Multisensory gamma stimulation promotes glymphatic clearance of amyloid

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, Noelle Leary, Sidney Wang, Adele Bubnys, Emily Ma, Leyla A. Akay, Madison Sneve, Yong Qian, Cuixin Lai, Michelle M. McCarthy, Nancy Kopell, Manolis Kellis, Kiryl D. Piatkevich, Edward S. Boyden and Li-Huei Tsai ()
Additional contact information
Mitchell H. Murdock: Massachusetts Institute of Technology
Cheng-Yi Yang: Massachusetts Institute of Technology
Na Sun: MIT Computer Science and Artificial Intelligence Laboratory
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
Yong Qian: McGovern Institute
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
Kiryl D. Piatkevich: McGovern Institute
Edward S. Boyden: McGovern Institute
Li-Huei Tsai: Massachusetts Institute of Technology

Nature, 2024, vol. 627, issue 8002, 149-156

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41586-024-07132-6

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