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AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Open accessAbstract
The regulated trafficking of AMPA receptors (AMPARs) to synapses is thought to underlie the enhanced transmission in long-term potentiation (LTP), a cellular model of memory. However, there is controversy regarding the nonsynaptic site, either on the surface or intracellularly, from which AMPARs move into synapses during LTP. Using recombinant surface-fluorescent receptors in organotypic rat hippocampal slices, we show that the majority of AMPARs incorporated into synapses during LTP is from lateral diffusion of spine surface receptors containing GluR1, an AMPAR subunit. Following synaptic potentiation, AMPARs in intracellular pools containing GluR1 are driven to the surface primarily on dendrites. These exocytosed receptors likely serve to replenish the local extrasynaptic pool available for subsequent bouts of plasticity. These results clarify the role of intracellular and surface AMPARs during synaptic plasticity.
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“Numerous studies have shown that blocking postsynaptic exocytosis by a variety of means blocks LTP/sLTP (195, 249, 250, 332–338).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
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“Surface localized AMPARs are supplied by exocytosis from pools of intracellular receptors contained within endosomes (Lin et al., 2009, Makino and Malinow, 2009).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Makino and Malinow, 2009
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“Large packets of GluA1 are inserted into the dendritic shaft from intracellular recycling endosomes, containing an estimated fifty GluA1-containing receptors, in an activity-dependent manner (Lin et al., 2009, Makino and Malinow, 2009).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Makino and Malinow, 2009
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“Combining SEP-GluA1 photobleaching experiments with glutamate uncaging in organotypic slices revealed that synaptic potentiation of AMPA receptors is achieved by restricting their diffusion out of the synaptic membrane (Makino and Malinow, 2009).”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Makino and Malinow, 2009
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“These synapses contain AMPARs, but LTP-inducing stimuli cause a rapid addition of AMPARs to the synapse (246–250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
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“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 [249]
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“By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), the insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols (249, 250, 335, 337, 338, 340).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
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“Fourth, in most cases the AMPARs are inserted via exocytosis into the dendritic shaft, some distance from the synapse (220, 249, 250, 337).”
From Synaptic memory and CaMKII (2023) · cites this paper as [249]
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“This form of plasticity shares many properties with Schaffer collateral LTP, including dependence on N-methyl-d-aspartate receptors (NMDARs), Rho GTPase signaling, Ca2+/calmodulin-dependent protein kinase II (CaMKII) phosphorylation, F-actin polymerization and synaptic AMPAR insertion (20–24).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [23]
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Citations
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Metadata
- Authors
- Makino, H., & Malinow, R.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Corresponding author
- Malinow, Roberto
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2009-11
- Volume
- 64
- Issue
- 3
- Pages
- 381-390
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2999463
- OpenAlex
- W2058113433
- Cited by
- 501
- References
- 41
- Citations by year
- 2026: 16 · 2025: 18 · 2024: 20 · 2023: 12 · 2022: 22 · 2021: 38 · 2020: 39 · 2019: 27 · 2018: 34 · 2017: 35 · 2016: 26 · 2015: 22 · 2014: 41 · 2013: 52 · 2012: 38
- FWCI
- 13.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1354 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- National Institute on Aging (R01AG032132)
- National Institute of Mental Health (R01MH049159, R37MH049159)
- 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
- AMPA receptors, long-term potentiation, receptor trafficking, synaptic plasticity, GluR1, lateral diffusion, exocytosis, hippocampus, memory
- MeSH terms
- Animals, Cell Membrane, Dendrites, Diffusion, Exocytosis, Fluorescence, Hippocampus, Neurons, Synapses, Video Recording, Long-Term Potentiation, Pyramidal Cells, Receptors, AMPA, Intracellular Space, Dendritic Spines, Rats, CA1 Region, Hippocampal, In Vitro Techniques
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