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The coding of valence and identity in the mammalian taste system

Author

Listed:
  • Li Wang

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Columbia College of Physicians and Surgeons, Columbia University)

  • Sarah Gillis-Smith

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Columbia College of Physicians and Surgeons, Columbia University)

  • Yueqing Peng

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Columbia College of Physicians and Surgeons, Columbia University)

  • Juen Zhang

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Columbia College of Physicians and Surgeons, Columbia University)

  • Xiaoke Chen

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Stanford University)

  • C. Daniel Salzman

    (Columbia College of Physicians and Surgeons, Columbia University
    Columbia University)

  • Nicholas J. P. Ryba

    (National Institutes of Health)

  • Charles S. Zuker

    (Columbia University
    Columbia College of Physicians and Surgeons, Columbia University
    Columbia College of Physicians and Surgeons, Columbia University)

Abstract

The ability of the taste system to identify a tastant (what it tastes like) enables animals to recognize and discriminate between the different basic taste qualities1,2. The valence of a tastant (whether it is appetitive or aversive) specifies its hedonic value and elicits the execution of selective behaviours. Here we examine how sweet and bitter are afforded valence versus identity in mice. We show that neurons in the sweet-responsive and bitter-responsive cortex project to topographically distinct areas of the amygdala, with strong segregation of neural projections conveying appetitive versus aversive taste signals. By manipulating selective taste inputs to the amygdala, we show that it is possible to impose positive or negative valence on a neutral water stimulus, and even to reverse the hedonic value of a sweet or bitter tastant. Remarkably, mice with silenced neurons in the amygdala no longer exhibit behaviour that reflects the valence associated with direct stimulation of the taste cortex, or with delivery of sweet and bitter chemicals. Nonetheless, these mice can still identify and discriminate between tastants, just as wild-type controls do. These results help to explain how the taste system generates stereotypic and predetermined attractive and aversive taste behaviours, and support the existence of distinct neural substrates for the discrimination of taste identity and the assignment of valence.

Suggested Citation

  • Li Wang & Sarah Gillis-Smith & Yueqing Peng & Juen Zhang & Xiaoke Chen & C. Daniel Salzman & Nicholas J. P. Ryba & Charles S. Zuker, 2018. "The coding of valence and identity in the mammalian taste system," Nature, Nature, vol. 558(7708), pages 127-131, June.
  • Handle: RePEc:nat:nature:v:558:y:2018:i:7708:d:10.1038_s41586-018-0165-4
    DOI: 10.1038/s41586-018-0165-4
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    Cited by:

    1. Lun Wang & Min Gao & Qinglong Wang & Liyuan Sun & Muhammad Younus & Sixing Ma & Can Liu & Li Shi & Yang Lu & Bo Zhou & Suhua Sun & Guoqing Chen & Jie Li & Quanfeng Zhang & Feipeng Zhu & Changhe Wang &, 2023. "Cocaine induces locomotor sensitization through a dopamine-dependent VTA-mPFC-FrA cortico-cortical pathway in male mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Yu, Junwei & Droulers, Olivier & Lacoste-Badie, Sophie, 2022. "Why display motion on packaging? The effect of implied motion on consumer behavior," Journal of Retailing and Consumer Services, Elsevier, vol. 64(C).
    3. C. Nicolas & A. Ju & Y. Wu & H. Eldirdiri & S. Delcasso & Y. Couderc & C. Fornari & A. Mitra & L. Supiot & A. Vérité & M. Masson & S. Rodriguez-Rozada & D. Jacky & J. S. Wiegert & A. Beyeler, 2023. "Linking emotional valence and anxiety in a mouse insula-amygdala circuit," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. repec:hal:journl:hal-03512772 is not listed on IDEAS
    5. Chi Chen & Dilja Krueger-Burg & Livia de Hoz, 2019. "Wide sensory filters underlie performance in memory-based discrimination and generalization," PLOS ONE, Public Library of Science, vol. 14(4), pages 1-29, April.
    6. Romane Cecchi & Antoine Collomb-Clerc & Inès Rachidi & Lorella Minotti & Philippe Kahane & Mathias Pessiglione & Julien Bastin, 2024. "Direct stimulation of anterior insula and ventromedial prefrontal cortex disrupts economic choices," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Qi Wang & Jia-Jie Zhu & Lizhao Wang & Yan-Peng Kan & Yan-Mei Liu & Yan-Jiao Wu & Xue Gu & Xin Yi & Ze-Jie Lin & Qin Wang & Jian-Fei Lu & Qin Jiang & Ying Li & Ming-Gang Liu & Nan-Jie Xu & Michael X. Z, 2022. "Insular cortical circuits as an executive gateway to decipher threat or extinction memory via distinct subcortical pathways," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Yihan Wang & Qian-Quan Sun, 2024. "A prefrontal motor circuit initiates persistent movement," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Li Shen & Guang-Wei Zhang & Can Tao & Michelle B. Seo & Nicole K. Zhang & Junxiang J. Huang & Li I. Zhang & Huizhong W. Tao, 2022. "A bottom-up reward pathway mediated by somatostatin neurons in the medial septum complex underlying appetitive learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Sasa Teng & Fenghua Zhen & Li Wang & Jose Canovas Schalchli & Jane Simko & Xinyue Chen & Hao Jin & Christopher D. Makinson & Yueqing Peng, 2022. "Control of non-REM sleep by ventrolateral medulla glutamatergic neurons projecting to the preoptic area," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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