Letter | Published:

Sweet and bitter taste in the brain of awake behaving animals

Nature volume 527, pages 512515 (26 November 2015) | Download Citation

Abstract

Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals1. In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain2. Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map3,4, with each taste quality encoded by distinct cortical fields4. Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal’s internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input.

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References

  1. 1.

    Receptors and transduction in taste. Nature 413, 219–225 (2001)

  2. 2.

    Taste responses of cortical neurons. Prog. Neurobiol. 23, 273–315 (1984)

  3. 3.

    , , & Differential spatial representation of taste modalities in the rat gustatory cortex. J. Neurosci. 27, 1396–1404 (2007)

  4. 4.

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

  5. 5.

    , , , & Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263–1268 (2005)

  6. 6.

    et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212–217 (2012)

  7. 7.

    in Drinking Behavior (eds & ) 1–92 (Springer, 1977)

  8. 8.

    et al. Procedures for behavioral experiments in head-fixed mice. PLoS ONE 9, e88678 (2014)

  9. 9.

    & The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res. 143, 263–279 (1978)

  10. 10.

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

  11. 11.

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

  12. 12.

    & Gustatory thalamus lesions in the rat: I. Innate taste preferences and aversions. Behav. Neurosci. 110, 737–745 (1996)

  13. 13.

    & Encoding and tracking of outcome-specific expectancy in the gustatory cortex of alert rats. J. Neurosci. 34, 13000–13017 (2014)

  14. 14.

    , & Temporal signatures of taste quality driven by active sensing. J. Neurosci. 34, 7398–7411 (2014)

  15. 15.

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

  16. 16.

    et al. Mammalian sweet taste receptors. Cell 106, 381–390 (2001)

  17. 17.

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

  18. 18.

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

  19. 19.

    , , , & Neural correlates of variations in event processing during learning in central nucleus of amygdala. Neuron 68, 991–1001 (2010)

  20. 20.

    et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471, 358–362 (2011)

  21. 21.

    et al. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39, 701–711 (2003)

  22. 22.

    & The representation of taste quality in the mammalian nervous system. Behav. Cogn. Neurosci. Rev. 4, 143–191 (2005)

  23. 23.

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

  24. 24.

    et al. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677–1681 (2010)

  25. 25.

    et al. Driving opposing behaviors with ensembles of piriform neurons. Cell 146, 1004–1015 (2011)

  26. 26.

    , , & Deconstruction of a neural circuit for hunger. Nature 488, 172–177 (2012)

  27. 27.

    et al. Decoding neural circuits that control compulsive sucrose seeking. Cell 160, 528–541 (2015)

  28. 28.

    , & Activation of lateral hypothalamus-projecting parabrachial neurons by intraorally delivered gustatory stimuli. Front. Neural Circuits 8, 86 (2014)

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Acknowledgements

We particularly thank H. Fischman and R. Lessard for suggestions, and members of the Zuker laboratory for comments. We also thank D. Salzman, K. Scott, and R. Axel for discussions. This research was supported in part by a grant from the National Institute of Drug Abuse (DA035025) to C.S.Z., and the Intramural Research Program of the National Institutes of Health, National Institute of Dental and Craniofacial Research (to N.J.P.R.). C.S.Z. is an investigator of the Howard Hughes Medical Institute and a Senior Fellow at Janelia Farms Research Campus, Howard Hughes Medical Institute.

Author information

Affiliations

  1. Howard Hughes Medical Institute, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA

    • Yueqing Peng
    • , Sarah Gillis-Smith
    • , Hao Jin
    • , Dimitri Tränkner
    •  & Charles S. Zuker
  2. Departments of Biochemistry and Molecular Biophysics, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA

    • Yueqing Peng
    • , Sarah Gillis-Smith
    • , Hao Jin
    • , Dimitri Tränkner
    •  & Charles S. Zuker
  3. Department of Neuroscience, Columbia College of Physicians and Surgeons, Columbia University, New York, New York 10032, USA

    • Yueqing Peng
    • , Sarah Gillis-Smith
    • , Hao Jin
    • , Dimitri Tränkner
    •  & Charles S. Zuker
  4. HHMI/Janelia Farm Research Campus, 19700 Helix Drive, Ashburn, Virginia 20147, USA

    • Dimitri Tränkner
    •  & Charles S. Zuker
  5. National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland 20892, USA

    • Nicholas J. P. Ryba

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Contributions

Y.P. designed the study, performed experiments, and analysed data; S.G.-S. performed animals studies, viral injections, histology and analysed data; H.J. performed c-Fos expression studies; D.T. developed the initial behavioural platforms; N.J.P.R. and C.S.Z. designed the study, analysed data, and together with Y.P. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Table

    This file contains Supplementary Table 1, coordinates of the injection and cannulation sites.

Videos

  1. 1.

    Behavioural responses to bitter cortex stimulation.

    A mouse expressing ChR2-YFP in the bitter cortex before and after photostimulation. First trial, control experiment with the animal robustly drinking water (yellow circle indicates trial-initiation). Second trial shows prototypical orofacial responses (normally triggered by oral presentation of bitter tastants), now elicited by direct stimulation of bitter cortex (5-10 mW). Third trial shows gaping responses, and attempts to clean the mouth of the "fictive" bitter taste following strong stimulation (10-20 mW); note that the animal does not even sample the water drop; under these stimulating conditions 30% of the animals exhibit gagging behaviour. Stimulation of sweet cortex never induced such behaviour.

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DOI

https://doi.org/10.1038/nature15763

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