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Neurons for hunger and thirst transmit a negative-valence teaching signal

Author

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  • J. Nicholas Betley

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Shengjin Xu

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Zhen Fang Huang Cao

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Rong Gong

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Christopher J. Magnus

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Yang Yu

    (Janelia Research Campus, Howard Hughes Medical Institute)

  • Scott M. Sternson

    (Janelia Research Campus, Howard Hughes Medical Institute)

Abstract

Homeostasis is a biological principle for regulation of essential physiological parameters within a set range. Behavioural responses due to deviation from homeostasis are critical for survival, but motivational processes engaged by physiological need states are incompletely understood. We examined motivational characteristics of two separate neuron populations that regulate energy and fluid homeostasis by using cell-type-specific activity manipulations in mice. We found that starvation-sensitive AGRP neurons exhibit properties consistent with a negative-valence teaching signal. Mice avoided activation of AGRP neurons, indicating that AGRP neuron activity has negative valence. AGRP neuron inhibition conditioned preference for flavours and places. Correspondingly, deep-brain calcium imaging revealed that AGRP neuron activity rapidly reduced in response to food-related cues. Complementary experiments activating thirst-promoting neurons also conditioned avoidance. Therefore, these need-sensing neurons condition preference for environmental cues associated with nutrient or water ingestion, which is learned through reduction of negative-valence signals during restoration of homeostasis.

Suggested Citation

  • J. Nicholas Betley & Shengjin Xu & Zhen Fang Huang Cao & Rong Gong & Christopher J. Magnus & Yang Yu & Scott M. Sternson, 2015. "Neurons for hunger and thirst transmit a negative-valence teaching signal," Nature, Nature, vol. 521(7551), pages 180-185, May.
  • Handle: RePEc:nat:nature:v:521:y:2015:i:7551:d:10.1038_nature14416
    DOI: 10.1038/nature14416
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    Cited by:

    1. Qin Wang & Rui-Yue Sun & Jia-Xue Hu & Yan-Hui Sun & Chun-Yue Li & Huiqian Huang & Hao Wang & Xiao-Ming Li, 2024. "Hypothalamic-hindbrain circuit for consumption-induced fear regulation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Keshav S. Subramanian & Logan Tierno Lauer & Anna M. R. Hayes & Léa Décarie-Spain & Kara McBurnett & Anna C. Nourbash & Kristen N. Donohue & Alicia E. Kao & Alexander G. Bashaw & Denis Burdakov & Emil, 2023. "Hypothalamic melanin-concentrating hormone neurons integrate food-motivated appetitive and consummatory processes in rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. In-Jee You & Yeeun Bae & Alec R. Beck & Sora Shin, 2023. "Lateral hypothalamic proenkephalin neurons drive threat-induced overeating associated with a negative emotional state," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Young Hee Lee & Yu-Been Kim & Kyu Sik Kim & Mirae Jang & Ha Young Song & Sang-Ho Jung & Dong-Soo Ha & Joon Seok Park & Jaegeon Lee & Kyung Min Kim & Deok-Hyeon Cheon & Inhyeok Baek & Min-Gi Shin & Eun, 2023. "Lateral hypothalamic leptin receptor neurons drive hunger-gated food-seeking and consummatory behaviours in male mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Yan Zhang & Jiayi Shen & Famin Xie & Zhiwei Liu & Fangfang Yin & Mingxiu Cheng & Liang Wang & Meiting Cai & Herbert Herzog & Ping Wu & Zhi Zhang & Cheng Zhan & Tiemin Liu, 2024. "Feedforward inhibition of stress by brainstem neuropeptide Y neurons," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Johanni Brea & Nicola S. Clayton & Wulfram Gerstner, 2023. "Computational models of episodic-like memory in food-caching birds," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Mireia Montaner & Jessica Denom & Vincent Simon & Wanqing Jiang & Marie K. Holt & Daniel I. Brierley & Claude Rouch & Ewout Foppen & Nadim Kassis & David Jarriault & Dawood Khan & Louise Eygret & Fran, 2024. "A neuronal circuit driven by GLP-1 in the olfactory bulb regulates insulin secretion," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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