Remodeling of Synaptic Membranes after Induction of Long-Term Potentiation
Open accessAbstract
Several morphological changes of synapses have been reported to be associated with the induction of long-term potentiation (LTP) in the CA1 hippocampus, including an transient increase in the proportion of synapses with perforated postsynaptic densities (PSDs) and a later occurrence of multiple spine boutons (MSBs) in which the two spines arise from the same dendrite. To investigate the functional significance of these modifications, we analyzed single sections and reconstructed 134 synapses labeled via activity using a calcium precipitation approach. Analyses of labeled spine profiles showed changes of the spine head area, PSD length, and proportion of spine profiles containing a coated vesicle that reflected variations in the relative proportion of different types of synapses. Three-dimensional reconstruction indicated that the increase of perforated spine profiles observed 30 min after LTP induction essentially resulted from synapses exhibiting segmented, completely partitioned PSDs. These synapses had spine head and PSD areas approximately three times larger than those of simple synapses. They contained coated vesicles in a much higher proportion than that of any other type of synapse and exhibited large spinules associated with the PSD. Also the MSBs with two spines arising from the same dendrite that were observed 1-2 hr after LTP induction included a spine that was smaller and a PSD that was smaller than those of simple synapses. These results support the idea that LTP induction is associated with an enhanced recycling of synaptic membrane and that this process could underlie the formation of synapses with segmented PSDs and eventually result in the formation of a new, immature spine.
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?
At the ultrastructural level in electron micrographs, synapses that underwent LTP had enlarged PSDs that were often discontinuous.
“Furthermore, at the ultrastructural level in electron micrographs, synapses that underwent LTP had enlarged PSDs that were often discontinuous (Toni et al. 2001).”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Toni et al. 2001
Cites
Harris, K., & Stevens, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02982.1989 · Cited by 1,073 · see citing works
Rapid Actin-Based Plasticity in Dendritic Spines
Fischer, M., Kaech, S., Knutti, D., & Matus, A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80467-5 · Cited by 905 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The yin and yang of neurotrophin action
Lu, B., Pang, P. T., & Woo, N. H. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1726 · Cited by 1,356 · see citing works
NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD).
Luscher, C., & Malenka, R. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005710 · Cited by 1,110 · see citing works
The ageing cortical synapse: hallmarks and implications for cognitive decline
Morrison, J. H., & Baxter, M. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3200 · Cited by 965 · see citing works
Dentritic spines : structure, dynamics and regulation
Hering, H., & Sheng, M. (2001) · Nature Reviews Neuroscience · doi:10.1038/35104061 · Cited by 961 · see citing works
Regulatory mechanisms of AMPA receptors in synaptic plasticity
Derkach, V. A., Oh, M. C., Guire, E. S., & Soderling, T. R. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2055 · Cited by 708 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · see citing works
Estrogen Effects on Cognitive and Synaptic Health Over the Lifecourse
Hara, Y., Waters, E. M., McEwen, B. S., & Morrison, J. H. (2015) · Physiological Reviews · doi:10.1152/physrev.00036.2014 · Cited by 470 · see citing works
The problem of pseudoreplication in neuroscientific studies: is it affecting your analysis?
Lazic, S. E. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-5 · Cited by 381 · see citing works
Homeostatic plasticity and NMDA receptor trafficking
Pérez-Otaño, I., & Ehlers, M. D. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.03.004 · Cited by 356 · see citing works
Important role of matrix metalloproteinase 9 in epileptogenesis
Wilczynski, G. M., Konopacki, F. A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P., Wawrzyniak, M., Malinowska, M., Okulski, P., Kolodziej, L. R., et al. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200708213 · Cited by 292 · see citing works
Hayashi, M. L., Choi, S.-Y., Rao, B. S. S., Jung, H.-Y., Lee, H.-K., Zhang, D., Chattarji, S., Kirkwood, A., & Tonegawa, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.003 · Cited by 280 · see citing works
Spine Expansion and Stabilization Associated with Long-Term Potentiation
Yang, Y., Wang, X.-B., Frerking, M., & Zhou, Q. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3998-07.2008 · Cited by 222 · see citing works
Donohue, H. S., Gabbott, P. L. A., Davies, H. A., Rodríguez, J. J., Cordero, M. I., Sandi, C., Medvedev, N. I., Popov, V. I., Colyer, F. M., Peddie, C. J., et al. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.072 · Cited by 139 · see citing works
Remodeling of Hippocampal Synaptic Networks by a Brief Anoxia–Hypoglycemia
Jourdain, P., Nikonenko, I., Alberi, S., & Muller, D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-08-03108.2002 · Cited by 116 · see citing works
Self-citationA brief period of sleep deprivation causes spine loss in the dentate gyrus of mice
Raven, F., Meerlo, P., Van der Zee, E. A., Abel, T., & Havekes, R. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.018 · Cited by 96 · see citing works
“Branched spines have multiple heads originating from the same base spine and might reflect the beginning of a synapse duplication, leading to enhanced receptor turnover, which also can be observed during LTP (Hering and Sheng, 2001; Toni et al., 2001).”
InfluentialThree-dimensional synaptic Organization of Layer III of the human temporal neocortex
Cano-Astorga, N., DeFelipe, J., & Alonso-Nanclares, L. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab120 · Cited by 49 · see citing works
3D synaptic organization of layer III of the human anterior cingulate and temporopolar cortex
Cano-Astorga, N., Plaza-Alonso, S., DeFelipe, J., & Alonso-Nanclares, L. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad232 · Cited by 26 · see citing works
- Authors
- Toni, N., Buchs, P.-A., Nikonenko, I., Povilaitite, P., Parisi, L., & Muller, D.
- Affiliations
- University of Geneva (CH)
- ORCID
- Toni, Nicolas
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-08-15
- Volume
- 21
- Issue
- 16
- Pages
- 6245-6251
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6763190
- OpenAlex
- W2106766347
- Cited by
- 244
- References
- 2
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 9 · 2021: 8 · 2020: 11 · 2019: 8 · 2018: 5 · 2017: 4 · 2016: 8 · 2015: 7 · 2014: 7 · 2013: 4 · 2012: 10
- FWCI
- 5.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (56852)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- long-term potentiation, hippocampal CA1, postsynaptic density, dendritic spines, spinules, coated vesicles, spine morphogenesis
- MeSH terms
- Animals, Calcium, Dendrites, Electric Stimulation, Hippocampus, Microscopy, Electron, Neuronal Plasticity, Synapses, Synaptic Membranes, Long-Term Potentiation, Coated Vesicles, Cell Surface Extensions, Rats, In Vitro Techniques
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