Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex

Abstract

Eye opening, a natural and timed event during animal development, influences cortical circuit assembly and maturation; yet, little is known about its precise effect on inhibitory synaptic connections. Here we show that coinciding with eye opening, the strength of unitary inhibitory postsynaptic currents (uIPSCs) from somatostatin-expressing interneurons (Sst-INs) to nearby excitatory neurons, but not interneurons, sharply decreases in layer 2/3 of the mouse visual cortex. In contrast, the strength of uIPSCs from fast-spiking interneurons (FS-INs) to excitatory neurons significantly increases during eye opening. More importantly, these developmental changes can be prevented by dark rearing or binocular lid suture, and reproduced by the artificial opening of sutured lids. Mechanistically, this differential maturation of synaptic transmission is accompanied by a significant change in the postsynaptic quantal size. Together, our study reveals a differential regulation in GABAergic circuits in the cortex driven by eye opening may be crucial for cortical maturation and function.

Article and author information

Author details

  1. Wuqiang Guan

    Institutes of Brain Science, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8412-1007
  2. Jun-Wei Cao

    Institutes of Brain Science, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Lin-Yun Liu

    Institutes of Brain Science, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Zhi-Hao Zhao

    Institutes of Brain Science, Fudan University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yinghui Fu

    Institutes of Brain Science, Fudan University, Shanghai, China
    For correspondence
    fuyh@fudan.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4748-4498
  6. Yong-Chun Yu

    Institutes of Brain Science, Fudan University, Shanghai, China
    For correspondence
    ycyu@fudan.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7456-7451

Funding

National Key Research and Development Program of China (2016YFA0100802)

  • Yinghui Fu

Ministry of Education of the People's Republic of China (20130071110065)

  • Yong-Chun Yu

Science and Technology Commission of Shanghai Municipality (No.15JC1400102)

  • Yong-Chun Yu

Science and Technology Commission of Shanghai Municipality (15XD1500700)

  • Yong-Chun Yu

National Natural Science Foundation of China (31200816)

  • Yinghui Fu

National Natural Science Foundation of China (31271157)

  • Yong-Chun Yu

National Natural Science Foundation of China (31471036)

  • Yong-Chun Yu

National Natural Science Foundation of China (31629004)

  • Yong-Chun Yu

National Natural Science Foundation of China (31421091)

  • Yong-Chun Yu

National Natural Science Foundation of China (91332110)

  • Yong-Chun Yu

Ministry of Science and Technology of the People's Republic of China (2014CB942800)

  • Yong-Chun Yu

Ministry of Science and Technology of the People's Republic of China (2012CB966303)

  • Yong-Chun Yu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All surgical and experimental procedures were in accordance with the protocols approved by the Committee on the Ethics of Animal Experiments of Fudan University Shanghai Medical College (permit number: 20110307-049). All surgery was performed under isoflurane anesthesia and ethanol disinfection to minimize suffering.

Reviewing Editor

  1. Marlene Bartos, University of Freiburg, Germany

Publication history

  1. Received: September 27, 2017
  2. Accepted: December 8, 2017
  3. Accepted Manuscript published: December 11, 2017 (version 1)
  4. Version of Record published: December 28, 2017 (version 2)

Copyright

© 2017, Guan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Wuqiang Guan
  2. Jun-Wei Cao
  3. Lin-Yun Liu
  4. Zhi-Hao Zhao
  5. Yinghui Fu
  6. Yong-Chun Yu
(2017)
Eye opening differentially modulates inhibitory synaptic transmission in the developing visual cortex
eLife 6:e32337.
https://doi.org/10.7554/eLife.32337

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