Journal of Neurocytology

, Volume 33, Issue 6, pp 631–646 | Cite as

Building sensory receptors on the tongue

  • Bruce Oakley
  • Martin WittEmail author


Neurotrophins, neurotrophin receptors and sensory neurons are required for the development of lingual sense organs. For example, neurotrophin 3 sustains lingual somatosensory neurons. In the traditional view, sensory axons will terminate where neurotrophin expression is most pronounced. Yet, lingual somatosensory axons characteristically terminate in each filiform papilla and in each somatosensory prominence within a cluster of cells expressing the p75 neurotrophin receptor (p75NTR), rather than terminating among the adjacent cells that secrete neurotrophin 3. The p75NTR on special specialized clusters of epithelial cells may promote axonal arborization in vivo since its over-expression by fibroblasts enhances neurite outgrowth from overlying somatosensory neurons in vitro. Two classical observations have implicated gustatory neurons in the development and maintenance of mammalian taste buds—the early arrival times of embryonic innervation and the loss of taste buds after their denervation in adults. In the modern era more than a dozen experimental studies have used early denervation or neurotrophin gene mutations to evaluate mammalian gustatory organ development. Necessary for taste organ development, brain-derived neurotrophic factor sustains developing gustatory neurons. The cardinal conclusion is readily summarized: taste buds in the palate and tongue are induced by innervation. Taste buds are unstable: the death and birth of taste receptor cells relentlessly remodels synaptic connections. As receptor cells turn over, the sensory code for taste quality is probably stabilized by selective synapse formation between each type of gustatory axon and its matching taste receptor cell. We anticipate important new discoveries of molecular interactions among the epithelium, the underlying mesenchyme and gustatory innervation that build the gustatory papillae, their specialized epithelial cells, and the resulting taste buds.


Neurotrophin Receptor Taste Receptor Cell Axonal Arborization Enhance Neurite Outgrowth Early Arrival Time 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. AGERMAN, K., HERLING-LEFFLER, J., BLANCHARD, M. P., SCARFONE, E., CANLON, B., NOSRAT, C. & ERNFORS, P. (2003) BDNF gene replacement reveals multiple mechanisms for establishing neurotrophin specificity during sensory nervous system development. Development 130, 1479–1491.CrossRefPubMedGoogle Scholar
  2. BARRY, M. A. & SAVOY, L. D. (1993). Persistence and calcium-dependent ATPase staining of denervated fungiform taste buds in the hamster. Archives of Oral Biology 38, 5–15.CrossRefPubMedGoogle Scholar
  3. BARLOW, L. A. (1999) A taste for development. Neuron 22, 209–212.CrossRefPubMedGoogle Scholar
  4. BARLOW, L.A., CHIEN. C.-B. & NORTHCUTT, R. G. (1996) Embryonic taste buds develop in the absence of innervation. Development 122, 1103–1111.PubMedGoogle Scholar
  5. BARLOW, L. A. & NORTHCUTT, R. G. (1997) Taste buds develop autonomously from endoderm without induction by cephalic neural crest or paraxial mesoderm. Development 124, 949–957.PubMedGoogle Scholar
  6. BEIDLER, L. M. & SMALLMAN, R. L. (1965) Renewal of cells within taste buds. Journal of Cell Biology 27, 263–272.CrossRefPubMedGoogle Scholar
  7. BIGIANI, A., GHIARONI, V. & FIENI, F. (2003) Channels as taste receptors in vertebrates. Progress in Biophysics & Molecular Biology 83, 193–225.Google Scholar
  8. BIGIANI, A. R. & ROPER, S. D. (1991) Mediation of responses to calcium in taste cells by modulation of a potassium conductance. Science 252, 126–128.PubMedGoogle Scholar
  9. BITGOOD, M. J. & MCMAHON, A. P. (1995). Hedgehog and bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Developmental Biology 172, 126–138.CrossRefPubMedGoogle Scholar
  10. BROCKES, J. P. (1997) Amphibian limb regeneration: Rebuilding a complex structure. Science 276, 81–87.CrossRefPubMedGoogle Scholar
  11. CHEAL, M., DICKEY, W. P., JONES, L. B. & OAKLEY, B. (1977) Taste fiber responses during reinnervation of fungiform papillae. The Journal of Comparative Neurology 172, 627–646.PubMedGoogle Scholar
  12. COOPER, D. & OAKLEY, B. (1998) Functional redundancy and gustatory development in bdnf null mutant mice. Developmental Brain Research 105, 79–84.CrossRefGoogle Scholar
  13. DECKWERTH, T. L., ELLIOTT, L. L., KNUDSON, C. M., JOHNSON, E. M., SNIDER, W. D. & KORSMEYER, S. J. (1996) Bax is required for neuronal death after trophic factor deprivation and during development. Neuron 17, 401–411.CrossRefPubMedGoogle Scholar
  14. DINGER B., FIDONE, S. J. & STENSAAS L. J. (1985) Regeneration of taste buds by nongustatory nerve fibers. Experimental Neurology 89, 189–203.CrossRefPubMedGoogle Scholar
  15. EL-SHARABY, A., UEDA, K. & WAKISADA, S. (2004) Immumohistochemical distribution of growth-associated protein 43 (GAP-43) in developing rat nasoincisor papilla. Anatomical Record, 277(A), 370–83.Google Scholar
  16. ERNFORS, P., LEE, K.-F., KUCERA, J. & JAENISCH, R. (1994) Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioception. Cell 77, 503–512.CrossRefPubMedGoogle Scholar
  17. FAN, L., GIRNIUS, S. & OAKLEY, B. (2004) Support of trigeminal sensory neurons by nonneuronal p75 neurotrophin receptors. Developmental Brain Research 150, 23–39.CrossRefPubMedGoogle Scholar
  18. FARBMAN, A. I. (1980) Renewal of taste bud cells in rat circumvallate papillae. Cell and Tissue Kinetics 13, 349–357.PubMedGoogle Scholar
  19. FARBMAN, A. I. (2003) Neurotrophins and taste buds.The Journal of Comparative Neurology 459, 9–14.CrossRefPubMedGoogle Scholar
  20. FARBMAN, A. I. & MBIENE, J. P. (1991). Early development and innervation of taste bud-bearing papillae on the rat tongue. The Journal of Comparative Neurology 304, 172–186.CrossRefPubMedGoogle Scholar
  21. FARIÑAS, I., JONES, K. R., BACKUS, C., WANG, X. & REICHARDT, L. F. (1994) Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369, 658–661.CrossRefPubMedGoogle Scholar
  22. FRITZSCH, B., SARAL, P. A., BARBACID, M. & SILOSSANTIAGO, I. (1997) Mice with a targeted disruption of the neurotrophin receptor trkB lose their gustatory ganglion cells early but do develop taste buds. International Journal of Developmental Neuroscience. 15, 563– 576.CrossRefPubMedGoogle Scholar
  23. GANCHROW, J. R. (2000) Taste cell function: Structural and biochemical implications. Physiology and Behavior 69, 29–40.PubMedGoogle Scholar
  24. GANCHROW, J. R. & GANCHROW, D. (1989) Long-term effects of gustatory neurectomy on fungiform papillae in the young rat. Anatomical Record 225, 224–231.CrossRefPubMedGoogle Scholar
  25. GANCHROW, D. GANCHROW, J. R., VERDIN-ALCAZAR, M. & WHITEHEAD, M. C. (2003) Brain-derived neurotrophic factor-, neurotrophin-3-, and tryrosine kinase receptor-like immunoreactivity in lingual taste bud fields of mature hamster after sensory denervation. The Journal of Comparative Neurology 455, 25–39.PubMedGoogle Scholar
  26. GILBERTSON, T. A. & BOUGHTER, J. D. Jr. (2003) Taste transduction: Appetizing times in gustation. Neuroreport 14, 905–911.PubMedGoogle Scholar
  27. HALL, J. M., BELL, M. L. & FINGER, T. E. (2003) Disruption of sonic hedgehog signaling alters growth and patterning of lingual taste papillae. Developmental Biology 255, 263–77.CrossRefPubMedGoogle Scholar
  28. HALL, J. M., HOOPER, J. E. & FINGER, T. E. (1999). Expression of sonic hedgehog patched, and Gli1 in developing taste papillae of the mouse. The Journal of Comparative Neurology 406, 143–155.CrossRefPubMedGoogle Scholar
  29. HÅRD AF SEGERSTAD, C., HELLEKANT, G. & FARBMAN, A.I. (1989) Changes in number and morphology of fungiform taste buds in rat after transection of the chorda tympani or chorda-lingual nerve. Chemical Senses 14, 335–348.Google Scholar
  30. HOSLEY, M. A., HUGHES, S. E. & OAKLEY, B. (1987a) Neural induction of taste buds. The Journal of Comparative Neurology 260, 224–232.CrossRefGoogle Scholar
  31. HOSLEY, M. A., HUGHES, S. E., MORTON, L. L. & OAKLEY, B. (1987b) A sensitive period for the neural induction of taste buds. Journal of Neuroscience 7, 2075–2080.Google Scholar
  32. HOSLEY, M.A. & OAKLEY, B. (1987) Postnatal development of the vallate papilla and taste buds in rats. Anatomical Record 218, 216–222.CrossRefPubMedGoogle Scholar
  33. JUNG, H. S., OROPEZA, V. & THESLEFF, I. (1999) Shh, Bmp-2, Bmp-4 and Fgf-8 are associated with initiation and patterning of mouse tongue papillae. Mechanisms of Development 81, 179–182.CrossRefPubMedGoogle Scholar
  34. KIM, U.-K., BRESLIN, P. A. S., REED, D. & DRAYNA, D. (2004) Genetics of human taste perception. Journal of Dental Research 83, 448–453.PubMedGoogle Scholar
  35. KIM, J. Y., MOCHIZUKI, T., AKITA, K. & JUNG, H. S. (2003) Morphological evidence of the importance of epithelial tissue during mouse tongue development. Experimental Cell Research 290, 217–226.CrossRefPubMedGoogle Scholar
  36. KNAPP, L., LAWTON, A., OAKLEY, B., WONG, L. & ZHANG, C. (1995) Keratins as markers of differentiated taste cells. Differentiation 58, 341–349.CrossRefPubMedGoogle Scholar
  37. KRIMM, R. F., MILLER, K. K., KITZMAN, P. H., DAVIS, B. M. & ALBERS, K. M. (2001) Epithelial overexpression of BDNF or NT4 disrupts targeting of taste neurons that innervate the anterior tongue. Developmental Biology 232, 508–21.CrossRefPubMedGoogle Scholar
  38. KUSAKABE, Y., MIURA, H., HASHIMOTO, R., SUGIYAMA, C. NONOMIYA, Y. & HINO, A. (2002) The neural differentiation gene mash-1 has a distinct pattern of expression from the taste reception-related genes gustducin and T1R2 in the taste buds. Chemical Senses 27, 445–51.CrossRefPubMedGoogle Scholar
  39. LANE, E. B., BARTEK, J., PURKIS, P. E. & LEIGH, I. M. (1985) Keratin antigens in differentiating skin. Annuals of the New York Academy of Sciences 455, 241–258.Google Scholar
  40. LEE, K. F., KI, E., HUMBER, L. J., LANDIS, S. C., SHARPE, A. H., CHAO, M. V. & JAENISCH, R. (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system, Cell 69, 737–749.CrossRefPubMedGoogle Scholar
  41. LIEBL, D. H., MBIENE, J. P. & PARADA, L. F. (1999) NT4/5 mutant mice have deficiency in gustatory papillae and taste bud formation. Developmental Biology 213, 378–389.CrossRefPubMedGoogle Scholar
  42. LIEBL, D.H., TESSAROLLO, L., PALKO, M. E. & PARADA, L. F. (1997) Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. The Journal of Neuroscience 17, 9113–9121.PubMedGoogle Scholar
  43. LIU, X., ERNFORS, P., WU, H. & JAENISCH, R. (1995). Sensory but not motor neuron deficits in mice lacking NT4 and BDNF. Nature 375, 238–241.PubMedGoogle Scholar
  44. MBIENE, J. P., MACCALLUM, D. & MISTRETTA, C. M. (1997) Organ cultures of embryonic rat tongue support tongue and gustatory papillae morphogenesis in vitro without intact sensory ganglia. The Journal of Comparative Neurology 377, 324–340.CrossRefPubMedGoogle Scholar
  45. MBIENE, J.-P. & ROBERTS, J. D. (2003) Distribution of keratin 8-containing cell clusters in mouse embryonic tongue: Evidence for a prepattern for taste bud development. The Journal of Comparative Neurology 457, 111–22.CrossRefPubMedGoogle Scholar
  46. MCGOWAN, K. M. & COULOMBRE, P. A. Onset of keratin 17 expression coincides wit the definition of major epithelial cell lineages during skin development. The Journal of Cell Biology 143, 469–486.Google Scholar
  47. MCLAUGHLIN, S. K. (2000). Erb and c-Kit receptors have distinctive patterns of expression in adult and developing taste papillae and taste buds. The Journal of Neuroscience 20, 5679–5688.PubMedGoogle Scholar
  48. MISTRETTA, C. M., GOOSENS, K. A., FARIÑAS, I. & REICHARDT, L. F. (1999) Alterations in size, number and morphology of gustatory papillae and taste buds in BDNF null mutant mice demonstrate neural dependence of developing taste organs. The Journal of Comparative Neurology 409, 13–24.CrossRefPubMedGoogle Scholar
  49. MISTRETTA, C. M., LIU, H.-X., GAFFIELD, W. & MACCALLUM, D. K. (2003) Cyclopamin and jervine in embryonic rat tongue cultures demonstrate a role for Shh signaling in taste papilla development and patterning: Fungiform papillae double in number and form in novel locations in dorsal lingual epithelium. Developmental Biology 254, 1–18.CrossRefPubMedGoogle Scholar
  50. MIURA, H., KATO, H., KUSAKABE, Y., TAGAMI, M., MIURA-OHNUMA, J., NINOMIYA, Y. & HINO, A. (2004). A Strong Nerve Dependence of Sonic hedgehog Expression in Basal Cells in Mouse Taste Bud and an Autonomous Transcriptional Control of Genes in Differentiated Taste Cells. Chemical Senses 29, 823– 31.CrossRefPubMedGoogle Scholar
  51. MIURA, H., KUSAKABE, Y., SUGIYAMA, C., KAWAMATSU, M., NINOMIYA, Y., MOTOYAMA, J. & HINO, A. (2001). Shh and ptc are associated with taste bud maintenance in the adult mouse. Mechanisms of Development 106, 143–45.CrossRefPubMedGoogle Scholar
  52. MONTAVON, P., HELLEKANT, G. & FARBMAN, A. (1996) Immunohistochemical, electrophysiological, and electron microscopical study of rat fungiform taste buds after regeneration of chorda tympani through the non-gustatory lingual nerve. The Journal of Comparative. Neurology. 367, 491–502.CrossRefPubMedGoogle Scholar
  53. MONTAVON, P. & LINDSTRAND, K. (1991) Immunocytochemical localization of neuron-specific enolase and calcitonin gene-related peptide in rat taste papillae. Regulatory Peptides 36, 219–233.PubMedGoogle Scholar
  54. MONTMAYEUR, J. P. & MATSUNAMI, H. (2002) Receptors for bitter and sweet taste. Current Opinion in Neurobiology 12, 366–371.CrossRefPubMedGoogle Scholar
  55. MORASSO, J. I., MAHON, K. A. & SARGENT, T. D. (1995). A Xenopus distal-less gene in transgenic mice: Conserved regulation in distal limb epidermis and other sites of epithelial-mesenchymal interaction. Proceedings of the National Academy of Science USA 92, 3968–3972.Google Scholar
  56. MORRIS-WIMAN, J., BASCO, E. & DU, Y. (1999). The effects of ß-Bungarotoxin on the morphogenesis of taste papillae and taste buds in the mouse. Chemical Senses 24, 7–17.CrossRefPubMedGoogle Scholar
  57. NAGATO, T., MATSUMOTO, K., TANIOKA, H., KODAMA, J. & TOH, H. (1995). Effect of denervation on morphogenesis of the rat fungiform papilla. Acta Anatomica 153, 301–309.PubMedGoogle Scholar
  58. NINOMIYA, Y. (1998) Reinnervation of cross-regenerated gustatory nerve fibers into amiloride-sensitive and amiloride-insenstive taste receptor cells. Proceedings of the National Academy of Science USA 95, 5347–5350.Google Scholar
  59. NORTHCUTT, R. G. (2004) Taste buds: Development and evolution. Brain Behavior and Evolution 64, 198–206.Google Scholar
  60. NORTHCUTT, R. G. & BARLOW, L. A. (1998) Amphibians provide new insights into taste-bud development. Trends in Neuroscience 21, 38–43.CrossRefGoogle Scholar
  61. NOSRAT, I. V., AGERMAN, K., ERNFORS, P. & NOSRAT, C. A. (2005) Combinatorial gustatory and somatosensory deficits in neurotrophin double knockout mice. Journal of Neurocytology, XXXGoogle Scholar
  62. NOSRAT, C. A., BLOMLOF, J., ELSHAMY, W. M., ERNFORS, P. & OLSON, L. (1997) Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively. Development 124, 1333–1342.PubMedGoogle Scholar
  63. NOSRAT, C. A., EBENDAL, L. & OLSON, L. (1996). Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mRNA in lingual papillae and taste buds indicates roles of gustatory and somatosensory innervation. The Journal of Comparative Neurology 376, 587–602.CrossRefPubMedGoogle Scholar
  64. NOSRAT, I. V., LINDSKOG, S., SEIGER A. & NOSRAT, C. A. (2000) Lingual BDNF and NT-3 mRNA expression patterns and their relation to innervation in the human tongue: Similarities and differences compared with rodents. The Journal of Comparative Neurology 417, 133–152.CrossRefPubMedGoogle Scholar
  65. NOSRAT, C. A., MACCALLUM, D. K. & MISTRETTA, C. M. (2001) Distinctive spatiotemporal expression patterns for neurotrophins develop in gustatory papillae and lingual tissues in embryonic tongue organ cultures. Cell and Tissue Research 303, 35–45.CrossRefPubMedGoogle Scholar
  66. NOSRAT, C. A. & OLSON, L. (1995) Brain-derived neurotrophic factor mRNA is expressed in the developing taste bud-bearing tongue papillae of rat. The Journal of Comparative Neurology 360, 698–704.CrossRefPubMedGoogle Scholar
  67. OAKLEY, B. (1967) Altered temperature and taste responses from cross-regenerated sensory nerves in the rat's tongue. Journal of Physiology 188, 353–371.PubMedGoogle Scholar
  68. OAKLEY, B. (1975) Receptive fields of cat taste fibers. Chemical Senses and Flavor 1, 431–442.Google Scholar
  69. OAKLEY, B. (1993a) Control mechanisms in taste bud development. In: Mechanisms of Taste Transduction (S.A. Simon and S.D. Roper, eds) CRC Press, Boca Raton, FL., pp. 105–125.Google Scholar
  70. OAKLEY, B. (1993b) The gustatory competence of the lingual epithelium requires neonatal innervation. Developmental Brain Research 72, 259–264.CrossRefGoogle Scholar
  71. OAKLEY, B. (1998) Taste neurons have multiple inductive roles in mammalian gustatory development. Annals of the New York Academy of Sciences 855, 50–57.PubMedGoogle Scholar
  72. OAKLEY, B. & BENJAMIN, R. M. (1966) Neural mechanisms of taste. Physiological Reviews 46, 173–211.PubMedGoogle Scholar
  73. OAKLEY, B., BRANDEMIHL, A., COOPER, D., LAU, D., LAWTON, A. & ZHANG, C. (1998) The morphogenesis of mouse vallate gustatory epithelium and taste buds requires BDNF-dependent taste neurons. Developmental Brain Research 105, 85–96.CrossRefGoogle Scholar
  74. OAKLEY, B, LABELLE, D. E., RILEY, R. A., WILSON, K. & LI, L.W. (1991) The rate and locus of development of rat vallate taste buds. Developmental Brain Research 58, 215–221.CrossRefPubMedGoogle Scholar
  75. OAKLEY, B., LAWTON, A., RIDDLE, D. R. & WU, L. H. (1993) Morphometric and immunocytochemical assessment of fungiform taste buds after interruption of the chorda-lingual nerve. Microscopy and Research Techniques 26, 187–195.Google Scholar
  76. OAKLEY, B., WU, L. H., LAWTON, A. & DESIBOUR, C. L. (1990) Neural control of ectopic filiform spines in adult tongue. Neuroscience 36, 831–838.CrossRefPubMedGoogle Scholar
  77. REUTTER, K. & WITT, M. (1993) Morphology of vertebrate taste organs and their nerve supply, In: Mechanisms of Taste Transduction (SIMON, S.A. & ROPER, S.D., eds.) CRC Press, Boca Raton, FL., pp. 29–81.Google Scholar
  78. RINGSTEDT, T., IBANEZ, C. F. & NOSRAT, C. A. (1999) Role of brain-derived neurotrophic factor in target invasion in the gustatory system. The Journal of Neuroscience 19, 3507–3518.PubMedGoogle Scholar
  79. RIDDLE, D. R., HUGHES, S. E. & OAKLEY, B. (1987) Some effects upon fungiform and foliate taste buds of condensing the innervation by the chorda tympani nerve. Chemical Senses, 12, 691.Google Scholar
  80. ROPER, S. (1983) Regenerative impulses in taste cells. Science, 220, 1311–1312PubMedGoogle Scholar
  81. SAWAF, M. H., OUHAYOUN, J. P. & FOREST, N. (1991) Cytokeratin profiles in oral epithelia: A review and a new classification. Journal of Biologie Buccale 19, 187–198.Google Scholar
  82. SETA, Y., TOYONO, T., TAKEDA, S. & TOYOSHIMA, K. (1999) Expression of Mash1 in basal cells of rat circumvallate taste buds is dependent upon gustatory innervation. Federation of Experimental Biology Societies Letters 444, 43–46.Google Scholar
  83. SHULER, M. G., KRIMM, R. F. & HILL, D. L. (2004) Neuron/target plasticity in the peripheral gustatory system. The Journal of Comparative Neurology 472, 183–92.CrossRefPubMedGoogle Scholar
  84. SLOAN, H. E., HUGHES, S. E. & OAKLEY, B. (1983) Chronic impairment of axonal transport eliminates taste responses and taste buds. The Journal of Neuroscience 3, 117–123.PubMedGoogle Scholar
  85. STONE, L. S. (1933) Independence of taste organs with respect to their nerve fibers demonstrated in living salamanders. Proceedings of the Society for Experimental Biology and Medicine 30, 1256–1257.Google Scholar
  86. STONE, L. S. (1940) The origin and development of taste organs in salamanders observed in the living condition. Journal of Experimental Zoology 83, 481– 506.Google Scholar
  87. SUN, H. & OAKLEY, B. (2002) Development of anterior gustatory epithelial in the palate and tongue requires epidermal growth factor receptor, Developmental Biology 242, 31–43.CrossRefPubMedGoogle Scholar
  88. SUZUKI, Y., TAKEDA, M. & OBARA, N. (2002) Expression of Neuro D in the mouse taste buds. Cell and Tissue Research 307, 423–428.PubMedGoogle Scholar
  89. TAKAISHI, M., TAKATA, Y., KUROKI, T. & HUH, N. (1998). Isolation and characterization of a putative keratin-associated protein gene expressed in embryonic skin of mice. Journal of Investigative Dermatology 111, 128–32.CrossRefPubMedGoogle Scholar
  90. TAKEDA, M. (1979) Tritiated thymidine autoradiographic study of taste buds in the mouse. Acta Anatomica Nippon 54, 230–231.Google Scholar
  91. TAKEDA, M., SUZUKI, Y., OBARA, N. & NAGAI, Y. (1992) Neural Cell adhesion molecule of taste buds. Journal of Electron Microscopy 41, 375–80.PubMedGoogle Scholar
  92. TOYOSHIMA, K., SETA, Y., TOYONO, T. & TAKEDA, S. (1999) Merkel cells are responsible for the initiation of taste organ morphogenesis in the frog. Journal of Comparative Neurology 406, 129–40.CrossRefPubMedGoogle Scholar
  93. TYLER, M., DANILOV, Y. & BACH-Y-RITA, P. (2003) Closing an open-loop control system: Vestibular substitution through the tongue. Journal of Integrative Neuroscience 2, 159–64.CrossRefPubMedGoogle Scholar
  94. UCHIDA, N., KANAZAWA, M., SUZUKI, Y. & TAKEDA, M. (2003) Expression of BDNF and TrkB in mouse taste buds after denervation and in circumvallate papillae during development. Archives of Histology & Cytology 66, 17–25.Google Scholar
  95. VINTSCHGAU VON, M.V. & HÖNIGSCHMIED, J. (1877) Nervus Glossopharyngeus und Schmeckbecher Archiv der Gesamten Physiologie 14, 443–448.Google Scholar
  96. WHITEHEAD, M. C., FRANK, M. E., HETTINGER, T. P., HOU, L. T. & NAH, H. D. (1985). Persistence of taste buds in denervated fungiform papillae. Brain Research 405, 192–195.Google Scholar
  97. WHITEHEAD, M. C., GANCHROW, J. P., GANCHROW, D. & YAO, B. (1998) Neural cell adhesion molecule, neuron-specific enolase and calcitonin gene-related peptide immunoreactivity in hamster taste buds after chorda tympani/lingual nerve denervation. Neuroscience 83, 843–56.CrossRefPubMedGoogle Scholar
  98. WHITEHEAD, M. C. & KACHELE, D. L. (1994) Development of fungiform papillae, taste buds, and their innervation in the hamster. The Journal of Comparative Neurology 340, 515–530.CrossRefPubMedGoogle Scholar
  99. WITT, M. & KASPER, M. (1998) Immunohistochemical distribution of CD44 and some of its isoforms during human taste bud development. Histochemistry and Cell Biology 110, 95–103.CrossRefPubMedGoogle Scholar
  100. WITT, M. & KASPER, M. (1999) Distribution of cytokeratin filaments and vimentin in developing human taste buds Anatomy and Embryology 199, 291–99.CrossRefPubMedGoogle Scholar
  101. WITT, M. & REUTTER, K. (1996) Embryonic and early fetal development of human taste buds: A transmission electron microscopical study Anatomical Record 246, 507– 23.CrossRefPubMedGoogle Scholar
  102. WITT, M. & REUTTER, K. (1998) Innervation of developing human taste buds. An immunohistochemical study. Histochemistry and Cell Biology 109, 281–91.CrossRefPubMedGoogle Scholar
  103. WITT, M., REUTTER, K. GANCHROW, D. & GANCHROW, J. R. (2000) Fingerprinting taste buds: Intermediate filaments and their implications for taste bud formation. Philosophical Transactions of the Royal Society of London B. 355, 1233–37.Google Scholar
  104. WITT, M., REUTTER, K. & MILLER, I.J. JR (2003) Morphology of the Peripheral Taste System. In: Handbook of Olfaction and Gustation (ed. DOTY, R.L.), Marcel Dekker, Inc., New York, Basel, pp 651–677Google Scholar
  105. WRIGHT, M. R. (1964) Taste organs in tongue-to-liver grafts in the newt, Triturus v. viridescens. Journal of Experimental Zoology 156, 377–389.CrossRefPubMedGoogle Scholar
  106. YASUMATSU, K., KATSUKAWA, H., SASAMOTO, K. & NINOMIYA, Y. (2003) Recovery of amiloride-sensitive neural coding during regeneration of the gustatory nerve: Behavioral-neural correlation of salt taste discrimination. The Journal of Neuroscience 23, 4362–4368.PubMedGoogle Scholar
  107. YEE, C. L., JONES, K. R. & FINGER, T. E. (2003) Brain-derived neurotrophic factor is present in adult mouse taste cells with synapses. The Journal of Comparative Neurology 459 15–24.CrossRefPubMedGoogle Scholar
  108. ZALEWSKI, A. A. (1972) Regeneration of taste buds after transplantation of tongue and ganglia grafts to the anterior chamber of the eye. Experimental Neurology 35, 519–528.CrossRefPubMedGoogle Scholar
  109. ZELENA, J. (1994) Nerves and mechanoreceptors: The role of innervation in the development and maintenance of mammalian mechanoreceptors, Chapman & Hall, London.Google Scholar
  110. ZENG, Q., KWAN, A. & OAKLEY, B. (2000) Gustatory innervation and Bax-dependent Caspase-2: Participants in the life and death pathways of mouse taste receptors cells. The Journal of Comparative Neurology 424, 640–650.CrossRefPubMedGoogle Scholar
  111. ZENG, Q. & OAKLEY, B. (1999) p53 and Bax: Putative death factors in taste cell turnover, Journal of Comparative Neurology. 413, 168–180.CrossRefPubMedGoogle Scholar
  112. ZHANG, C., COTTER, M., LAWTON, A., OAKLEY, B., WONG, L. & ZENG, Q. (1995) Keratin 18 is associated with a subset of older taste cells in the rat. Differentiation 59, 155–162.CrossRefPubMedGoogle Scholar
  113. ZHANG, C. & OAKLEY, B. (1996) The distribution and origin of keratin 20-containing taste buds in rat and human. Differentiation 61, 121–128.CrossRefPubMedGoogle Scholar
  114. ZHANG, C., BRANDEMIHL, A., LAU, D., LAWTON, A. & OAKLEY, B. (1997) BDNF is required for the normal development of taste neurons in vivo. Neuroreport 8, 1013–1017.PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Department of Molecular, Cellular, and Developmental BiologyUniversity of MichiganAnn Arbor
  2. 2.Department of AnatomyUniversity of Technology Dresden, and Center for Smell and Taste, Medical SchoolDresdenGermany

Personalised recommendations