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Electrical coupling regulates layer 1 interneuron microcircuit formation in the neocortex

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  • Xing-Hua Yao

    (Institute of Neurobiology, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Collaborative Innovation Center for Brain Science, Fudan University)

  • Min Wang

    (Institute of Neurobiology, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Collaborative Innovation Center for Brain Science, Fudan University)

  • Xiang-Nan He

    (Centre for Computational Systems Biology and the School of Mathematical Sciences, Fudan University)

  • Fei He

    (Stem Cell Translational Research Center, Tongji Hospital, Tongji University School of Medicine)

  • Shu-Qing Zhang

    (Institute of Neurobiology, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Collaborative Innovation Center for Brain Science, Fudan University)

  • Wenlian Lu

    (Centre for Computational Systems Biology and the School of Mathematical Sciences, Fudan University)

  • Zi-Long Qiu

    (Institute of Neuroscience and State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences and University of Chinese Academy of Sciences)

  • Yong-Chun Yu

    (Institute of Neurobiology, Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Collaborative Innovation Center for Brain Science, Fudan University)

Abstract

The coexistence of electrical and chemical synapses among interneurons is essential for interneuron function in the neocortex. However, it remains largely unclear whether electrical coupling between interneurons influences chemical synapse formation and microcircuit assembly during development. Here, we show that electrical and GABAergic chemical connections robustly develop between interneurons in neocortical layer 1 over a similar time course. Electrical coupling promotes action potential generation and synchronous firing between layer 1 interneurons. Furthermore, electrically coupled interneurons exhibit strong GABA-A receptor-mediated synchronous synaptic activity. Disruption of electrical coupling leads to a loss of bidirectional, but not unidirectional, GABAergic connections. Moreover, a reduction in electrical coupling induces an increase in excitatory synaptic inputs to layer 1 interneurons. Together, these findings strongly suggest that electrical coupling between neocortical interneurons plays a critical role in regulating chemical synapse development and precise formation of circuits.

Suggested Citation

  • Xing-Hua Yao & Min Wang & Xiang-Nan He & Fei He & Shu-Qing Zhang & Wenlian Lu & Zi-Long Qiu & Yong-Chun Yu, 2016. "Electrical coupling regulates layer 1 interneuron microcircuit formation in the neocortex," Nature Communications, Nature, vol. 7(1), pages 1-15, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12229
    DOI: 10.1038/ncomms12229
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