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Sleep decreases neuronal activity control of microglial dynamics in mice

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  • I. Hristovska

    (INSERM U1314, CNRS UMR5284, MeLiS
    Université Claude Bernard Lyon 1)

  • M. Robert

    (INSERM U1314, CNRS UMR5284, MeLiS
    Université Claude Bernard Lyon 1
    French Reference Center on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique)

  • K. Combet

    (INSERM U1314, CNRS UMR5284, MeLiS
    Université Claude Bernard Lyon 1)

  • J. Honnorat

    (INSERM U1314, CNRS UMR5284, MeLiS
    Université Claude Bernard Lyon 1
    French Reference Center on Paraneoplastic Neurological Syndromes and Autoimmune Encephalitis, Hospices Civils de Lyon, Hôpital Neurologique)

  • J-C Comte

    (Université Claude Bernard Lyon 1
    INSERM U1028, CNRS UMR5292
    Centre de Recherche en Neuroscience de Lyon)

  • O. Pascual

    (INSERM U1314, CNRS UMR5284, MeLiS
    Université Claude Bernard Lyon 1)

Abstract

Microglia, the brain-resident immune cells, are highly ramified with dynamic processes transiently contacting synapses. These contacts have been reported to be activity-dependent, but this has not been thoroughly studied yet, especially in physiological conditions. Here we investigate neuron-microglia contacts and microglia morphodynamics in mice in an activity-dependent context such as the vigilance states. We report that microglial morphodynamics and microglia-spine contacts are regulated by spontaneous and evoked neuronal activity. We also found that sleep modulates microglial morphodynamics through Cx3cr1 signaling. At the synaptic level, microglial processes are attracted towards active spines during wake, and this relationship is hindered during sleep. Finally, microglial contact increases spine activity, mainly during NREM sleep. Altogether, these results indicate that microglial function at synapses is dependent on neuronal activity and the vigilance states, providing evidence that microglia could be important for synaptic homeostasis and plasticity.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34035-9
    DOI: 10.1038/s41467-022-34035-9
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    References listed on IDEAS

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    1. 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.
    2. Laetitia Weinhard & Giulia Bartolomei & Giulia Bolasco & Pedro Machado & Nicole L. Schieber & Urte Neniskyte & Melanie Exiga & Auguste Vadisiute & Angelo Raggioli & Andreas Schertel & Yannick Schwab &, 2018. "Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    3. Yi Zuo & Guang Yang & Elaine Kwon & Wen-Biao Gan, 2005. "Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex," Nature, Nature, vol. 436(7048), pages 261-265, July.
    4. Julie Seibt & Clément J. Richard & Johanna Sigl-Glöckner & Naoya Takahashi & David I. Kaplan & Guy Doron & Denis Limoges & Christina Bocklisch & Matthew E. Larkum, 2017. "Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    5. Ana Badimon & Hayley J. Strasburger & Pinar Ayata & Xinhong Chen & Aditya Nair & Ako Ikegami & Philip Hwang & Andrew T. Chan & Steven M. Graves & Joseph O. Uweru & Carola Ledderose & Munir Gunes Kutlu, 2020. "Negative feedback control of neuronal activity by microglia," Nature, Nature, vol. 586(7829), pages 417-423, October.
    6. Julie Seibt & Clément J. Richard & Johanna Sigl-Glöckner & Naoya Takahashi & David I. Kaplan & Guy Doron & Denis Limoges & Christina Bocklisch & Matthew E. Larkum, 2017. "Publisher Correction: Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents," Nature Communications, Nature, vol. 8(1), pages 1-1, December.
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