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Gamma frequency entrainment attenuates amyloid load and modifies microglia

Author

Listed:
  • Hannah F. Iaccarino

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

  • Annabelle C. Singer

    (McGovern Institute for Brain Research, Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    MIT Media Lab, Massachusetts Institute of Technology)

  • Anthony J. Martorell

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

  • Andrii Rudenko

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

  • Fan Gao

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

  • Tyler Z. Gillingham

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

  • Hansruedi Mathys

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

  • Jinsoo Seo

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

  • Oleg Kritskiy

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

  • Fatema Abdurrob

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

  • Chinnakkaruppan Adaikkan

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

  • Rebecca G. Canter

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

  • Richard Rueda

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

  • Emery N. Brown

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Institute of Medical Engineering and Sciences, Massachusetts Institute of Technology
    Massachusetts General Hospital, Boston)

  • Edward S. Boyden

    (McGovern Institute for Brain Research, Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    MIT Media Lab, Massachusetts Institute of Technology)

  • Li-Huei Tsai

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

Abstract

Changes in gamma oscillations (20–50 Hz) have been observed in several neurological disorders. However, the relationship between gamma oscillations and cellular pathologies is unclear. Here we show reduced, behaviourally driven gamma oscillations before the onset of plaque formation or cognitive decline in a mouse model of Alzheimer’s disease. Optogenetically driving fast-spiking parvalbumin-positive (FS-PV)-interneurons at gamma (40 Hz), but not other frequencies, reduces levels of amyloid-β (Aβ)1–40 and Aβ 1–42 isoforms. Gene expression profiling revealed induction of genes associated with morphological transformation of microglia, and histological analysis confirmed increased microglia co-localization with Aβ. Subsequently, we designed a non-invasive 40 Hz light-flickering regime that reduced Aβ1–40 and Aβ1–42 levels in the visual cortex of pre-depositing mice and mitigated plaque load in aged, depositing mice. Our findings uncover a previously unappreciated function of gamma rhythms in recruiting both neuronal and glial responses to attenuate Alzheimer’s-disease-associated pathology.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:540:y:2016:i:7632:d:10.1038_nature20587
    DOI: 10.1038/nature20587
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    Cited by:

    1. Lou T. Blanpain & Eric R. Cole & Emily Chen & James K. Park & Michael Y. Walelign & Robert E. Gross & Brian T. Cabaniss & Jon T. Willie & Annabelle C. Singer, 2024. "Multisensory flicker modulates widespread brain networks and reduces interictal epileptiform discharges," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. Ankita Sengupta & Sanjna Banerjee & Suhas Ganesh & Shrey Grover & Devarajan Sridharan, 2024. "The right posterior parietal cortex mediates spatial reorienting of attentional choice bias," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. 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.
    4. Amy Clements-Cortes & Lee Bartel, 2022. "Long-Term Multi-Sensory Gamma Stimulation of Dementia Patients: A Case Series Report," IJERPH, MDPI, vol. 19(23), pages 1-10, November.
    5. Koustav Roy & Xuzhao Zhou & Rintaro Otani & Ping-Chuan Yuan & Shuji Ioka & Kaspar E. Vogt & Tamae Kondo & Nouran H. T. Farag & Haruto Ijiri & Zhaofa Wu & Youhei Chitose & Mao Amezawa & David S. Uygun , 2024. "Optochemical control of slow-wave sleep in the nucleus accumbens of male mice by a photoactivatable allosteric modulator of adenosine A2A receptors," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Ayuto Kodama & Yasuhiro Suzuki & Kazuki Sakuraba & Yu Kume & Hidetaka Ota, 2022. "The Effect of Deep Micro Vibrotactile Stimulation on Cognitive Function of Mild Cognitive Impairment and Mild Dementia," IJERPH, MDPI, vol. 19(7), pages 1-10, March.
    7. Thenille Braun Janzen & Denise Paneduro & Larry Picard & Allan Gordon & Lee R Bartel, 2019. "A parallel randomized controlled trial examining the effects of rhythmic sensory stimulation on fibromyalgia symptoms," PLOS ONE, Public Library of Science, vol. 14(3), pages 1-19, March.
    8. Ana Sofía Ríos & Simón Oxenford & Clemens Neudorfer & Konstantin Butenko & Ningfei Li & Nanditha Rajamani & Alexandre Boutet & Gavin J. B. Elias & Jurgen Germann & Aaron Loh & Wissam Deeb & Fuyixue Wa, 2022. "Optimal deep brain stimulation sites and networks for stimulation of the fornix in Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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