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Open AccessArticle

Synaptic Organization of the Human Temporal Lobe Neocortex as Revealed by High-Resolution Transmission, Focused Ion Beam Scanning, and Electron Microscopic Tomography

1
Institute of Neuroscience and Medicine INM-10, Research Centre Jülich GmbH, Leo-Brandt Str., 52425 Jülich, Germany
2
Imaging Center Essen (IMCES), Electron Microscopy Unit (EMU), Medical Faculty of the University of Duisburg-Essen, Hufelandstr. 55, 45147 Essen, Germany
3
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty/RWTH University Hospital Aachen, Pauwelsstr. 30, 52074 Aachen, Germany
4
JARA Translational Brain Medicine, Jülich/Aachen, Germany
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Both authors equally share senior authorship.
Int. J. Mol. Sci. 2020, 21(15), 5558; https://doi.org/10.3390/ijms21155558
Received: 2 July 2020 / Revised: 27 July 2020 / Accepted: 29 July 2020 / Published: 3 August 2020
(This article belongs to the Special Issue Molecular Structure and Function of Synapses)
Modern electron microscopy (EM) such as fine-scale transmission EM, focused ion beam scanning EM, and EM tomography have enormously improved our knowledge about the synaptic organization of the normal, developmental, and pathologically altered brain. In contrast to various animal species, comparably little is known about these structures in the human brain. Non-epileptic neocortical access tissue from epilepsy surgery was used to generate quantitative 3D models of synapses. Beside the overall geometry, the number, size, and shape of active zones and of the three functionally defined pools of synaptic vesicles representing morphological correlates for synaptic transmission and plasticity were quantified. EM tomography further allowed new insights in the morphological organization and size of the functionally defined readily releasable pool. Beside similarities, human synaptic boutons, although comparably small (approximately 5 µm), differed substantially in several structural parameters, such as the shape and size of active zones, which were on average 2 to 3-fold larger than in experimental animals. The total pool of synaptic vesicles exceeded that in experimental animals by approximately 2 to 3-fold, in particular the readily releasable and recycling pool by approximately 2 to 5-fold, although these pools seemed to be layer-specifically organized. Taken together, synaptic boutons in the human temporal lobe neocortex represent unique entities perfectly adapted to the “job” they have to fulfill in the circuitry in which they are embedded. Furthermore, the quantitative 3D models of synaptic boutons are useful to explain and even predict the functional properties of synaptic connections in the human neocortex. View Full-Text
Keywords: human temporal lobe neocortex; synaptic boutons; active zones; synaptic vesicles; transmission and focused ion beam scanning EM; EM tomography; quantitative three-dimensional models of synaptic boutons human temporal lobe neocortex; synaptic boutons; active zones; synaptic vesicles; transmission and focused ion beam scanning EM; EM tomography; quantitative three-dimensional models of synaptic boutons
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MDPI and ACS Style

Rollenhagen, A.; Walkenfort, B.; Yakoubi, R.; Klauke, S.A.; Schmuhl-Giesen, S.F.; Heinen-Weiler, J.; Voortmann, S.; Marshallsay, B.; Palaz, T.; Holz, U.; Hasenberg, M.; Lübke, J.H.R. Synaptic Organization of the Human Temporal Lobe Neocortex as Revealed by High-Resolution Transmission, Focused Ion Beam Scanning, and Electron Microscopic Tomography. Int. J. Mol. Sci. 2020, 21, 5558. https://doi.org/10.3390/ijms21155558

AMA Style

Rollenhagen A, Walkenfort B, Yakoubi R, Klauke SA, Schmuhl-Giesen SF, Heinen-Weiler J, Voortmann S, Marshallsay B, Palaz T, Holz U, Hasenberg M, Lübke JHR. Synaptic Organization of the Human Temporal Lobe Neocortex as Revealed by High-Resolution Transmission, Focused Ion Beam Scanning, and Electron Microscopic Tomography. International Journal of Molecular Sciences. 2020; 21(15):5558. https://doi.org/10.3390/ijms21155558

Chicago/Turabian Style

Rollenhagen, Astrid; Walkenfort, Bernd; Yakoubi, Rachida; Klauke, Sarah A.; Schmuhl-Giesen, Sandra F.; Heinen-Weiler, Jacqueline; Voortmann, Sylvia; Marshallsay, Brigitte; Palaz, Tayfun; Holz, Ulrike; Hasenberg, Mike; Lübke, Joachim H.R. 2020. "Synaptic Organization of the Human Temporal Lobe Neocortex as Revealed by High-Resolution Transmission, Focused Ion Beam Scanning, and Electron Microscopic Tomography" Int. J. Mol. Sci. 21, no. 15: 5558. https://doi.org/10.3390/ijms21155558

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