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Gut vagal sensory signaling regulates hippocampus function through multi-order pathways

Author

Listed:
  • Andrea N. Suarez

    (University of Southern California)

  • Ted M. Hsu

    (University of Southern California
    University of Illinois at Chicago)

  • Clarissa M. Liu

    (University of Southern California
    University of Southern California)

  • Emily E. Noble

    (University of Southern California)

  • Alyssa M. Cortella

    (University of Southern California)

  • Emily M. Nakamoto

    (University of Southern California)

  • Joel D. Hahn

    (University of Southern California)

  • Guillaume Lartigue

    (The John B. Pierce Laboratory
    Yale Medical School)

  • Scott E. Kanoski

    (University of Southern California
    University of Southern California
    University of Southern California)

Abstract

The vagus nerve is the primary means of neural communication between the gastrointestinal (GI) tract and the brain. Vagally mediated GI signals activate the hippocampus (HPC), a brain region classically linked with memory function. However, the endogenous relevance of GI-derived vagal HPC communication is unknown. Here we utilize a saporin (SAP)-based lesioning procedure to reveal that selective GI vagal sensory/afferent ablation in rats impairs HPC-dependent episodic and spatial memory, effects associated with reduced HPC neurotrophic and neurogenesis markers. To determine the neural pathways connecting the gut to the HPC, we utilize monosynaptic and multisynaptic virus-based tracing methods to identify the medial septum as a relay connecting the medial nucleus tractus solitarius (where GI vagal afferents synapse) to dorsal HPC glutamatergic neurons. We conclude that endogenous GI-derived vagal sensory signaling promotes HPC-dependent memory function via a multi-order brainstem–septal pathway, thereby identifying a previously unknown role for the gut–brain axis in memory control.

Suggested Citation

  • Andrea N. Suarez & Ted M. Hsu & Clarissa M. Liu & Emily E. Noble & Alyssa M. Cortella & Emily M. Nakamoto & Joel D. Hahn & Guillaume Lartigue & Scott E. Kanoski, 2018. "Gut vagal sensory signaling regulates hippocampus function through multi-order pathways," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04639-1
    DOI: 10.1038/s41467-018-04639-1
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    Cited by:

    1. Toya Okonogi & Nahoko Kuga & Musashi Yamakawa & Tasuku Kayama & Yuji Ikegaya & Takuya Sasaki, 2024. "Stress-induced vagal activity influences anxiety-relevant prefrontal and amygdala neuronal oscillations in male mice," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Yuni Kay & Linda Tsan & Elizabeth A. Davis & Chen Tian & Léa Décarie-Spain & Anastasiia Sadybekov & Anna N. Pushkin & Vsevolod Katritch & Scott E. Kanoski & Bruce E. Herring, 2022. "Schizophrenia-associated SAP97 mutations increase glutamatergic synapse strength in the dentate gyrus and impair contextual episodic memory in rats," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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