Human pyramidal to interneuron synapses are mediated by multi-vesicular release and multiple docked vesicles
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
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.
Reviewing Editor
- Marlene Bartos, Albert-Ludwigs-Universität Freiburg, Germany
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.
Version history
- Received: May 25, 2016
- Accepted: August 15, 2016
- Accepted Manuscript published: August 18, 2016 (version 1)
- 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.
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