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Low-intensity pulsed ultrasound stimulation (LIPUS) modulates microglial activation following intracortical microelectrode implantation

Author

Listed:
  • Fan Li

    (University of Pittsburgh
    Center for Neural Basis of Cognition
    University of Pittsburgh)

  • Jazlyn Gallego

    (University of Pittsburgh
    Center for Neural Basis of Cognition)

  • Natasha N. Tirko

    (Pennsylvania State University)

  • Jenna Greaser

    (Actuated Medical)

  • Derek Bashe

    (Washington University in St. Louis)

  • Rudra Patel

    (University of Pittsburgh)

  • Eric Shaker

    (University of Pittsburgh)

  • Grace E. Valkenburg

    (University of Pittsburgh)

  • Alanoud S. Alsubhi

    (Actuated Medical)

  • Steven Wellman

    (Columbia University)

  • Vanshika Singh

    (University of Pittsburgh)

  • Camila Garcia Padilla

    (University of Pittsburgh
    Center for Neural Basis of Cognition)

  • Kyle W. Gheres

    (Actuated Medical)

  • John I. Broussard

    (Actuated Medical)

  • Roger Bagwell

    (Actuated Medical)

  • Maureen Mulvihill

    (Actuated Medical)

  • Takashi D. Y. Kozai

    (University of Pittsburgh
    Center for Neural Basis of Cognition
    University of Pittsburgh
    University of Pittsburgh)

Abstract

Microglia are important players in surveillance and repair of the brain. Implanting an electrode into the cortex activates microglia, produces an inflammatory cascade, triggers the foreign body response, and opens the blood-brain barrier. These changes can impede intracortical brain-computer interfaces performance. Using two-photon imaging of implanted microelectrodes, we test the hypothesis that low-intensity pulsed ultrasound stimulation can reduce microglia-mediated neuroinflammation following the implantation of microelectrodes. In the first week of treatment, we found that low-intensity pulsed ultrasound stimulation increased microglia migration speed by 128%, enhanced microglia expansion area by 109%, and a reduction in microglial activation by 17%, indicating improved tissue healing and surveillance. Microglial coverage of the microelectrode was reduced by 50% and astrocytic scarring by 36% resulting in an increase in recording performance at chronic time. The data indicate that low-intensity pulsed ultrasound stimulation helps reduce the foreign body response around chronic intracortical microelectrodes.

Suggested Citation

  • Fan Li & Jazlyn Gallego & Natasha N. Tirko & Jenna Greaser & Derek Bashe & Rudra Patel & Eric Shaker & Grace E. Valkenburg & Alanoud S. Alsubhi & Steven Wellman & Vanshika Singh & Camila Garcia Padill, 2024. "Low-intensity pulsed ultrasound stimulation (LIPUS) modulates microglial activation following intracortical microelectrode implantation," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49709-9
    DOI: 10.1038/s41467-024-49709-9
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    1. Leigh R. Hochberg & Daniel Bacher & Beata Jarosiewicz & Nicolas Y. Masse & John D. Simeral & Joern Vogel & Sami Haddadin & Jie Liu & Sydney S. Cash & Patrick van der Smagt & John P. Donoghue, 2012. "Reach and grasp by people with tetraplegia using a neurally controlled robotic arm," Nature, Nature, vol. 485(7398), pages 372-375, May.
    2. Kai Yu & Xiaodan Niu & Esther Krook-Magnuson & Bin He, 2021. "Intrinsic functional neuron-type selectivity of transcranial focused ultrasound neuromodulation," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Dimitrios Davalos & Jae Kyu Ryu & Mario Merlini & Kim M. Baeten & Natacha Le Moan & Mark A. Petersen & Thomas J. Deerinck & Dimitri S. Smirnoff & Catherine Bedard & Hiroyuki Hakozaki & Sara Gonias Mur, 2012. "Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation," Nature Communications, Nature, vol. 3(1), pages 1-15, January.
    4. Kanchan Bisht & Kenneth A. Okojie & Kaushik Sharma & Dennis H. Lentferink & Yu-Yo Sun & Hong-Ru Chen & Joseph O. Uweru & Saipranusha Amancherla & Zainab Calcuttawala & Antony Brayan Campos-Salazar & B, 2021. "Capillary-associated microglia regulate vascular structure and function through PANX1-P2RY12 coupling in mice," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    5. Koichiro Haruwaka & Ako Ikegami & Yoshihisa Tachibana & Nobuhiko Ohno & Hiroyuki Konishi & Akari Hashimoto & Mami Matsumoto & Daisuke Kato & Riho Ono & Hiroshi Kiyama & Andrew J. Moorhouse & Junichi N, 2019. "Dual microglia effects on blood brain barrier permeability induced by systemic inflammation," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    6. D. Huber & D. A. Gutnisky & S. Peron & D. H. O’Connor & J. S. Wiegert & L. Tian & T. G. Oertner & L. L. Looger & K. Svoboda, 2012. "Multiple dynamic representations in the motor cortex during sensorimotor learning," Nature, Nature, vol. 484(7395), pages 473-478, April.
    7. Shane A. Liddelow & Kevin A. Guttenplan & Laura E. Clarke & Frederick C. Bennett & Christopher J. Bohlen & Lucas Schirmer & Mariko L. Bennett & Alexandra E. Münch & Won-Suk Chung & Todd C. Peterson & , 2017. "Neurotoxic reactive astrocytes are induced by activated microglia," Nature, Nature, vol. 541(7638), pages 481-487, January.
    8. Francesco De Logu & Romina Nassini & Serena Materazzi & Muryel Carvalho Gonçalves & Daniele Nosi & Duccio Rossi Degl’Innocenti & Ilaria M. Marone & Juliano Ferreira & Simone Li Puma & Silvia Benemei &, 2017. "Schwann cell TRPA1 mediates neuroinflammation that sustains macrophage-dependent neuropathic pain in mice," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
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