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The neural representation of taste quality at the periphery

Nature volume 517, pages 373376 (15 January 2015) | Download Citation



The mammalian taste system is responsible for sensing and responding to the five basic taste qualities: sweet, sour, bitter, salty and umami. Previously, we showed that each taste is detected by dedicated taste receptor cells (TRCs) on the tongue and palate epithelium1. To understand how TRCs transmit information to higher neural centres, we examined the tuning properties of large ensembles of neurons in the first neural station of the gustatory system. Here, we generated and characterized a collection of transgenic mice expressing a genetically encoded calcium indicator2 in central and peripheral neurons, and used a gradient refractive index microendoscope3 combined with high-resolution two-photon microscopy to image taste responses from ganglion neurons buried deep at the base of the brain. Our results reveal fine selectivity in the taste preference of ganglion neurons; demonstrate a strong match between TRCs in the tongue and the principal neural afferents relaying taste information to the brain; and expose the highly specific transfer of taste information between taste cells and the central nervous system.

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  1. 1.

    , & Common sense about taste: from mammals to insects. Cell 139, 234–244 (2009)

  2. 2.

    et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6, 875–881 (2009)

  3. 3.

    , , , & In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. J. Neurophysiol. 92, 3121–3133 (2004)

  4. 4.

    , , & The neural mechanisms of gustation: a distributed processing code. Nature Rev. Neurosci. 7, 890–901 (2006)

  5. 5.

    et al. The cells and peripheral representation of sodium taste in mice. Nature 464, 297–301 (2010)

  6. 6.

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

  7. 7.

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

  8. 8.

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

  9. 9.

    & The cell biology of taste. J. Cell Biol. 190, 285–296 (2010)

  10. 10.

    & Taste nerve fibers: a random distribution of sensitivities to four tastes. Science 164, 1183–1185 (1969)

  11. 11.

    et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51 (2000)

  12. 12.

    et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32, 13819–13840 (2012)

  13. 13.

    et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013)

  14. 14.

    et al. Human receptors for sweet and umami taste. Proc. Natl Acad. Sci. USA 99, 4692–4696 (2002)

  15. 15.

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

  16. 16.

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

  17. 17.

    , , , & High salt recruits aversive taste pathways. Nature 494, 472–475 (2013)

  18. 18.

    , , , & Breadth of tuning and taste coding in mammalian taste buds. J. Neurosci. 27, 10840–10848 (2007)

  19. 19.

    et al. The effect of pH on β2 adrenoceptor function. Evidence for protonation-dependent activation. J. Biol. Chem. 275, 3121–3127 (2000)

  20. 20.

    , , & Monosodium glutamate and sweet taste: generalization of conditioned taste aversion between glutamate and sweet stimuli in rats. Chem. Senses 28, 631–641 (2003)

  21. 21.

    , , , & A gustotopic map of taste qualities in the mammalian brain. Science 333, 1262–1266 (2011)

  22. 22.

    & Renewal of cells within taste buds. J. Cell Biol. 27, 263–272 (1965)

  23. 23.

    & The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res. 143, 281–297 (1978)

  24. 24.

    & Discrete innervation of murine taste buds by peripheral taste neurons. J. Neurosci. 26, 8243–8253 (2006)

  25. 25.

    et al. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nature Med. 17, 223–228 (2011)

  26. 26.

    & In vivo recordings from rat geniculate ganglia: taste response properties of individual greater superficial petrosal and chorda tympani neurones. J. Physiol. (Lond.) 564, 877–893 (2005)

  27. 27.

    , & A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27–41 (1998)

  28. 28.

    , & Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63, 747–760 (2009)

  29. 29.

    & Alternatives to the median absolute deviation. J. Am. Stat. Assoc. 88, 1273–1283 (1993)

  30. 30.

    & Effects of binary taste stimuli on the neural activity of the hamster chorda tympani. J. Gen. Physiol. 76, 125–142 (1980)

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We thank the National Institute of Dental and Craniofacial Research (NIDCR) transgenic-core and C. Guo at Janelia Farms for help in generating the Thy1-GCaMP3 mouse lines, B. Shields for histology support, and Y. Oka and M. Butnaru for nerve recording and pharmacological advice. We also thank members of the Zuker laboratory for helpful comments. This research was supported in part by the intramural research program of NIDCR (N.J.P.R.). C.S.Z. is an investigator of the Howard Hughes Medical Institute and a Senior Fellow at Janelia Farms.

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  1. Howard Hughes Medical Institute and Departments of Biochemistry and Molecular Biophysics and of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, New York 10032, USA

    • Robert P. J. Barretto
    • , Sarah Gillis-Smith
    • , David A. Yarmolinsky
    •  & Charles S. Zuker
  2. Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147, USA

    • Jayaram Chandrashekar
    •  & Charles S. Zuker
  3. James H. Clark Center, Stanford University, Stanford, California 94305, USA

    • Mark J. Schnitzer
  4. National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland 20892, USA

    • Nicholas J. P. Ryba


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R.P.J.B. designed the study, carried out the imaging experiments, analysed data and wrote the paper; S.G.-S. developed viral gene delivery to ganglion neurons and characterized the transgenic lines; J.C. characterized the transgenic lines, carried out initial imaging experiments and analysed data; D.A.Y. collected and analysed data; M.J.S. provided microendoscopy expertise; N.J.P.R. and C.S.Z. designed the study, analysed data and wrote the paper.

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The authors declare no competing financial interests.

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Correspondence to Nicholas J. P. Ryba or Charles S. Zuker.

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