The role of AMPAR lateral diffusion in memory
Open accessAbstract
The accumulation of AMPARs to synapses is a fundamental step in Long-term potentiation (LTP) of synaptic transmission, a well-established cellular correlate of learning and memory. The discovery of a sizeable and highly mobile population of extrasynaptic AMPARs - randomly scanning the synaptic surface under basal conditions - provided a conceptual framework for a simplified model: LTP can be induced by the capture, and hence accumulation, of laterally diffusing extrasynaptic AMPARs. Here, we review the evidence supporting a rate-limiting role of AMPAR lateral diffusion in LTP and as consequence, in learning and memory. We propose that there are "multiple solutions" for achieving the diffusional trapping of AMPAR during LTP, mainly mediated by the interaction between interchangeable AMPAR auxiliary subunits and cell-adhesion molecules containing PDZ-binding domains and synaptic scaffolds containing PDZ-domains. We believe that this molecular degeneracy in the diffusional trapping of AMPAR during LTP serve to ensure the robustness of this crucial step in the making of memories. All in all, the role of AMPAR lateral diffusion in LTP is not only a conceptual leap in our understanding of memory, but it might also hold the keys for the development of therapeutics against disorders associated with memory deficits such as Alzheimer's disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Digestion of HA with hyaluronidase modulates synaptic function by increasing AMPA receptor mobility and surface expression of NMDA receptors.
“Digestion of HA with hyaluronidase modulates synaptic function by increasing AMPA receptor mobility (reviewed in [50] and surface expression of NMDA receptors [35, 51].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [50]
Interfering with the surface diffusion of AMPARs by receptor cross-linking markedly impairs LTP.
“Consistent with this result is the finding that interfering with the surface diffusion of AMPARs by receptor cross-linking markedly impairs LTP (345–347).”
From Synaptic memory and CaMKII (2023) · cites this paper as [347]
Cites
Structural basis of long-term potentiation in single dendritic spines
Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. R., & Kasai, H. (2004) · Nature · doi:10.1038/nature02617 · Cited by 2,500 · see citing works
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · see citing works
Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms
Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000) · Nature · doi:10.1038/35050030 · Cited by 1,111 · see citing works
Recycling Endosomes Supply AMPA Receptors for LTP
Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., & Ehlers, M. D. (2004) · Science · doi:10.1126/science.1102026 · Cited by 730 · see citing works
A trans-synaptic nanocolumn aligns neurotransmitter release to receptors
Tang, A.-H., Chen, H., Li, T. P., Metzbower, S. R., MacGillavry, H. D., & Blanpied, T. A. (2016) · Nature · doi:10.1038/nature19058 · Cited by 677 · see citing works
Regulation of AMPA receptor trafficking and synaptic plasticity
Anggono, V., & Huganir, R. L. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.006 · Cited by 588 · see citing works
Regulation of AMPA receptor lateral movements
Borgdorff, A. J., & Choquet, D. (2002) · Nature · doi:10.1038/nature00780 · Cited by 542 · see citing works
Self-citationImpaired Spatial Learning after Saturation of Long-Term Potentiation
Moser, E. I., Krobert, K. A., Moser, M.-B., & Morris, R. G. M. (1998) · Science · doi:10.1126/science.281.5385.2038 · Cited by 505 · see citing works
AMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Makino, H., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.035 · Cited by 501 · see citing works
Emotion Enhances Learning via Norepinephrine Regulation of AMPA-Receptor Trafficking
Hu, H., Real, E., Takamiya, K., Kang, M.-G., Ledoux, J., Huganir, R. L., & Malinow, R. (2007) · Cell · doi:10.1016/j.cell.2007.09.017 · Cited by 496 · see citing works
Patterson, M. A., Szatmari, E. M., & Yasuda, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913875107 · Cited by 259 · see citing works
Regulation of AMPA receptor surface diffusion by PSD-95 slots
Opazo, P., Sainlos, M., & Choquet, D. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.010 · Cited by 234 · see citing works
Self-citationA three-step model for the synaptic recruitment of AMPA receptors
Opazo, P., & Choquet, D. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.08.014 · Cited by 190 · see citing works
Self-citationChang, J.-Y., Parra-Bueno, P., Laviv, T., Szatmari, E. M., Lee, S.-J. R., & Yasuda, R. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.041 · Cited by 161 · see citing works
CaMKII activation persistently segregates postsynaptic proteins via liquid phase separation
Hosokawa, T., Liu, P.-W., Cai, Q., Ferreira, J. S., Levet, F., Butler, C., Sibarita, J.-B., Choquet, D., Groc, L., Hosy, E., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00843-3 · Cited by 146 · see citing works
Self-citationPostsynaptic Complexin Controls AMPA Receptor Exocytosis during LTP
Ahmad, M., Polepalli, J. S., Goswami, D., Yang, X., Kaeser-Woo, Y. J., Südhof, T. C., & Malenka, R. C. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.020 · Cited by 133 · see citing works
Synaptic transmission and plasticity require AMPA receptor anchoring via its N-terminal domain
Watson, J. F., Ho, H., & Greger, I. H. (2017) · eLife · doi:10.7554/elife.23024 · Cited by 117 · see citing works
Sheng, N., Bemben, M. A., Díaz-Alonso, J., Tao, W., Shi, Y. S., & Nicoll, R. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800719115 · Cited by 65 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The extracellular matrix and perineuronal nets in memory
Fawcett, J. W., Fyhn, M., Jendelova, P., Kwok, J. C. F., Ruzicka, J., & Sorg, B. A. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01634-3 · Cited by 169 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“Consistent with this result is the fi nding that interfering with the surface diffusion of AMPARs by receptor cross-linking markedly impairs LTP (345 – 347).”
Result
- Authors
- Choquet, D., & Opazo, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- The University of Queensland (AU)
- Corresponding author
- Choquet, Daniel
- Opazo, Patricio
- Venue
- Seminars in Cell & Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2022-05
- Volume
- 125
- Pages
- 76-83
- ISSN
- 1084-9521 (ISSN-L)
- OpenAlex
- W4210270532
- Cited by
- 31
- References
- 18
- Citations by year
- 2026: 8 · 2025: 8 · 2024: 7 · 2023: 6 · 2022: 2
- FWCI
- 0.82
- 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/ (am, 332 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
- Seminars in Cell and Developmental Biology (acceptedVersion)
- PubMed (publishedVersion)
- 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
- AMPA receptors, lateral diffusion, long-term potentiation, synaptic plasticity, learning and memory, PDZ-binding domain, adhesion molecules, synaptic scaffolds, Alzheimer's disease, memory impairment
- MeSH terms
- Diffusion, Synaptic Transmission, Synapses, Long-Term Potentiation, Receptors, AMPA
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
