Cited by 30Neuroscience and Neuropharmacology ResearchCellular transport and secretionMemory and Neural Mechanisms

Recruitment of release sites underlies chemical presynaptic potentiation at hippocampal mossy fiber boutons

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Orlando, Marta, Dvorzhak, Anton, Bruentgens, Felicitas, Maglione, Marta, Rost, Benjamin R., Sigrist, Stephan J., Breustedt, Jörg, Schmitz, Dietmar·2021·PLOS Biology

Published version of a preprint

Abstract

Synaptic plasticity is a cellular model for learning and memory. However, the expression mechanisms underlying presynaptic forms of plasticity are not well understood. Here, we investigate functional and structural correlates of presynaptic potentiation at large hippocampal mossy fiber boutons induced by the adenylyl cyclase activator forskolin. We performed 2-photon imaging of the genetically encoded glutamate sensor iGluu that revealed an increase in the surface area used for glutamate release at potentiated terminals. Time-gated stimulated emission depletion microscopy revealed no change in the coupling distance between P/Q-type calcium channels and release sites mapped by Munc13-1 cluster position. Finally, by high-pressure freezing and transmission electron microscopy analysis, we found a fast remodeling of synaptic ultrastructure at potentiated boutons: Synaptic vesicles dispersed in the terminal and accumulated at the active zones, while active zone density and synaptic complexity increased. We suggest that these rapid and early structural rearrangements might enable long-term increase in synaptic strength.

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Authors
Orlando, M., Dvorzhak, A., Bruentgens, F., Maglione, M., Rost, B. R., Sigrist, S. J., Breustedt, J., & Schmitz, D.
Affiliations
  • Humboldt-Universität zu Berlin (DE)
  • NeuroCure Cluster of Excellence (DE)
  • German Center for Neurodegenerative Diseases (DE)
  • Max Delbrück Center (DE)
Corresponding author
Schmitz, Dietmar
Venue
PLOS Biology
Published
2021-06-21
Volume
19
Issue
6
Pages
e3001149
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
OpenAlex
W3173499376
Cited by
30
References
68
Citations by year
2026: 4 · 2025: 3 · 2024: 8 · 2023: 9 · 2022: 6
FWCI
2.65
Type
journal article
Language
en
Open access
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DZNE Pub (submittedVersion, other-oa)
Funders
Deutsche Forschungsgemeinschaft (390688087, 327654276, 184695641, 431572356, 273915538, 365082554)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
presynaptic potentiation, hippocampus, synaptic plasticity, forskolin, adenylate cyclase, P/Q-type calcium channels, Munc13-1, synaptic vesicles, active zone, synaptic ultrastructure, glutamate release
MeSH terms
Animals, Colforsin, Male, Mice, Inbred C57BL, Synaptic Vesicles, Presynaptic Terminals, Neurotransmitter Agents, Glutamic Acid, Mossy Fibers, Hippocampal, Microscopy, Fluorescence, Multiphoton, Mice

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