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The neural representation of taste quality at the periphery

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

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Abstract

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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Acknowledgements

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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Affiliations

  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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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

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https://doi.org/10.1038/nature13873

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