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.

Metrics

  • 3,916
    views
  • 916
    downloads
  • 61
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Neuroscience
    Juan Jose Rodriguez Gotor, Kashif Mahfooz ... John F Wesseling
    Research Article

    Vesicles within presynaptic terminals are thought to be segregated into a variety of readily releasable and reserve pools. The nature of the pools and trafficking between them is not well understood, but pools that are slow to mobilize when synapses are active are often assumed to feed pools that are mobilized more quickly, in a series. However, electrophysiological studies of synaptic transmission have suggested instead a parallel organization where vesicles within slowly and quickly mobilized reserve pools would separately feed independent reluctant- and fast-releasing subdivisions of the readily releasable pool. Here, we use FM-dyes to confirm the existence of multiple reserve pools at hippocampal synapses and a parallel organization that prevents intermixing between the pools, even when stimulation is intense enough to drive exocytosis at the maximum rate. The experiments additionally demonstrate extensive heterogeneity among synapses in the relative sizes of the slowly and quickly mobilized reserve pools, which suggests equivalent heterogeneity in the numbers of reluctant and fast-releasing readily releasable vesicles that may be relevant for understanding information processing and storage.

    1. Evolutionary Biology
    2. Neuroscience
    Daniel Thiel, Luis Alfonso Yañez Guerra ... Gáspár Jékely
    Research Article

    Neuropeptides are ancient signaling molecules in animals but only few peptide receptors are known outside bilaterians. Cnidarians possess a large number of G protein-coupled receptors (GPCRs) – the most common receptors of bilaterian neuropeptides – but most of these remain orphan with no known ligands. We searched for neuropeptides in the sea anemone Nematostella vectensis and created a library of 64 peptides derived from 33 precursors. In a large-scale pharmacological screen with these peptides and 161 N. vectensis GPCRs, we identified 31 receptors specifically activated by 1 to 3 of 14 peptides. Mapping GPCR and neuropeptide expression to single-cell sequencing data revealed how cnidarian tissues are extensively connected by multilayer peptidergic networks. Phylogenetic analysis identified no direct orthology to bilaterian peptidergic systems and supports the independent expansion of neuropeptide signaling in cnidarians from a few ancestral peptide-receptor pairs.