Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation
Open accessAbstract
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 variable, and correlated with memory formation.
“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]
The Introduction (page unavailable) says spines enlarge during long-term potentiation and shrink during long-term depression, supporting dynamic morphology. It also describes synaptic structural change as a basis of learning and memory, but does not establish a correlation between spine number and memory formation or show that spine number is highly dynamic. (LLM, conf=0.86)
Experimental — accuracy not yet measuredChanges in PSD are not proportionally induced during spine enlargement but occur after a delay of approximately 30 min.
“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]
The Results section on PSD growth reports that Homer1b and Shank1b did not increase during the first 45 minutes after sLTP induction and began increasing at about 60 minutes. This supports delayed, non-proportional PSD changes during initial spine enlargement, but not a delay of approximately 30 minutes. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCofilin accumulates during spine enlargement, and long-term spine enlargement is inhibited by shRNA-mediated cofilin knockdown.
“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]
The Results section reports that cofilin accumulated after sLTP induction and that spine enlargement was reduced at 20–30 minutes when shRNAs knocked down both cofilin and ADF. Crucially, cofilin-targeting shRNA alone did not produce that reduction, so the claim overstates what cofilin knockdown by itself achieved. (LLM, conf=0.89)
Experimental — accuracy not yet measuredLTP 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 [56]
The Results section reports delayed PSD enlargement after structural LTP, and the Discussion describes PSD remodeling beginning about 60 minutes after induction. Our copy also reports persistent spine enlargement, but the passages located for presynaptic bouton growth do not report a slow increase in bouton size. That part of the claim is unsupported by this source. (LLM, conf=0.87)
Experimental — accuracy not yet measuredBoth constitutively active and inactive-phosphomimetic cofilin mutants failed to resume long-term spine enlargement and cofilin accumulation.
“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]
Protein synthesis is proposed to be required for "late" LTP.
“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]
Although there is no change in the number of PSD-95 molecules, saturating LTP results in a two- to threefold enhancement of the AMPAR EPSC, as does the expression of constitutively active CaMKII.
“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]
Actin is largely excluded from the core of the PSD, 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.
“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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- 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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