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Multisensory gamma stimulation mitigates the effects of demyelination induced by cuprizone in male mice

Author

Listed:
  • Daniela Rodrigues-Amorim

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • P. Lorenzo Bozzelli

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • TaeHyun Kim

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Liwang Liu

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Oliver Gibson

    (Ltd)

  • Cheng-Yi Yang

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Mitchell H. Murdock

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Fabiola Galiana-Melendez

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Brooke Schatz

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Alexis Davison

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Md Rezaul Islam

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Dong Shin Park

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Ravikiran M. Raju

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology
    Harvard Medical School, Boston Children’s Hospital)

  • Fatema Abdurrob

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Alissa J. Nelson

    (Cell Signaling Technology)

  • Jian Min Ren

    (Cell Signaling Technology)

  • Vicky Yang

    (Cell Signaling Technology)

  • Matthew P. Stokes

    (Cell Signaling Technology)

  • Li-Huei Tsai

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology
    Broad Institute of Harvard and MIT)

Abstract

Demyelination is a common pathological feature in a wide range of diseases, characterized by the loss of myelin sheath and myelin-supporting oligodendrocytes. These losses lead to impaired axonal function, increased vulnerability of axons to damage, and result in significant brain atrophy and neuro-axonal degeneration. Multiple pathomolecular processes contribute to neuroinflammation, oligodendrocyte cell death, and progressive neuronal dysfunction. In this study, we use the cuprizone mouse model of demyelination to investigate long-term non-invasive gamma entrainment using sensory stimulation as a potential therapeutic intervention for promoting myelination and reducing neuroinflammation in male mice. Here, we show that multisensory gamma stimulation mitigates demyelination, promotes oligodendrogenesis, preserves functional integrity and synaptic plasticity, attenuates oligodendrocyte ferroptosis-induced cell death, and reduces brain inflammation. Thus, the protective effects of multisensory gamma stimulation on myelin and anti-neuroinflammatory properties support its potential as a therapeutic approach for demyelinating disorders.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51003-7
    DOI: 10.1038/s41467-024-51003-7
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    References listed on IDEAS

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    1. Hannah F. Iaccarino & Annabelle C. Singer & Anthony J. Martorell & Andrii Rudenko & Fan Gao & Tyler Z. Gillingham & Hansruedi Mathys & Jinsoo Seo & Oleg Kritskiy & Fatema Abdurrob & Chinnakkaruppan Ad, 2016. "Gamma frequency entrainment attenuates amyloid load and modifies microglia," Nature, Nature, vol. 540(7632), pages 230-235, December.
    2. 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.
    3. Lucas Schirmer & Dmitry Velmeshev & Staffan Holmqvist & Max Kaufmann & Sebastian Werneburg & Diane Jung & Stephanie Vistnes & John H. Stockley & Adam Young & Maike Steindel & Brian Tung & Nitasha Goya, 2019. "Neuronal vulnerability and multilineage diversity in multiple sclerosis," Nature, Nature, vol. 573(7772), pages 75-82, September.
    4. Lifeng Zheng & Mei Yu & Rui Lin & Yunxuan Wang & Zhan Zhuo & Ning Cheng & Mengzhen Wang & Yongqiang Tang & Liping Wang & Sheng-Tao Hou, 2020. "Rhythmic light flicker rescues hippocampal low gamma and protects ischemic neurons by enhancing presynaptic plasticity," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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