Human pyramidal to interneuron synapses are mediated by multi-vesicular release and multiple docked vesicles

  1. Gábor Molnár
  2. Márton Rózsa
  3. Judith Baka
  4. Noémi Holderith
  5. Pál Barzó
  6. Zoltan Nusser
  7. Gábor Tamás  Is a corresponding author
  1. University of Szeged, Hungary
  2. Hungarian Academy of Sciences, Hungary

Abstract

Classic theories link cognitive abilities to synaptic properties and human-specific biophysical features of synapses might contribute to the unparalleled performance of the human cerebral cortex. Paired recordings and multiple probability fluctuation analysis revealed similar quantal sizes, but 4-times more functional release sites in human pyramidal cell to fast-spiking interneuron connections compared to rats. These connections were mediated on average by three synaptic contacts in both species. Each presynaptic active zone (AZ) contains 6.2 release sites in human, but only 1.6 in rats. Electron microscopy (EM) and EM tomography showed that an AZ harbors 4 docked vesicles in human, but only a single one in rats. Consequently, a Katz's functional release site occupies ~0.012 μm2 in the human presynaptic AZ and ~0.025 μm2 in the rat. Our results reveal a robust difference in the biophysical properties of a well-defined synaptic connection of the cortical microcircuit of human and rodents.

Article and author information

Author details

  1. Gábor Molnár

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  2. Márton Rózsa

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  3. Judith Baka

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  4. Noémi Holderith

    Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0024-3980
  5. Pál Barzó

    Department of Neurosurgery, University of Szeged, Szeged, Hungary
    Competing interests
    The authors declare that no competing interests exist.
  6. Zoltan Nusser

    Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7004-4111
  7. Gábor Tamás

    MTA-SZTE Research Group for Cortical Microcircuits, University of Szeged, Szeged, Hungary
    For correspondence
    gtamas@bio.u-szeged.hu
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (INTERIMPACT)

  • Gábor Tamás

European Research Council (293681)

  • Zoltan Nusser

Magyar Tudományos Akadémia (MTA-SZTE Agykergi Neuronhalozatok Kutatocsoport)

  • Gábor Tamás

Magyar Tudományos Akadémia (Lendület, LP2012-29)

  • Zoltan Nusser

Magyar Tudományos Akadémia (Janos Bolyai Scholarship)

  • Noémi Holderith

Nemzeti Kutatási és Technológiai Hivatal (VKSZ_14-1-2015-0155)

  • Gábor Tamás

Nemzeti Agykutatasi Program (NAP-A)

  • Gábor Molnár

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 experimental protocols and procedures were performed according to the European Communities Council Directives of 1986 (86/609/EEC) and 2003 (2003/65/CE) for animal research and were approved by the Ethics Committee of the University of Szeged.

Human subjects: All procedures were performed according to the Declaration of Helsinki with the approval of the University of Szeged Ethical Committee. Informed consent, and consent to publish, was obtained from patients. The permit number for our human experiments is 75/2004 issued by the Human Investigation Review Board of the University of Szeged.

Copyright

© 2016, Molnár 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. Gábor Molnár
  2. Márton Rózsa
  3. Judith Baka
  4. Noémi Holderith
  5. Pál Barzó
  6. Zoltan Nusser
  7. Gábor Tamás
(2016)
Human pyramidal to interneuron synapses are mediated by multi-vesicular release and multiple docked vesicles
eLife 5:e18167.
https://doi.org/10.7554/eLife.18167

Share this article

https://doi.org/10.7554/eLife.18167

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