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Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation
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Synapses store information by long-lasting modifications of their structure and molecular composition, but the precise chronology of these changes has not been studied at single-synapse resolution in real time. Here we describe the spatiotemporal reorganization of postsynaptic substructures during long-term potentiation (LTP) at individual dendritic spines. Proteins translocated to the spine in four distinct patterns through three sequential phases. In the initial phase, the actin cytoskeleton was rapidly remodeled while active cofilin was massively transported to the spine. In the stabilization phase, cofilin formed a stable complex with F-actin, was persistently retained at the spine, and consolidated spine expansion. In contrast, the postsynaptic density (PSD) was independently remodeled, as PSD scaffolding proteins did not change their amount and localization until a late protein synthesis-dependent third phase. Our findings show how and when spine substructures are remodeled during LTP and explain why synaptic plasticity rules change over time.
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“Dendritic spine morphology and number are highly dynamic and variable56, which were reported to be correlated with memory formation.”
From Early developmental bisphenol-A exposure sex-independently impairs spatial memory by remodeling hippocampal dendritic architecture and synaptic transmission in rats (2016) · cites this paper as [6]
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“In contrast, changes in PSD are not proportionally induced during spine enlargement but occur after a delay of approximately 30 min12.”
From State-dependent diffusion of actin-depolymerizing factor/cofilin underlies the enlargement and shrinkage of dendritic spines (2016) · cites this paper as [12]
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“Recently, cofilin has been shown to accumulate during spine enlargement, and long-term spine enlargement was inhibited by shRNA-mediated cofilin knockdown12.”
From State-dependent diffusion of actin-depolymerizing factor/cofilin underlies the enlargement and shrinkage of dendritic spines (2016) · cites this paper as [12]
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“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 [56]
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“Both constitutively active and inactive-phosphomimetic cofilin mutants failed to resume long-term spine enlargement and the cofilin accumulation12.”
From State-dependent diffusion of actin-depolymerizing factor/cofilin underlies the enlargement and shrinkage of dendritic spines (2016) · cites this paper as [12]
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“Protein synthesis is also proposed to be required for “late” LTP (55–57) (see sect. 3.3).”
From Synaptic memory and CaMKII (2023) · cites this paper as [56]
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“Although there is no change in the number of PSD-95 molecules (56), saturating LTP results in a two- to threefold enhancement of the AMPAR EPSC, as does the expression of constitutively active CaMKII.”
From Synaptic memory and CaMKII (2023) · cites this paper as [56]
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“Actin is largely excluded from the core of the PSD (66, 322), and evidence suggests that, at least for the first hour, the changes in spine size are not accompanied by changes in the size of the PSD (56).”
From Synaptic memory and CaMKII (2023) · cites this paper as [56]
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Phosphoprofile reorganization of the actin binding protein Drebrin during long term depression
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Metadata
- Authors
- Bosch, M., Castro, J., Saneyoshi, T., Matsuno, H., Sur, M., & Hayashi, Y.
- Affiliations
- Massachusetts Institute of Technology (US)
- RIKEN Center for Brain Science (JP)
- Corresponding author
- Bosch, Miquel
- Hayashi, Yasunori
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-04
- Volume
- 82
- Issue
- 2
- Pages
- 444-459
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4281348
- OpenAlex
- W2024694517
- Cited by
- 637
- References
- 58
- Citations by year
- 2026: 28 · 2025: 52 · 2024: 54 · 2023: 54 · 2022: 46 · 2021: 71 · 2020: 70 · 2019: 61 · 2018: 46 · 2017: 51 · 2016: 50 · 2015: 36 · 2014: 18
- FWCI
- 23.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- Funders
- Japan Society for the Promotion of Science (22110006, 24650204, 26640020)
- National Institute on Drug Abuse (R01DA17310, R01DA017310)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- long-term potentiation, dendritic spines, postsynaptic density, actin cytoskeleton remodeling, cofilin, F-actin, synaptic plasticity, postsynaptic scaffolding proteins, protein translocation
- MeSH terms
- Animals, Animals, Newborn, Cells, Cultured, Hippocampus, Humans, Luminescent Proteins, Models, Biological, Nerve Tissue Proteins, Neurons, Organ Culture Techniques, Synapses, Transduction, Genetic, Long-Term Potentiation, Receptors, Neurotransmitter, Glutamic Acid, Dendritic Spines, Mice, Rats, Post-Synaptic Density
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