The Cell Biology of Synaptic Plasticity
Open accessAbstract
Synaptic plasticity is the experience-dependent change in connectivity between neurons that is believed to underlie learning and memory. Here, we discuss the cellular and molecular processes that are altered when a neuron responds to external stimuli, and how these alterations lead to an increase or decrease in synaptic connectivity. Modification of synaptic components and changes in gene expression are necessary for many forms of plasticity. We focus on excitatory neurons in the mammalian hippocampus, one of the best-studied model systems of learning-related plasticity.
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Synaptic strength moderates neural signaling between cells over an extended period, underlying circuit functionality.
“Synaptic strength moderates neural signaling between cells over an extended period175, 176, underlying circuit functionality.”
From Dysregulation of adult hippocampal neuroplasticity in major depression: Pathogenesis and therapeutic implications (2022) · cites this paper as [175]
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Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J., & Selkoe, D. J. (2002) · Nature · doi:10.1038/416535a · Cited by 4,291 · see citing works
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917 · see citing works
Experience-dependent structural synaptic plasticity in the mammalian brain
Holtmaat, A., & Svoboda, K. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2699 · Cited by 1,934 · see citing works
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860 · see citing works
Astrocyte-Neuron Lactate Transport Is Required for Long-Term Memory Formation
Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., & Alberini, C. M. (2011) · Cell · doi:10.1016/j.cell.2011.02.018 · Cited by 1,711 · see citing works
Dendritic spine changes associated with hippocampal long-term synaptic plasticity
Engert, F., & Bonhoeffer, T. (1999) · Nature · doi:10.1038/19978 · Cited by 1,664 · see citing works
Matsuzaki, M., Ellis-Davies, G. C. R., Nemoto, T., Miyashita, Y., Iino, M., & Kasai, H. (2001) · Nature Neuroscience · doi:10.1038/nn736 · Cited by 1,563 · see citing works
Deficient Hippocampal Long-Term Potentiation in α-Calcium-Calmodulin Kinase II Mutant Mice
Silva, A. J., Stevens, C. F., Tonegawa, S., & Wang, Y. (1992) · Science · doi:10.1126/science.1378648 · Cited by 1,472 · see citing works
Long-term potentiation depends on release of d-serine from astrocytes
Henneberger, C., Papouin, T., Oliet, S. H. R., & Rusakov, D. A. (2010) · Nature · doi:10.1038/nature08673 · Cited by 1,389 · see citing works
Impaired Spatial Learning in α-Calcium-Calmodulin Kinase II Mutant Mice
Silva, A. J., Paylor, R. E., Wehner, J. M., & Tonegawa, S. (1992) · Science · doi:10.1126/science.1321493 · Cited by 1,351 · see citing works
Inhibition of Postsynaptic PKC or CaMKII Blocks Induction But Not Expression of LTP
Malinow, R., Schulman, H., & Tsien, R. W. (1989) · Science · doi:10.1126/science.2549638 · Cited by 1,325 · see citing works
Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting
Ehlers, M. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00129-x · Cited by 1,096 · see citing works
An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation
Malenka, R. C., Kauer, J. A., Perkel, D. J., Mauk, M. D., Kelly, P. T., Nicoll, R. A., & Waxham, M. N. (1989) · Nature · doi:10.1038/340554a0 · Cited by 1,025 · see citing works
Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression.
Huber, K., Kayser, M., & Bear, M. (2000) · Science · doi:10.1126/science.288.5469.1254 · Cited by 1,015 · see citing works
A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity
Kang, H., & Schuman, E. (1996) · Science · doi:10.1126/science.273.5280.1402 · Cited by 1,010 · see citing works
Requirement for BDNF in activity-dependent survival of cortical neurons
Ghosh, A., Carnahan, J., & Greenberg, M. E. (1994) · Science · doi:10.1126/science.7907431 · Cited by 989 · see citing works
Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system
Ehlers, M. D. (2003) · Nature Neuroscience · doi:10.1038/nn1013 · Cited by 977 · see citing works
Do thin spines learn to be mushroom spines that remember?
Bourne, J., & Harris, K. M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.009 · Cited by 843 · see citing works
Regulation of synaptic connectivity by glia.
Eroglu, C., & Barres, B. A. (2010) · Nature · doi:10.1038/nature09612 · Cited by 813 · see citing works
Lee, H.-K., Takamiya, K., Han, J.-S., Man, H., Kim, C.-H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R. S., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00122-3 · Cited by 802 · 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
Essential functions of synapsins I and II in synaptic vesicle regulation
Rosahl, T. W., Spillane, D., Missler, M., Herz, J., Selig, D. K., Wolff, J. R., Hammer, R. E., Malenka, R. C., & Südhof, T. C. (1995) · Nature · doi:10.1038/375488a0 · Cited by 719 · see citing works
Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number
Schnell, E., Sizemore, M., Karimzadegan, S., Chen, L., Bredt, D. S., & Nicoll, R. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172511199 · Cited by 691 · see citing works
Steward, O., & Levy, W. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00284.1982 · Cited by 676 · see citing works
Greer, P. L., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.002 · Cited by 661 · see citing works
The synapsins: Key actors of synapse function and plasticity
Cesca, F., Baldelli, P., Valtorta, F., & Benfenati, F. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.006 · Cited by 654 · see citing works
Sutton, M. A., Ito, H. T., Cressy, P., Kempf, C., Woo, J. C., & Schuman, E. M. (2006) · Cell · doi:10.1016/j.cell.2006.03.040 · Cited by 633 · see citing works
The Fragile X Syndrome Protein Represses Activity-Dependent Translation through CYFIP1, a New 4E-BP
Napoli, I., Mercaldo, V., Boyl, P. P., Eleuteri, B., Zalfa, F., De Rubeis, S., Di Marino, D., Mohr, E., Massimi, M., Falconi, M., et al. (2008) · Cell · doi:10.1016/j.cell.2008.07.031 · Cited by 609 · see citing works
RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction
Kaeser, P. S., Deng, L., Wang, Y., Dulubova, I., Liu, X., Rizo, J., & Südhof, T. C. (2011) · Cell · doi:10.1016/j.cell.2010.12.029 · Cited by 607 · see citing works
Neuronal RNA Granules: Movers and Makers
Kiebler, M. A., & Bassell, G. J. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.021 · Cited by 576 · see citing works
Richter, J. D. (2007) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2007.04.004 · Cited by 526 · see citing works
Wu, L., Wells, D., Tay, J., Mendis, D., Abbott, M.-A., Barnitt, A., Quinlan, E., Heynen, A., Fallon, J. R., & Richter, J. D. (1998) · Neuron · doi:10.1016/s0896-6273(00)80630-3 · Cited by 488 · see citing works
Endocannabinoid Signaling and Long-Term Synaptic Plasticity
Heifets, B. D., & Castillo, P. E. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163149 · Cited by 488 · see citing works
Waung, M. W., Pfeiffer, B. E., Nosyreva, E. D., Ronesi, J. A., & Huber, K. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.014 · Cited by 474 · see citing works
PSA-NCAM in mammalian structural plasticity and neurogenesis
Bonfanti, L. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.08.003 · Cited by 437 · see citing works
How does PKMζ maintain long-term memory?
Sacktor, T. C. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2949 · Cited by 431 · see citing works
Hippocampal Short- and Long-Term Plasticity Are Not Modulated by Astrocyte Ca 2+ Signaling
Agulhon, C., Fiacco, T. A., & McCarthy, K. D. (2010) · Science · doi:10.1126/science.1184821 · Cited by 409 · see citing works
RIM1α is required for presynaptic long-term potentiation
Castillo, P. E., Schoch, S., Schmitz, F., Südhof, T. C., & Malenka, R. C. (2002) · Nature · doi:10.1038/415327a · Cited by 389 · see citing works
Boehm, J., Kang, M.-G., Johnson, R. C., Esteban, J., Huganir, R. L., & Malinow, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.013 · Cited by 382 · see citing works
RIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone
Han, Y., Kaeser, P. S., Südhof, T. C., & Schneggenburger, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.014 · Cited by 354 · see citing works
Rapid Erasure of Long-Term Memory Associations in the Cortex by an Inhibitor of PKMζ
Shema, R., Sacktor, T. C., & Dudai, Y. (2007) · Science · doi:10.1126/science.1144334 · Cited by 353 · see citing works
Activity-dependent dynamics and sequestration of proteasomes in dendritic spines
Bingol, B., & Schuman, E. M. (2006) · Nature · doi:10.1038/nature04769 · Cited by 347 · see citing works
Bidirectional Synaptic Plasticity Regulated by Phosphorylation of Stargazin-like TARPs
Tomita, S., Stein, V., Stocker, T. J., Nicoll, R. A., & Bredt, D. S. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.009 · Cited by 343 · see citing works
Man, H.-Y., Sekine-Aizawa, Y., & Huganir, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611698104 · Cited by 311 · see citing works
Fonseca, R., Vabulas, R. M., Hartl, F. U., Bonhoeffer, T., & Nägerl, U. V. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.015 · Cited by 310 · see citing works
RIM Proteins Activate Vesicle Priming by Reversing Autoinhibitory Homodimerization of Munc13
Deng, L., Kaeser, P. S., Xu, W., & Südhof, T. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.005 · Cited by 287 · see citing works
Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport
Filosa, A., Paixão, S., Honsek, S. D., Carmona, M. A., Becker, L., Feddersen, B., Gaitanos, L., Rudhard, Y., Schoepfer, R., Klopstock, T., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2394 · Cited by 283 · see citing works
Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP
Contractor, A., Rogers, C., Maron, C., Henkemeyer, M. J., Swanson, G. T., & Heinemann, S. F. (2002) · Science · doi:10.1126/science.1069081 · Cited by 262 · see citing works
Ubiquitination in postsynaptic function and plasticity
Mabb, A. M., & Ehlers, M. D. (2010) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104129 · Cited by 255 · see citing works
Banerjee, S., Neveu, P. A., & Kosik, K. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.023 · Cited by 227 · see citing works
Synapse development and plasticity: roles of ephrin/Eph receptor signaling
Lai, K., & Ip, N. Y. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.04.009 · Cited by 191 · see citing works
Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated
Kirov, S. A., & Harris, K. M. (1999) · Nature Neuroscience · doi:10.1038/13178 · Cited by 189 · see citing works
Wells, D. G., Dong, X., Quinlan, E., Huang, Y.-S., Bear, M., Richter, J., & Fallon, J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-24-09541.2001 · Cited by 176 · see citing works
Buard, I., Coultrap, S. J., Freund, R. K., Lee, Y.-S., Dell'Acqua, M. L., Silva, A. J., & Bayer, K. U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1469-10.2010 · Cited by 160 · see citing works
Roles of the Endocannabinoid System in Learning and Memory
Marsicano, G., & Lafenêtre, P. (2009) · Current topics in behavioral neurosciences · doi:10.1007/978-3-540-88955-7_8 · Cited by 140 · see citing works
Translational Control by Neuroguidin, a Eukaryotic Initiation Factor 4E and CPEB Binding Protein
Jung, M.-Y., Lorenz, L. J., & Richter, J. D. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02470-05 · Cited by 110 · see citing works
Ch’ng, T. H., & Martin, K. C. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.01.011 · Cited by 73 · see citing works
Self-citationChanges in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones
Andrásfalvy, B. K., & Magee, J. C. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.065219 · Cited by 70 · see citing works
Delgado, J. Y., Coba, M., Anderson, C. N. G., Thompson, K. R., Gray, E. E., Heusner, C. L., Martin, K. C., Grant, S. G. N., & O'Dell, T. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3056-07.2007 · Cited by 62 · see citing works
Self-citationAMPA receptors and synaptic plasticity: a chemist's perspective
Fleming, J. J., & England, P. M. (2010) · Nature Chemical Biology · doi:10.1038/nchembio.298 · Cited by 36 · see citing works
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- Authors
- Ho, V. M., Lee, J.-A., & Martin, K. C.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Martin, Kelsey C.
- Venue
- Science
- Published
- 2011-11-04
- Volume
- 334
- Issue
- 6056
- Pages
- 623-628
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3286636
- OpenAlex
- W1979566060
- Cited by
- 573
- References
- 60
- Citations by year
- 2026: 24 · 2025: 73 · 2024: 51 · 2023: 59 · 2022: 65 · 2021: 60 · 2020: 42 · 2019: 46 · 2018: 28 · 2017: 14 · 2016: 22 · 2015: 13 · 2014: 23 · 2013: 32 · 2012: 18
- FWCI
- 9.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH077022, R21MH069645, T32MH073526)
- National Institute of General Medical Sciences (T32GM008042)
- National Institute of Neurological Disorders and Stroke (R01NS045324)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- synaptic plasticity, learning and memory, hippocampus, excitatory neurons, synaptic connectivity, gene expression, experience-dependent plasticity
- MeSH terms
- Animals, Gene Expression Regulation, Hippocampus, Humans, Learning, Memory, Synaptic Transmission, Neuroglia, Neuronal Plasticity, Neurons, Synapses
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