Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing.

Shanting Zhao, Daniel Studer, Xuejun Chai, Werner Graber, Nils Brose, Sigrun Nestel, Christina Young, E. Patricia Rodriguez, Kurt Saetzler, Michael Frotscher

Research output: Contribution to journalArticle

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Abstract

Despite recent progress in fluorescence microscopy techniques, electron microscopy (EM) is still superior in the simultaneous analysis of all tissue components at high resolution. However, it is unclear to what extent conventional fixation for EM using aldehydes results in tissue alteration. Here, we made an attempt to minimize tissue alteration by using rapid high-pressure freezing (HPF) of hippocampal slice cultures. We used this approach to monitor fine-structural changes at hippocampal mossy fiber synapses associated with chemically induced long-term potentiation (LTP). Synaptic plasticity in LTP has been known to involve structural changes at synapses including reorganization of the actin cytoskeleton and de novo formation of spines. While LTP-induced formation and growth of postsynaptic spines have been reported, little is known about associated structural changes in presynaptic boutons. Mossy fiber synapses are assumed to exhibit presynaptic LTP expression and are easily identified by EM. In slice cultures from wild-type mice, we found that chemical LTP increased the length of the presynaptic membrane of mossy fiber boutons, associated with a de novo formation of small spines and an increase in the number of active zones. Of note, these changes were not observed in slice cultures from Munc13-1 knock-out mutants exhibiting defective vesicle priming. These findings show that activation of hippocampal mossy fibers induces pre- and postsynaptic structural changes at mossy fiber synapses that can be monitored by EM. J. Comp. Neurol., 2012. © 2012 Wiley-Liss, Inc.
LanguageEnglish
Pages2340-2351
JournalJournal of Comparative Neurology
Volume520
Issue number11
DOIs
Publication statusPublished - Aug 2012

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Hippocampal Mossy Fibers
Long-Term Potentiation
Synapses
Freezing
Electron Microscopy
Pressure
Spine
Neuronal Plasticity
Actin Cytoskeleton
Fluorescence Microscopy
Aldehydes
Membranes
Growth

Cite this

Zhao, S., Studer, D., Chai, X., Graber, W., Brose, N., Nestel, S., ... Frotscher, M. (2012). Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. Journal of Comparative Neurology, 520(11), 2340-2351. https://doi.org/10.1002/cne.23040
Zhao, Shanting ; Studer, Daniel ; Chai, Xuejun ; Graber, Werner ; Brose, Nils ; Nestel, Sigrun ; Young, Christina ; Rodriguez, E. Patricia ; Saetzler, Kurt ; Frotscher, Michael. / Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. In: Journal of Comparative Neurology. 2012 ; Vol. 520, No. 11. pp. 2340-2351.
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Zhao, S, Studer, D, Chai, X, Graber, W, Brose, N, Nestel, S, Young, C, Rodriguez, EP, Saetzler, K & Frotscher, M 2012, 'Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing.', Journal of Comparative Neurology, vol. 520, no. 11, pp. 2340-2351. https://doi.org/10.1002/cne.23040

Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. / Zhao, Shanting; Studer, Daniel; Chai, Xuejun; Graber, Werner; Brose, Nils; Nestel, Sigrun; Young, Christina; Rodriguez, E. Patricia; Saetzler, Kurt; Frotscher, Michael.

In: Journal of Comparative Neurology, Vol. 520, No. 11, 08.2012, p. 2340-2351.

Research output: Contribution to journalArticle

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T1 - Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing.

AU - Zhao, Shanting

AU - Studer, Daniel

AU - Chai, Xuejun

AU - Graber, Werner

AU - Brose, Nils

AU - Nestel, Sigrun

AU - Young, Christina

AU - Rodriguez, E. Patricia

AU - Saetzler, Kurt

AU - Frotscher, Michael

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N2 - Despite recent progress in fluorescence microscopy techniques, electron microscopy (EM) is still superior in the simultaneous analysis of all tissue components at high resolution. However, it is unclear to what extent conventional fixation for EM using aldehydes results in tissue alteration. Here, we made an attempt to minimize tissue alteration by using rapid high-pressure freezing (HPF) of hippocampal slice cultures. We used this approach to monitor fine-structural changes at hippocampal mossy fiber synapses associated with chemically induced long-term potentiation (LTP). Synaptic plasticity in LTP has been known to involve structural changes at synapses including reorganization of the actin cytoskeleton and de novo formation of spines. While LTP-induced formation and growth of postsynaptic spines have been reported, little is known about associated structural changes in presynaptic boutons. Mossy fiber synapses are assumed to exhibit presynaptic LTP expression and are easily identified by EM. In slice cultures from wild-type mice, we found that chemical LTP increased the length of the presynaptic membrane of mossy fiber boutons, associated with a de novo formation of small spines and an increase in the number of active zones. Of note, these changes were not observed in slice cultures from Munc13-1 knock-out mutants exhibiting defective vesicle priming. These findings show that activation of hippocampal mossy fibers induces pre- and postsynaptic structural changes at mossy fiber synapses that can be monitored by EM. J. Comp. Neurol., 2012. © 2012 Wiley-Liss, Inc.

AB - Despite recent progress in fluorescence microscopy techniques, electron microscopy (EM) is still superior in the simultaneous analysis of all tissue components at high resolution. However, it is unclear to what extent conventional fixation for EM using aldehydes results in tissue alteration. Here, we made an attempt to minimize tissue alteration by using rapid high-pressure freezing (HPF) of hippocampal slice cultures. We used this approach to monitor fine-structural changes at hippocampal mossy fiber synapses associated with chemically induced long-term potentiation (LTP). Synaptic plasticity in LTP has been known to involve structural changes at synapses including reorganization of the actin cytoskeleton and de novo formation of spines. While LTP-induced formation and growth of postsynaptic spines have been reported, little is known about associated structural changes in presynaptic boutons. Mossy fiber synapses are assumed to exhibit presynaptic LTP expression and are easily identified by EM. In slice cultures from wild-type mice, we found that chemical LTP increased the length of the presynaptic membrane of mossy fiber boutons, associated with a de novo formation of small spines and an increase in the number of active zones. Of note, these changes were not observed in slice cultures from Munc13-1 knock-out mutants exhibiting defective vesicle priming. These findings show that activation of hippocampal mossy fibers induces pre- and postsynaptic structural changes at mossy fiber synapses that can be monitored by EM. J. Comp. Neurol., 2012. © 2012 Wiley-Liss, Inc.

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