Rapid Ultrastructural Changes in the PSD and Surrounding Membrane after Induction of Structural LTP in Single Dendritic Spines
Open accessAbstract
The structural plasticity of dendritic spines is considered to be an important basis of synaptic plasticity, learning, and memory. Here, we induced input-specific structural LTP (sLTP) in single dendritic spines in organotypic hippocampal slices from mice of either sex and performed ultrastructural analyses of the spines using efficient correlative light and electron microscopy. We observed reorganization of the PSD nanostructure, such as perforation and segmentation, at 2–3, 20, and 120 min after sLTP induction. In addition, PSD and nonsynaptic axon–spine interface (nsASI) membrane expanded unevenly during sLTP. Specifically, the PSD area showed a transient increase at 2–3 min after sLTP induction. The PSD growth was to a degree less than spine volume growth at 2–3 min and 20 min after sLTP induction but became similar at 120 min. On the other hand, the nsASI area showed a profound and lasting expansion, to a degree similar to spine volume growth throughout the process. These rapid ultrastructural changes in PSD and surrounding membrane may contribute to rapid electrophysiological plasticity during sLTP. SIGNIFICANCE STATEMENT To understand the ultrastructural changes during synaptic plasticity, it is desired to efficiently image single dendritic spines that underwent structural plasticity in electron microscopy. We induced structural long-term potentiation (sLTP) in single dendritic spines by two-photon glutamate uncaging. We then identified the same spines at different phases of sLTP and performed ultrastructural analysis by using an efficient correlative light and electron microscopy method. We found that postsynaptic density undergoes dramatic modification in its structural complexity immediately after sLTP induction. Meanwhile, the nonsynaptic axon–spine interface area shows a rapid and sustained increase throughout sLTP. Our results indicate that the uneven modification of synaptic and nonsynaptic postsynaptic membrane might contribute to rapid electrophysiological plasticity during sLTP.
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LTP is associated with a long-lasting increase in spine size, including a late increase in the size of the PSD and a slow increase in the size of the presynaptic bouton.
“LTP is associated with a long-lasting increase in spine size (247, 248), including a late increase in the size of the PSD (56, 213, 414, 415) and additionally a slow increase in the size of the presynaptic bouton (213, 414).”
From Synaptic memory and CaMKII (2023) · cites this paper as [415]
The Introduction and PSD-reorganization section describe spine enlargement after LTP and PSD growth that lags spine-volume growth by hours. The Discussion mentions presynaptic bouton volume change, but does not establish the claimed slow increase in bouton size. The paper also reports that late-phase spine volume was not significantly different from controls. (LLM, conf=0.86)
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Cites
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Self-citationAMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
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“…activity can withstand protein turnover to structural changes associated with LTP. LTP is associated with a long-lasting increase in spine size (247, 248), including a late increase in the size of the PSD (56, 213, 414, 415) and additionally a slow increase in the size of the bouton (213, 414).”
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- Authors
- Sun, Y., Smirnov, M., Kamasawa, N., & Yasuda, R.
- Affiliations
- Max Planck Florida Institute for Neuroscience (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2021-07-15
- Volume
- 41
- Issue
- 33
- Pages
- 7003-7014
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC8372018
- OpenAlex
- W3177926500
- Cited by
- 51
- References
- 14
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 11 · 2023: 13 · 2022: 10 · 2021: 1
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Brain Research Foundation
- National Institutes of Health
- National Institute of Mental Health (R01MH080047)
- National Institute of Neurological Disorders and Stroke (DP1NS096787, R35NS116804)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Electrical and Electronic Engineering › Advanced Memory and Neural Computing
- Keywords
- dendritic spines, postsynaptic density, ultrastructural changes, synaptic plasticity, organotypic hippocampal slices, correlative light and electron microscopy
- MeSH terms
- Animals, Axons, Cell Membrane, Female, Glutamates, Hippocampus, Image Processing, Computer-Assisted, Indoles, Male, Microscopy, Electron, Scanning, Photochemistry, Long-Term Potentiation, Biolistics, Dendritic Spines, Mice, Post-Synaptic Density
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