sodium channel (ENaC)/degenerin (Deg) is a superfamily of ion channels involved in epithelial Na+ transport, mechanotransduction and neurotransmission.

Forebrain

The anterior portion of the brain that includes the telencephalon and the diencephalon. It contains the cerebral cortex, the thalamus and the hypothalamus.

Gap junction

A junction between two cells consisting of pores that allow the passage of molecules (up to 1 kDa).

Glossopharyngeal nerve

Cranial nerve IX, receiving sensory fibres from the posterior one-third of the tongue, the tonsils and the pharynx.

Greater superior petrosal nerve

Branch of cranial nerve VII that innervates the back of the tongue and palate.

Gustducin

A G protein that is almost exclusively expressed in taste cells.

Neuropeptide Y

(NPY). A member of the pancreatic polypeptide hormone family, this peptide is produced and released by cell groups located in the hypothalamic arcuate nucleus. Central administration of NPY increases food intake and metabolism.

Purinergic receptors

These receptors are ion channels that are activated by ATP.

Sensory-specific satiety

Term referring to a specific reduction in the reward value of a particular food that has been eaten until satiety.

Superior laryngeal branch

Nerve that arises from the inferior vagal ganglion inferior to the pharyngeal branch of the vagus nerve.

Temporal coding models

These models propose that information on taste identity and quality is encoded in the temporal structure of spike trains.

TRPM5

A cation channel member of the transient receptor potential superfamily (subfamily M, member 5). Regulation of TRPM5 by Ca2+ could mediate transduction in taste receptor cells. It is required for the normal transduction of sweet, bitter and umami tastes.

Umami

A Japanese word used to describe the fifth primary taste. It corresponds to the savoury taste of food as produced, for example, by monosodium glutamate. Umami taste is found in vegetables, fish, meats and cheese.

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Simon, S., de Araujo, I., Gutierrez, R. et al. The neural mechanisms of gustation: a distributed processing code. Nat Rev Neurosci 7, 890–901 (2006). https://doi.org/10.1038/nrn2006

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