1. Neuroscience
Download icon

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
Short Report
  • Cited 33
  • Annotations
Cite this article as: eLife 2016;5:e18167 doi: 10.7554/eLife.18167

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.

Reviewing Editor

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

Publication history

  1. Received: May 25, 2016
  2. Accepted: August 15, 2016
  3. Accepted Manuscript published: August 18, 2016 (version 1)
  4. Version of Record published: August 25, 2016 (version 2)

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.

Metrics

  • 33
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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)

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

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

Further reading

    1. Neuroscience
    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience
    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.