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Microglia contact induces synapse formation in developing somatosensory cortex

Author

Listed:
  • Akiko Miyamoto

    (National Institute for Physiological Sciences
    Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development)

  • Hiroaki Wake

    (National Institute for Physiological Sciences
    Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development
    The Graduate School for Advanced Study
    Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency)

  • Ayako Wendy Ishikawa

    (The Graduate School for Advanced Study
    National Institute for Physiological Sciences)

  • Kei Eto

    (National Institute for Physiological Sciences
    Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development
    The Graduate School for Advanced Study)

  • Keisuke Shibata

    (Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development
    Graduated School of Medical and Engineering, Yamanashi University)

  • Hideji Murakoshi

    (Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency
    Section of Multiphoton Neuroimaging, National Institute for Physiological Sciences)

  • Schuichi Koizumi

    (Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development
    Graduated School of Medical and Engineering, Yamanashi University)

  • Andrew J. Moorhouse

    (School of Medical Sciences, The University of New South Wales)

  • Yumiko Yoshimura

    (The Graduate School for Advanced Study
    National Institute for Physiological Sciences)

  • Junichi Nabekura

    (National Institute for Physiological Sciences
    Core Research for Evolutional Science and Technology, Japan Agency for Medical Research and Development
    The Graduate School for Advanced Study)

Abstract

Microglia are the immune cells of the central nervous system that play important roles in brain pathologies. Microglia also help shape neuronal circuits during development, via phagocytosing weak synapses and regulating neurogenesis. Using in vivo multiphoton imaging of layer 2/3 pyramidal neurons in the developing somatosensory cortex, we demonstrate here that microglial contact with dendrites directly induces filopodia formation. This filopodia formation occurs only around postnatal day 8–10, a period of intense synaptogenesis and when microglia have an activated phenotype. Filopodia formation is preceded by contact-induced Ca2+ transients and actin accumulation. Inhibition of microglia by genetic ablation decreases subsequent spine density, functional excitatory synapses and reduces the relative connectivity from layer 4 neurons. Our data provide the direct demonstration of microglial-induced spine formation and provide further insights into immune system regulation of neuronal circuit development, with potential implications for developmental disorders of immune and brain dysfunction.

Suggested Citation

  • Akiko Miyamoto & Hiroaki Wake & Ayako Wendy Ishikawa & Kei Eto & Keisuke Shibata & Hideji Murakoshi & Schuichi Koizumi & Andrew J. Moorhouse & Yumiko Yoshimura & Junichi Nabekura, 2016. "Microglia contact induces synapse formation in developing somatosensory cortex," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12540
    DOI: 10.1038/ncomms12540
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    Cited by:

    1. Péter Berki & Csaba Cserép & Zsuzsanna Környei & Balázs Pósfai & Eszter Szabadits & Andor Domonkos & Anna Kellermayer & Miklós Nyerges & Xiaofei Wei & Istvan Mody & Araki Kunihiko & Heinz Beck & He Ka, 2024. "Microglia contribute to neuronal synchrony despite endogenous ATP-related phenotypic transformation in acute mouse brain slices," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    2. Danyang Chen & Qianqian Lou & Xiang-Jie Song & Fang Kang & An Liu & Changjian Zheng & Yanhua Li & Di Wang & Sen Qun & Zhi Zhang & Peng Cao & Yan Jin, 2024. "Microglia govern the extinction of acute stress-induced anxiety-like behaviors in male mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. I. Hristovska & M. Robert & K. Combet & J. Honnorat & J-C Comte & O. Pascual, 2022. "Sleep decreases neuronal activity control of microglial dynamics in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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