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NPY-mediated synaptic plasticity in the extended amygdala prioritizes feeding during starvation

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Listed:
  • Stephan Dodt

    (Max Planck Institute for Metabolism Research
    Max Planck Institute for Metabolism Research)

  • Noah V. Widdershooven

    (Max Planck Institute for Metabolism Research)

  • Marie-Luise Dreisow

    (Max Planck Institute for Metabolism Research
    University Hospital Cologne)

  • Lisa Weiher

    (Max Planck Institute for Metabolism Research)

  • Lukas Steuernagel

    (Max Planck Institute for Metabolism Research)

  • F. Thomas Wunderlich

    (Max Planck Institute for Metabolism Research
    University Hospital Cologne
    University of Cologne
    University of Cologne)

  • Jens C. Brüning

    (Max Planck Institute for Metabolism Research
    University Hospital Cologne
    University of Cologne
    University of Cologne)

  • Henning Fenselau

    (Max Planck Institute for Metabolism Research
    University Hospital Cologne
    University of Cologne)

Abstract

Efficient control of feeding behavior requires the coordinated adjustment of complex motivational and affective neurocircuits. Neuropeptides from energy-sensing hypothalamic neurons are potent feeding modulators, but how these endogenous signals shape relevant circuits remains unclear. Here, we examine how the orexigenic neuropeptide Y (NPY) adapts GABAergic inputs to the bed nucleus of the stria terminalis (BNST). We find that fasting increases synaptic connectivity between agouti-related peptide (AgRP)-expressing ‘hunger’ and BNST neurons, a circuit that promotes feeding. In contrast, GABAergic input from the central amygdala (CeA), an extended amygdala circuit that decreases feeding, is reduced. Activating NPY-expressing AgRP neurons evokes these synaptic adaptations, which are absent in NPY-deficient mice. Moreover, fasting diminishes the ability of CeA projections in the BNST to suppress food intake, and NPY-deficient mice fail to decrease anxiety in order to promote feeding. Thus, AgRP neurons drive input-specific synaptic plasticity, enabling a selective shift in hunger and anxiety signaling during starvation through NPY.

Suggested Citation

  • Stephan Dodt & Noah V. Widdershooven & Marie-Luise Dreisow & Lisa Weiher & Lukas Steuernagel & F. Thomas Wunderlich & Jens C. Brüning & Henning Fenselau, 2024. "NPY-mediated synaptic plasticity in the extended amygdala prioritizes feeding during starvation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49766-0
    DOI: 10.1038/s41467-024-49766-0
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    References listed on IDEAS

    as
    1. Nao Horio & Stephen D. Liberles, 2021. "Hunger enhances food-odour attraction through a neuropeptide Y spotlight," Nature, Nature, vol. 592(7853), pages 262-266, April.
    2. Amelia M. Douglass & Jon M. Resch & Joseph C. Madara & Hakan Kucukdereli & Ofer Yizhar & Abhinav Grama & Masahito Yamagata & Zongfang Yang & Bradford B. Lowell, 2023. "Neural basis for fasting activation of the hypothalamic–pituitary–adrenal axis," Nature, Nature, vol. 620(7972), pages 154-162, August.
    3. Sung-Yon Kim & Avishek Adhikari & Soo Yeun Lee & James H. Marshel & Christina K. Kim & Caitlin S. Mallory & Maisie Lo & Sally Pak & Joanna Mattis & Byung Kook Lim & Robert C. Malenka & Melissa R. Ward, 2013. "Diverging neural pathways assemble a behavioural state from separable features in anxiety," Nature, Nature, vol. 496(7444), pages 219-223, April.
    4. Michael A. Cowley & James L. Smart & Marcelo Rubinstein & Marcelo G. Cerdán & Sabrina Diano & Tamas L. Horvath & Roger D. Cone & Malcolm J. Low, 2001. "Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus," Nature, Nature, vol. 411(6836), pages 480-484, May.
    5. Deniz Atasoy & J. Nicholas Betley & Helen H. Su & Scott M. Sternson, 2012. "Deconstruction of a neural circuit for hunger," Nature, Nature, vol. 488(7410), pages 172-177, August.
    6. Linda Engström Ruud & Mafalda M. A. Pereira & Alain J. Solis & Henning Fenselau & Jens C. Brüning, 2020. "NPY mediates the rapid feeding and glucose metabolism regulatory functions of AgRP neurons," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
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