Independent Expression of Synaptic and Morphological Plasticity Associated with Long-Term Depression
Open accessAbstract
Physiological and morphological alterations occur with long-term synaptic modifications, such as long-term potentiation (LTP) and long-term depression (LTD), but whether these two processes are independent or interactive is unclear. It is also unknown whether or how morphological modifications, like spine remodeling, may contribute to physiological modifications, such as trafficking of glutamate receptors which underlies, at least partially, the expression of LTP and LTD. In this study, we monitored spine size and synaptic responses simultaneously using combined two photon time-lapse imaging with patch-clamp recording in acute hippocampal slices. We show that spine shrinkage and LTD can occur independently of each other. We further show that changes in spine size are unrelated to trafficking of AMPA receptors (AMPARs) under various conditions: constitutive trafficking of AMPARs, insulin-induced internalization of AMPARs, or lateral movement of AMPARs to extrasynaptic sites. Induction of LTD of NMDA receptor-mediated responses (NMDAR-LTD) is associated with spine shrinkage. Nonetheless, NMDAR-LTD and spine shrinkage diverge in the downstream signaling events, and can occur independently of each other. Thus, spine shrinkage is not caused by or required for trafficking of glutamate receptors. In a broader sense, there is a clear dissociation between physiological and morphological expression of LTD. However, inhibition of actin depolymerization blocked the expression of LTD, suggesting that morphologically silent actin remodeling may be involved in the physiological expression of LTD and different subpopulations of actin filaments undergo changes during LTD.
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The triggering of LTD is associated with the shrinkage of dendritic spines and perhaps even their disappearance.
“Conversely, the triggering of LTD is associated with the shrinkage of dendritic spines and perhaps even their disappearance (Na ¨gerl et al. 2004;Zhou et al. 2004;Wang et al. 2007;Kasai et al. 2010).”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Wang et al. 2007
Selective interference with the structural changes that accompany LTD does not affect the increase in synaptic strength, at least not in early stages, up to 1-2 hr following induction.
“Moreover, selective interference with the structural changes that accompany LTD do not seem to affect the increase in synaptic strength, at least not in early stages, up to 1 -2 hr following induction (Fig. 4) (Wang et al. 2007;Redondo and Morris 2011).”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Wang et al. 2007
Cites
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
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
Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., & Sabatini, B. L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4970-06.2007 · Cited by 1,592 · see citing works
Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses
Zhou, Q., Homma, K. J., & Poo, M.-M. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.011 · Cited by 1,025 · see citing works
Self-citationRapid 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
Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD
Beattie, E. C., Carroll, R. C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M., & Malenka, R. C. (2000) · Nature Neuroscience · doi:10.1038/81823 · Cited by 745 · 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
Dendritic spines and long-term plasticity
Segal, M. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1649 · Cited by 489 · see citing works
Merrifield, C. J., Perrais, D., & Zenisek, D. (2005) · Cell · doi:10.1016/j.cell.2005.03.015 · Cited by 476 · see citing works
Developmental regulation of spine motility in the mammalian central nervous system
Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C., & Yuste, R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13438 · Cited by 412 · see citing works
Regulation of F-Actin Stability in Dendritic Spines by Glutamate Receptors and Calcineurin
Halpain, S., Hipolito, A., & Saffer, L. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09835.1998 · Cited by 408 · cited 1× · see citing works
“It is possible that distinct populations of F-actin, defined by their subcellular locations and regulation, differentially contribute to neuronal functions (Halpain et al., 1998; Capani et al., 2001; Horne and Dell’Acqua, 2007).”
BackgroundA Role of Actin Filament in Synaptic Transmission and Long-Term Potentiation
Kim, C.-H., & Lisman, J. E. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04314.1999 · Cited by 386 · see citing works
Regulation of Synaptic Strength by Protein Phosphatase 1
Morishita, W., Connor, J. H., Xia, H., Quinlan, E. M., Shenolikar, S., & Malenka, R. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00554-2 · Cited by 227 · see citing works
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Hoover, B. R., Reed, M. N., Su, J., Penrod, R. D., Kotilinek, L. A., Grant, M. K., Pitstick, R., Carlson, G. A., Lanier, L. M., Yuan, L.-L., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.030 · Cited by 1,118 · 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
Long-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · see citing works
Structural dynamics of dendritic spines in memory and cognition
Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., & Noguchi, J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.001 · Cited by 804 · see citing works
Structural plasticity of dendritic spines
Bosch, M., & Hayashi, Y. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.09.002 · Cited by 415 · see citing works
Local protein synthesis, actin dynamics, and LTP consolidation
Bramham, C. R. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.09.013 · Cited by 301 · 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
Self-citationBiochemical Computation for Spine Structural Plasticity
Nishiyama, J., & Yasuda, R. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.043 · Cited by 199 · see citing works
Pathania, M., Davenport, E. C., Muir, J., Sheehan, D. F., López-Doménech, G., & Kittler, J. T. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.16 · Cited by 189 · see citing works
SynGAP Regulates Steady-State and Activity-Dependent Phosphorylation of Cofilin
Carlisle, H. J., Manzerra, P., Marcora, E., & Kennedy, M. B. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4695-08.2008 · Cited by 128 · see citing works
Bozdagi, O., Wang, X.-B., Nikitczuk, J. S., Anderson, T. R., Bloss, E. B., Radice, G. L., Zhou, Q., Benson, D. L., & Huntley, G. W. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1223-10.2010 · Cited by 116 · see citing works
Self-citationPICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity
Nakamura, Y., Wood, C. L., Patton, A. P., Jaafari, N., Henley, J. M., Mellor, J. R., & Hanley, J. G. (2011) · The EMBO Journal · doi:10.1038/emboj.2010.357 · Cited by 97 · see citing works
- Authors
- Wang, X.-B., Yang, Y., & Zhou, Q.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-11-07
- Volume
- 27
- Issue
- 45
- Pages
- 12419-12429
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673249
- OpenAlex
- W2054856866
- Cited by
- 100
- References
- 13
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 4 · 2020: 5 · 2019: 2 · 2018: 7 · 2017: 4 · 2016: 8 · 2015: 2 · 2014: 9 · 2013: 3 · 2012: 6
- FWCI
- 4.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ellison Medical Foundation
- Whitehall Foundation
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- long-term depression, synaptic plasticity, dendritic spine morphology, AMPA receptor trafficking, actin cytoskeleton remodeling, hippocampus, patch-clamp recording
- MeSH terms
- Animals, Animals, Newborn, Gene Expression Regulation, Neuronal Plasticity, Synapses, Rats, Sprague-Dawley, Long-Term Synaptic Depression, Rats
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