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Multisensory gamma stimulation promotes glymphatic clearance of amyloid

Author

Listed:
  • Mitchell H. Murdock

    (Massachusetts Institute of Technology)

  • Cheng-Yi Yang

    (Massachusetts Institute of Technology)

  • Na Sun

    (MIT Computer Science and Artificial Intelligence Laboratory
    Broad Institute of MIT and Harvard)

  • Ping-Chieh Pao

    (Massachusetts Institute of Technology)

  • Cristina Blanco-Duque

    (Massachusetts Institute of Technology)

  • Martin C. Kahn

    (Massachusetts Institute of Technology)

  • TaeHyun Kim

    (Massachusetts Institute of Technology)

  • Nicolas S. Lavoie

    (Massachusetts Institute of Technology)

  • Matheus B. Victor

    (Massachusetts Institute of Technology)

  • Md Rezaul Islam

    (Massachusetts Institute of Technology)

  • Fabiola Galiana

    (Massachusetts Institute of Technology)

  • Noelle Leary

    (Massachusetts Institute of Technology)

  • Sidney Wang

    (Massachusetts Institute of Technology)

  • Adele Bubnys

    (Massachusetts Institute of Technology)

  • Emily Ma

    (Massachusetts Institute of Technology)

  • Leyla A. Akay

    (Massachusetts Institute of Technology)

  • Madison Sneve

    (McGovern Institute
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Yong Qian

    (McGovern Institute
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Cuixin Lai

    (Westlake University, Westlake Laboratory of Life Sciences and Biomedicine, and Westlake Institute for Advanced Study)

  • Michelle M. McCarthy

    (Boston University)

  • Nancy Kopell

    (Boston University)

  • Manolis Kellis

    (MIT Computer Science and Artificial Intelligence Laboratory
    Broad Institute of MIT and Harvard)

  • Kiryl D. Piatkevich

    (McGovern Institute
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Westlake University, Westlake Laboratory of Life Sciences and Biomedicine, and Westlake Institute for Advanced Study)

  • Edward S. Boyden

    (McGovern Institute
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Li-Huei Tsai

    (Massachusetts Institute of Technology
    Broad Institute of MIT and Harvard)

Abstract

The glymphatic movement of fluid through the brain removes metabolic waste1–4. Noninvasive 40 Hz stimulation promotes 40 Hz neural activity in multiple brain regions and attenuates pathology in mouse models of Alzheimer’s disease5–8. Here we show that multisensory gamma stimulation promotes the influx of cerebrospinal fluid and the efflux of interstitial fluid in the cortex of the 5XFAD mouse model of Alzheimer’s disease. Influx of cerebrospinal fluid was associated with increased aquaporin-4 polarization along astrocytic endfeet and dilated meningeal lymphatic vessels. Inhibiting glymphatic clearance abolished the removal of amyloid by multisensory 40 Hz stimulation. Using chemogenetic manipulation and a genetically encoded sensor for neuropeptide signalling, we found that vasoactive intestinal peptide interneurons facilitate glymphatic clearance by regulating arterial pulsatility. Our findings establish novel mechanisms that recruit the glymphatic system to remove brain amyloid.

Suggested Citation

  • Mitchell H. Murdock & Cheng-Yi Yang & Na Sun & Ping-Chieh Pao & Cristina Blanco-Duque & Martin C. Kahn & TaeHyun Kim & Nicolas S. Lavoie & Matheus B. Victor & Md Rezaul Islam & Fabiola Galiana & Noell, 2024. "Multisensory gamma stimulation promotes glymphatic clearance of amyloid," Nature, Nature, vol. 627(8002), pages 149-156, March.
  • Handle: RePEc:nat:nature:v:627:y:2024:i:8002:d:10.1038_s41586-024-07132-6
    DOI: 10.1038/s41586-024-07132-6
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    Cited by:

    1. Daniela Rodrigues-Amorim & P. Lorenzo Bozzelli & TaeHyun Kim & Liwang Liu & Oliver Gibson & Cheng-Yi Yang & Mitchell H. Murdock & Fabiola Galiana-Melendez & Brooke Schatz & Alexis Davison & Md Rezaul , 2024. "Multisensory gamma stimulation mitigates the effects of demyelination induced by cuprizone in male mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Xin Huang & Chris Fowler & Yihan Li & Qiao-Xin Li & Jiaqi Sun & Yijun Pan & Liang Jin & Keyla A. Perez & Céline Dubois & Yen Y. Lim & Candace Drysdale & Rebecca L. Rumble & Holly R. Chinnery & Christo, 2024. "Clearance and transport of amyloid β by peripheral monocytes correlate with Alzheimer’s disease progression," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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