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Homeostatic circuits selectively gate food cue responses in insular cortex

Author

Listed:
  • Yoav Livneh

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Rohan N. Ramesh

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School
    Program in Neuroscience, Harvard Medical School)

  • Christian R. Burgess

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Kirsten M. Levandowski

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Joseph C. Madara

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Henning Fenselau

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Glenn J. Goldey

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Veronica E. Diaz

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Nick Jikomes

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School
    Program in Neuroscience, Harvard Medical School)

  • Jon M. Resch

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School)

  • Bradford B. Lowell

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School
    Program in Neuroscience, Harvard Medical School)

  • Mark L. Andermann

    (Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School
    Program in Neuroscience, Harvard Medical School)

Abstract

Physiological needs bias perception and attention to relevant sensory cues. This process is ‘hijacked’ by drug addiction, causing cue-induced cravings and relapse. Similarly, its dysregulation contributes to failed diets, obesity, and eating disorders. Neuroimaging studies in humans have implicated insular cortex in these phenomena. However, it remains unclear how ‘cognitive’ cortical representations of motivationally relevant cues are biased by subcortical circuits that drive specific motivational states. Here we develop a microprism-based cellular imaging approach to monitor visual cue responses in the insular cortex of behaving mice across hunger states. Insular cortex neurons demonstrate food-cue-biased responses that are abolished during satiety. Unexpectedly, while multiple satiety-related visceral signals converge in insular cortex, chemogenetic activation of hypothalamic ‘hunger neurons’ (expressing agouti-related peptide (AgRP)) bypasses these signals to restore hunger-like response patterns in insular cortex. Circuit mapping and pathway-specific manipulations uncover a pathway from AgRP neurons to insular cortex via the paraventricular thalamus and basolateral amygdala. These results reveal a neural basis for state-specific biased processing of motivationally relevant cues.

Suggested Citation

  • Yoav Livneh & Rohan N. Ramesh & Christian R. Burgess & Kirsten M. Levandowski & Joseph C. Madara & Henning Fenselau & Glenn J. Goldey & Veronica E. Diaz & Nick Jikomes & Jon M. Resch & Bradford B. Low, 2017. "Homeostatic circuits selectively gate food cue responses in insular cortex," Nature, Nature, vol. 546(7660), pages 611-616, June.
  • Handle: RePEc:nat:nature:v:546:y:2017:i:7660:d:10.1038_nature22375
    DOI: 10.1038/nature22375
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    Citations

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    Cited by:

    1. 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.
    2. Yosuke Yawata & Yu Shikano & Jun Ogasawara & Kenichi Makino & Tetsuhiko Kashima & Keiko Ihara & Airi Yoshimoto & Shota Morikawa & Sho Yagishita & Kenji F. Tanaka & Yuji Ikegaya, 2023. "Mesolimbic dopamine release precedes actively sought aversive stimuli in mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Anna J. Bowen & Y. Waterlily Huang & Jane Y. Chen & Jordan L. Pauli & Carlos A. Campos & Richard D. Palmiter, 2023. "Topographic representation of current and future threats in the mouse nociceptive amygdala," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. 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.

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