Functional effects of distinct innervation styles of pyramidal cells by fast spiking cortical interneurons

  1. Yoshiyuki Kubota  Is a corresponding author
  2. Satoru Kondo
  3. Masaki Nomura
  4. Sayuri Hatada
  5. Noboru Yamaguchi
  6. Alsayed A Mohamed
  7. Fuyuki Karube
  8. Joachim Lübke
  9. Yasuo Kawaguchi
  1. National Institute for Physiological Sciences, Japan
  2. Japan Science and Technology Agency, Japan
  3. Kyoto University, Japan
  4. Research Centre Jülich, Germany

Abstract

Inhibitory interneurons target precise membrane regions on pyramidal cells, but differences in their functional effects on somata, dendrites and spines remain unclear. We analyzed inhibitory synaptic events induced by cortical, fast-spiking (FS) basket cells which innervate dendritic shafts and spines as well as pyramidal cell somata. Serial electron micrographs (EMgs) reconstruction showed that somatic synapses were larger than dendritic contacts. Simulations with precise anatomical and physiological data reveal functional differences between different innervation styles. FS cell soma-targeting synapses initiate a strong, global inhibition, those on shafts inhibit more restricted dendritic zones, while synapses on spines may mediate a strictly local veto. Thus, FS cell synapses of different sizes and sites provide functionally diverse forms of pyramidal cell inhibition.

Article and author information

Author details

  1. Yoshiyuki Kubota

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    For correspondence
    yoshiy@nips.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
  2. Satoru Kondo

    Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Masaki Nomura

    Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Sayuri Hatada

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Noboru Yamaguchi

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Alsayed A Mohamed

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Fuyuki Karube

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Joachim Lübke

    Institute for Neuroscience and Medicine, Research Centre Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Yasuo Kawaguchi

    Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Marlene Bartos, Albert-Ludwigs-Universität Freiburg, Germany

Ethics

Animal experimentation: All surgical and animal care methods was performed in strict accordance with the Guidelines for the Use of Animals of IBRO and our institutional Animal Care and Use committee (National Institute for Physiological Sciences) with reference number 14A011. All surgery was performed under ketamine and xylazine, or isoflurane anesthesia, and every effort was made to minimize suffering.

Version history

  1. Received: April 3, 2015
  2. Accepted: July 4, 2015
  3. Accepted Manuscript published: July 4, 2015 (version 1)
  4. Version of Record published: July 29, 2015 (version 2)

Copyright

© 2015, Kubota 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. Yoshiyuki Kubota
  2. Satoru Kondo
  3. Masaki Nomura
  4. Sayuri Hatada
  5. Noboru Yamaguchi
  6. Alsayed A Mohamed
  7. Fuyuki Karube
  8. Joachim Lübke
  9. Yasuo Kawaguchi
(2015)
Functional effects of distinct innervation styles of pyramidal cells by fast spiking cortical interneurons
eLife 4:e07919.
https://doi.org/10.7554/eLife.07919

Share this article

https://doi.org/10.7554/eLife.07919

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