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Structural plasticity of spines at giant mossy fiber synapses
The granule cells of the dentate gyrus give rise to thin unmyelinated axons, the mossy fibers. They form giant presynaptic boutons impinging on large complex spines on the proximal dendritic portions of hilar mossy cells and CA3 pyramidal neurons. While these anatomical characteristics have been kno...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3524460/ https://www.ncbi.nlm.nih.gov/pubmed/23264762 http://dx.doi.org/10.3389/fncir.2012.00103 |
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author | Zhao, Shanting Studer, Daniel Chai, Xuejun Graber, Werner Brose, Nils Nestel, Sigrun Young, Christina Rodriguez, E. Patricia Saetzler, Kurt Frotscher, Michael |
author_facet | Zhao, Shanting Studer, Daniel Chai, Xuejun Graber, Werner Brose, Nils Nestel, Sigrun Young, Christina Rodriguez, E. Patricia Saetzler, Kurt Frotscher, Michael |
author_sort | Zhao, Shanting |
collection | PubMed |
description | The granule cells of the dentate gyrus give rise to thin unmyelinated axons, the mossy fibers. They form giant presynaptic boutons impinging on large complex spines on the proximal dendritic portions of hilar mossy cells and CA3 pyramidal neurons. While these anatomical characteristics have been known for some time, it remained unclear whether functional changes at mossy fiber synapses such as long-term potentiation (LTP) are associated with structural changes. Since subtle structural changes may escape a fine-structural analysis when the tissue is fixed by using aldehydes and is dehydrated in ethanol, rapid high-pressure freezing (HPF) of the tissue was applied. Slice cultures of hippocampus were prepared and incubated in vitro for 2 weeks. Then, chemical LTP (cLTP) was induced by the application of 25 mM tetraethylammonium (TEA) for 10 min. Whole-cell patch-clamp recordings from CA3 pyramidal neurons revealed a highly significant potentiation of mossy fiber synapses when compared to control conditions before the application of TEA. Next, the slice cultures were subjected to HPF, cryosubstitution, and embedding in Epon for a fine-structural analysis. When compared to control tissue, we noticed a significant decrease of synaptic vesicles in mossy fiber boutons and a concomitant increase in the length of the presynaptic membrane. On the postsynaptic side, we observed the formation of small, finger-like protrusions, emanating from the large complex spines. These short protrusions gave rise to active zones that were shorter than those normally found on the thorny excrescences. However, the total number of active zones was significantly increased. Of note, none of these cLTP-induced structural changes was observed in slice cultures from Munc13-1 deficient mouse mutants showing severely impaired vesicle priming and docking. In conclusion, application of HPF allowed us to monitor cLTP-induced structural reorganization of mossy fiber synapses. |
format | Online Article Text |
id | pubmed-3524460 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-35244602012-12-21 Structural plasticity of spines at giant mossy fiber synapses Zhao, Shanting Studer, Daniel Chai, Xuejun Graber, Werner Brose, Nils Nestel, Sigrun Young, Christina Rodriguez, E. Patricia Saetzler, Kurt Frotscher, Michael Front Neural Circuits Neuroscience The granule cells of the dentate gyrus give rise to thin unmyelinated axons, the mossy fibers. They form giant presynaptic boutons impinging on large complex spines on the proximal dendritic portions of hilar mossy cells and CA3 pyramidal neurons. While these anatomical characteristics have been known for some time, it remained unclear whether functional changes at mossy fiber synapses such as long-term potentiation (LTP) are associated with structural changes. Since subtle structural changes may escape a fine-structural analysis when the tissue is fixed by using aldehydes and is dehydrated in ethanol, rapid high-pressure freezing (HPF) of the tissue was applied. Slice cultures of hippocampus were prepared and incubated in vitro for 2 weeks. Then, chemical LTP (cLTP) was induced by the application of 25 mM tetraethylammonium (TEA) for 10 min. Whole-cell patch-clamp recordings from CA3 pyramidal neurons revealed a highly significant potentiation of mossy fiber synapses when compared to control conditions before the application of TEA. Next, the slice cultures were subjected to HPF, cryosubstitution, and embedding in Epon for a fine-structural analysis. When compared to control tissue, we noticed a significant decrease of synaptic vesicles in mossy fiber boutons and a concomitant increase in the length of the presynaptic membrane. On the postsynaptic side, we observed the formation of small, finger-like protrusions, emanating from the large complex spines. These short protrusions gave rise to active zones that were shorter than those normally found on the thorny excrescences. However, the total number of active zones was significantly increased. Of note, none of these cLTP-induced structural changes was observed in slice cultures from Munc13-1 deficient mouse mutants showing severely impaired vesicle priming and docking. In conclusion, application of HPF allowed us to monitor cLTP-induced structural reorganization of mossy fiber synapses. Frontiers Media S.A. 2012-12-18 /pmc/articles/PMC3524460/ /pubmed/23264762 http://dx.doi.org/10.3389/fncir.2012.00103 Text en Copyright © 2012 Zhao, Studer, Chai, Graber, Brose, Nestel, Young, Rodriguez, Saetzler and Frotscher. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc. |
spellingShingle | Neuroscience Zhao, Shanting Studer, Daniel Chai, Xuejun Graber, Werner Brose, Nils Nestel, Sigrun Young, Christina Rodriguez, E. Patricia Saetzler, Kurt Frotscher, Michael Structural plasticity of spines at giant mossy fiber synapses |
title | Structural plasticity of spines at giant mossy fiber synapses |
title_full | Structural plasticity of spines at giant mossy fiber synapses |
title_fullStr | Structural plasticity of spines at giant mossy fiber synapses |
title_full_unstemmed | Structural plasticity of spines at giant mossy fiber synapses |
title_short | Structural plasticity of spines at giant mossy fiber synapses |
title_sort | structural plasticity of spines at giant mossy fiber synapses |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3524460/ https://www.ncbi.nlm.nih.gov/pubmed/23264762 http://dx.doi.org/10.3389/fncir.2012.00103 |
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