Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity
Abstract
The synapse is a highly organized cellular specialization whose structure and composition are reorganized, both positively and negatively, depending on the strength of input signals. The mechanisms orchestrating these changes are not well understood. A plausible locus for the reorganization of synapse components and structure is actin, because it serves as both cytoskeleton and scaffold for synapses and exists in a dynamic equilibrium between F-actin and G-actin that is modulated bidirectionally by cellular signaling. Using a new FRET-based imaging technique to monitor F-actin/G-actin equilibrium, we show here that tetanic stimulation causes a rapid, persistent shift of actin equilibrium toward F-actin in the dendritic spines of rat hippocampal neurons. This enlarges the spines and increases postsynaptic binding capacity. In contrast, prolonged low-frequency stimulation shifts the equilibrium toward G-actin, resulting in a loss of postsynaptic actin and of structure. This bidirectional regulation of actin is actively involved in protein assembly and disassembly and provides a substrate for bidirectional synaptic plasticity.
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Many synaptic proteins are remarkably dynamic, including AMPARs, NMDARs, CaMKII, and scaffolding proteins such as PSD-95.
“These studies show that many synaptic proteins are remarkably dynamic, including AMPARs (237, 249, 327, 328), NMDARs (329), CaMKII (330), and scaffolding proteins, such as PSD-95 (331).”
From Synaptic memory and CaMKII (2023) · cites this paper as [330]
Spine enlargement associated with LTP can be immediately induced by intensive stimulation of postsynaptic NMDA-sensitive glutamate receptors (the conventional protocol) in CA1 pyramidal neurons.
“The spine enlargement associated with LTP can be immediately induced by intensive stimulation of postsynaptic N-methyl-d-aspartate (NMDA)–sensitive glutamate receptors (the conventional protocol) in CA1 pyramidal neurons (3–5).”
From Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines (2008) · cites this paper as [4]
LTD is associated with the shrinkage and elimination of spines.
“whereas LTD is associated with the shrinkage and elimination of spines (Okamoto et al., 2004)”
From The E3 ubiquitin ligase IDOL regulates synaptic ApoER2 levels and is important for plasticity and learning (2017) · cites this paper as Okamoto et al., 2004
Rho GTPases play important roles in regulating the actin cytoskeleton, which is essential for spine-specific, long-term structural and functional plasticity.
“Rho GTPases may constitute such signalling, because they play important roles in regulating actin cytoskeleton3,16, which is essential for spine-specific, long-term structural and functional plasticity14,17.”
From Local, persistent activation of Rho GTPases during plasticity of single dendritic spines (2011) · cites this paper as [17]
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- Authors
- Okamoto, K.-I., Nagai, T., Miyawaki, A., & Hayashi, Y.
- Affiliations
- RIKEN (JP)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Hayashi, Yasunori
- Venue
- Nature Neuroscience
- Published
- 2004-09-07
- Volume
- 7
- Issue
- 10
- Pages
- 1104-1112
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2093807579
- Cited by
- 854
- References
- 12
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 23 · 2023: 36 · 2022: 23 · 2021: 34 · 2020: 36 · 2019: 30 · 2018: 43 · 2017: 43 · 2016: 42 · 2015: 33 · 2014: 66 · 2013: 48 · 2012: 42
- FWCI
- 14.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- actin dynamics, dendritic spines, bidirectional synaptic plasticity, tetanic stimulation, low-frequency stimulation, hippocampal neurons, FRET imaging, synaptic structure, cytoskeleton
- MeSH terms
- Actins, Animals, Brain, Electric Stimulation, Hippocampus, Actin Cytoskeleton, Synaptic Transmission, Neuronal Plasticity, Organ Culture Techniques, Protein Binding, Synaptic Membranes, Time Factors, Up-Regulation, Nonlinear Dynamics, Calcium-Calmodulin-Dependent Protein Kinases, Image Cytometry, Fluorescence Resonance Energy Transfer, NIH 3T3 Cells, Dendritic Spines, Mice, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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