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A neural circuit mechanism for mechanosensory feedback control of ingestion

Author

Listed:
  • Dong-Yoon Kim

    (Seoul National University
    Seoul National University)

  • Gyuryang Heo

    (Seoul National University)

  • Minyoo Kim

    (Seoul National University
    Seoul National University)

  • Hyunseo Kim

    (Seoul National University)

  • Ju Ae Jin

    (Seoul National University)

  • Hyun-Kyung Kim

    (Seoul National University
    Seoul National University)

  • Sieun Jung

    (Seoul National University
    Seoul National University)

  • Myungmo An

    (Seoul National University
    Seoul National University)

  • Benjamin H. Ahn

    (Seoul National University
    Seoul National University)

  • Jong Hwi Park

    (Seoul National University)

  • Han-Eol Park

    (Seoul National University)

  • Myungsun Lee

    (Seoul National University
    Seoul National University)

  • Jung Weon Lee

    (Seoul National University)

  • Gary J. Schwartz

    (Albert Einstein College of Medicine)

  • Sung-Yon Kim

    (Seoul National University
    Seoul National University
    Seoul National University)

Abstract

Mechanosensory feedback from the digestive tract to the brain is critical for limiting excessive food and water intake, but the underlying gut–brain communication pathways and mechanisms remain poorly understood1–12. Here we show that, in mice, neurons in the parabrachial nucleus that express the prodynorphin gene (hereafter, PBPdyn neurons) monitor the intake of both fluids and solids, using mechanosensory signals that arise from the upper digestive tract. Most individual PBPdyn neurons are activated by ingestion as well as the stimulation of the mouth and stomach, which indicates the representation of integrated sensory signals across distinct parts of the digestive tract. PBPdyn neurons are anatomically connected to the digestive periphery via cranial and spinal pathways; we show that, among these pathways, the vagus nerve conveys stomach-distension signals to PBPdyn neurons. Upon receipt of these signals, these neurons produce aversive and sustained appetite-suppressing signals, which discourages the initiation of feeding and drinking (fully recapitulating the symptoms of gastric distension) in part via signalling to the paraventricular hypothalamus. By contrast, inhibiting the same population of PBPdyn neurons induces overconsumption only if a drive for ingestion exists, which confirms that these neurons mediate negative feedback signalling. Our findings reveal a neural mechanism that underlies the mechanosensory monitoring of ingestion and negative feedback control of intake behaviours upon distension of the digestive tract.

Suggested Citation

  • Dong-Yoon Kim & Gyuryang Heo & Minyoo Kim & Hyunseo Kim & Ju Ae Jin & Hyun-Kyung Kim & Sieun Jung & Myungmo An & Benjamin H. Ahn & Jong Hwi Park & Han-Eol Park & Myungsun Lee & Jung Weon Lee & Gary J., 2020. "A neural circuit mechanism for mechanosensory feedback control of ingestion," Nature, Nature, vol. 580(7803), pages 376-380, April.
  • Handle: RePEc:nat:nature:v:580:y:2020:i:7803:d:10.1038_s41586-020-2167-2
    DOI: 10.1038/s41586-020-2167-2
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    Cited by:

    1. Fu-Chao Zhang & Rui-Xia Weng & Di Li & Yong-Chang Li & Xiao-Xuan Dai & Shufen Hu & Qian Sun & Rui Li & Guang-Yin Xu, 2024. "A vagus nerve dominant tetra-synaptic ascending pathway for gastric pain processing," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Stefano Nardone & Roberto Luca & Antonino Zito & Nataliya Klymko & Dimitris Nicoloutsopoulos & Oren Amsalem & Cory Brannigan & Jon M. Resch & Christopher L. Jacobs & Deepti Pant & Molly Veregge & Hari, 2024. "A spatially-resolved transcriptional atlas of the murine dorsal pons at single-cell resolution," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. Satvinder Kaur & Nicole Lynch & Yaniv Sela & Janayna D. Lima & Renner C. Thomas & Sathyajit S. Bandaru & Clifford B. Saper, 2024. "Lateral parabrachial FoxP2 neurons regulate respiratory responses to hypercapnia," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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