AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation
Open accessAbstract
The exocytosis of AMPA receptors is a key step in long-term potentiation (LTP), yet the timing and location of exocytosis and the signaling pathways involved in exocytosis during synaptic plasticity are not fully understood. Here we combine two-photon uncaging with two-photon imaging of a fluorescent label of surface AMPA receptors to monitor individual AMPA receptor exocytosis events near spines undergoing LTP. AMPA receptors that reached the stimulated spine came from a combination of preexisting surface receptors (70–90%) and newly exocytosed receptors (10–30%). We observed exocytosis in both the dendrite and spine under basal conditions. The rate of AMPA receptor exocytosis increased ∼5-fold during LTP induction and decayed to the basal level within ∼1 min, both in the stimulated spine and in the dendrite within ∼3 μm of the stimulated spine. AMPA receptors inserted in the spine were trapped in the spine in an activity-dependent manner. The activity-dependent exocytosis required the Ras-ERK pathway, but not CaMKII. Thus, diffusive Ras-ERK signaling presumably serves as an important means for signaling from synapses to dendritic shafts to recruit AMPA receptors into synapses during LTP.
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Rho signaling leads to local AMPA receptor integration in the dendrite.
“while Rho signaling leads to local AMPA receptor integration in the dendrite (Patterson et al., 2010)”
From Barriers in the brain: resolving dendritic spine morphology and compartmentalization (2014) · cites this paper as Patterson et al., 2010
The Results passage on signaling inhibitors reports that blocking Ras or ERK reduced the increase in AMPA receptor exocytosis in nearby dendrites. The Discussion likewise identifies Ras-ERK—not Rho—as the pathway involved. The paper supports local dendritic AMPA receptor exocytosis, but attributes its signaling dependence to a different pathway. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredBlocking postsynaptic exocytosis by a variety of means blocks LTP/sLTP.
“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 [250]
The results describing Fig. 2D report that tetanus toxin, which inhibits vesicle-dependent exocytosis, partially blocked structural plasticity. This supports a role for postsynaptic exocytosis in sLTP, but not the claim that blocking it fully blocks LTP/sLTP; the paper does not establish that result by a variety of means. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn most cases AMPARs are inserted via exocytosis into the dendritic shaft, some distance from the synapse.
“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 [250]
The Abstract and Results report AMPAR exocytosis in dendrites near stimulated spines, including sites about 2 μm away (Fig. 3B). But the paper also observes exocytosis directly in stimulated spines and does not establish that dendritic-shaft insertion occurs in most cases. (LLM, conf=0.84)
Experimental — accuracy not yet measuredLTP-inducing stimuli cause rapid addition of AMPARs to classical dendritic spines.
“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 [250]
By tagging AMPARs with a pH-sensitive tag (SEP-GluA1), insertion of AMPARs into the surface membrane can be directly visualized during LTP-inducing protocols.
“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 [250]
Recovery from bleaching spine SEP-GluA1 following glutamate uncaging shows a modest dependence on CaMKII, while single SEP-GluA1 exocytotic events during glutamate uncaging appear to be independent of CaMKII.
“Sixth, whereas the recovery from bleaching spine SEP-GluA1 following glutamate uncaging shows a modest dependence on CaMKII, single SEP-GluA1 exocytotic events during glutamate uncaging appear to be independent of CaMKII (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
Comparison of synaptic accumulation of SEP-GluA1 by glutamate uncaging, with and without prior bleaching of surface receptors, indicates that much of the accumulation is due to lateral diffusion and not exocytotic insertion of receptors.
“Fifth, a comparison of the synaptic accumulation of SEP-GluA1 by glutamate uncaging, with and without prior bleaching of surface receptors, indicates that much of the accumulation is due to lateral diffusion and not exocytotic insertion of receptors (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
CaMKII appears not to be required for AMPAR exocytotic events.
“but, as discussed, CaMKII appears not to be required for AMPAR exocytotic events (250).”
From Synaptic memory and CaMKII (2023) · cites this paper as [250]
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Self-citation
- Authors
- Patterson, M. A., Szatmari, E. M., & Yasuda, R.
- Affiliations
- Duke Medical Center (US)
- Department of Neurobiology and
- Howard Hughes Medical Institute (US)
- Corresponding author
- Yasuda, Ryohei
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-08-23
- Volume
- 107
- Issue
- 36
- Pages
- 15951-15956
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2936631
- OpenAlex
- W2014868528
- Cited by
- 259
- References
- 37
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 12 · 2023: 16 · 2022: 11 · 2021: 19 · 2020: 20 · 2019: 11 · 2018: 22 · 2017: 17 · 2016: 14 · 2015: 14 · 2014: 21 · 2013: 22 · 2012: 21
- FWCI
- 7.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Alzheimer's Association
- National Institute of Mental Health (R01MH080047)
- National Institute on Drug Abuse (R01DA027807)
- National Institute of Neurological Disorders and Stroke (R01NS068410)
- 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
- long-term potentiation, dendritic spines, Ras/ERK signaling, CaMKII, synaptic plasticity, two-photon uncaging, two-photon imaging
- MeSH terms
- Animals, Exocytosis, Fluorescent Dyes, Kinetics, Long-Term Potentiation, Receptors, AMPA, ras Proteins, Extracellular Signal-Regulated MAP Kinases, Rats
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