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Sequential appetite suppression by oral and visceral feedback to the brainstem

Author

Listed:
  • Truong Ly

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Jun Y. Oh

    (University of California, San Francisco)

  • Nilla Sivakumar

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Sarah Shehata

    (University of California, San Francisco)

  • Naymalis La Santa Medina

    (University of California, San Francisco)

  • Heidi Huang

    (University of California, San Francisco)

  • Zhengya Liu

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Wendy Fang

    (University of California, San Francisco)

  • Chris Barnes

    (University of California, San Francisco)

  • Naz Dundar

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Brooke C. Jarvie

    (University of California, San Francisco
    University of California, San Francisco)

  • Anagh Ravi

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Olivia K. Barnhill

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Chelsea Li

    (University of California, San Francisco)

  • Grace R. Lee

    (University of California, San Francisco)

  • Jaewon Choi

    (University of California, San Francisco)

  • Heeun Jang

    (University of California, San Francisco)

  • Zachary A. Knight

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

Abstract

The termination of a meal is controlled by dedicated neural circuits in the caudal brainstem. A key challenge is to understand how these circuits transform the sensory signals generated during feeding into dynamic control of behaviour. The caudal nucleus of the solitary tract (cNTS) is the first site in the brain where many meal-related signals are sensed and integrated1–4, but how the cNTS processes ingestive feedback during behaviour is unknown. Here we describe how prolactin-releasing hormone (PRLH) and GCG neurons, two principal cNTS cell types that promote non-aversive satiety, are regulated during ingestion. PRLH neurons showed sustained activation by visceral feedback when nutrients were infused into the stomach, but these sustained responses were substantially reduced during oral consumption. Instead, PRLH neurons shifted to a phasic activity pattern that was time-locked to ingestion and linked to the taste of food. Optogenetic manipulations revealed that PRLH neurons control the duration of seconds-timescale feeding bursts, revealing a mechanism by which orosensory signals feed back to restrain the pace of ingestion. By contrast, GCG neurons were activated by mechanical feedback from the gut, tracked the amount of food consumed and promoted satiety that lasted for tens of minutes. These findings reveal that sequential negative feedback signals from the mouth and gut engage distinct circuits in the caudal brainstem, which in turn control elements of feeding behaviour operating on short and long timescales.

Suggested Citation

  • Truong Ly & Jun Y. Oh & Nilla Sivakumar & Sarah Shehata & Naymalis La Santa Medina & Heidi Huang & Zhengya Liu & Wendy Fang & Chris Barnes & Naz Dundar & Brooke C. Jarvie & Anagh Ravi & Olivia K. Barn, 2023. "Sequential appetite suppression by oral and visceral feedback to the brainstem," Nature, Nature, vol. 624(7990), pages 130-137, December.
  • Handle: RePEc:nat:nature:v:624:y:2023:i:7990:d:10.1038_s41586-023-06758-2
    DOI: 10.1038/s41586-023-06758-2
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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.

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