Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP
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Enlargement of dendritic spines and synapses correlates with enhanced synaptic strength during long‐term potentiation (LTP), especially in immature hippocampal neurons. Less clear is the nature of this structural synaptic plasticity on mature hippocampal neurons, and nothing is known about the structural plasticity of inhibitory synapses during LTP. Here the timing and extent of structural synaptic plasticity and changes in local protein synthesis evidenced by polyribosomes were systematically evaluated at both excitatory and inhibitory synapses on CA1 dendrites from mature rats following induction of LTP with theta‐burst stimulation (TBS). Recent work suggests dendritic segments can act as functional units of plasticity. To test whether structural synaptic plasticity is similarly coordinated, we reconstructed from serial section transmission electron microscopy all of the spines and synapses along representative dendritic segments receiving control stimulation or TBS‐LTP. At 5 min after TBS, polyribosomes were elevated in large spines suggesting an initial burst of local protein synthesis, and by 2 h only those spines with further enlarged synapses contained polyribosomes. Rapid induction of synaptogenesis was evidenced by an elevation in asymmetric shaft synapses and stubby spines at 5 min and more nonsynaptic filopodia at 30 min. By 2 h, the smallest synaptic spines were markedly reduced in number. This synapse loss was perfectly counterbalanced by enlargement of the remaining excitatory synapses such that the summed synaptic surface area per length of dendritic segment was constant across time and conditions. Remarkably, the inhibitory synapses showed a parallel synaptic plasticity, also demonstrating a decrease in number perfectly counterbalanced by an increase in synaptic surface area. Thus, TBS‐LTP triggered spinogenesis followed by loss of small excitatory and inhibitory synapses and a subsequent enlargement of the remaining synapses by 2 h. These data suggest that dendritic segments coordinate structural plasticity across multiple synapses and maintain a homeostatic balance of excitatory and inhibitory inputs through local protein‐synthesis and selective capture or redistribution of dendritic resources. ©2010 Wiley‐Liss, Inc.
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Stimulated dendritic spines were remodelled over a period of more than 1 hour, leading to enlargement of the existing functional postsynaptic density and the presynaptic active zone.
“Stimulated dendritic spines were remodelled over a period of more than 1 hour, leading to enlargement of the existing functional postsynaptic density45 and the presynaptic active zone44.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [45]
The resulting increase in the numbers of AMPA-type and NMDA-type glutamate receptors at the synapse correlated with the magnitude of LTP.
“The resulting increase in the numbers of AMPA-type and NMDA-type glutamate receptors at the synapse correlated with the magnitude of LTP.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [45]
In rat hippocampal slices, LTP induced by multiple trains of theta-burst stimuli was accompanied by extensive remodelling of synaptic ultrastructures.
“Studies using rat hippocampal slices found that LTP induced by multiple trains of theta-burst stimuli was accompanied by extensive remodelling of synaptic ultrastructures44,45”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [45]
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Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · 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
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · cited 1× · see citing works
“Finally, slices were transferred through propylene oxide at room temperature and then embedded in LX112 and cured for 48 h at 608C in an oven (Harris et al., 2006).”
MethodDendritic 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
(1976) · Medical Entomology and Zoology · Cited by 1,328 · see citing works
A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons
Magee, J. C., & Johnston, D. (1997) · Science · doi:10.1126/science.275.5297.209 · Cited by 1,303 · see citing works
Morphological Changes in Dendritic Spines Associated with Long-Term Synaptic Plasticity
Yuste, R., & Bonhoeffer, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1071 · Cited by 1,269 · see citing works
Rapid Dendritic Morphogenesis in CA1 Hippocampal Dendrites Induced by Synaptic Activity
Maletić‐Savatić, M., Malinow, R., & Svoboda, K. (1999) · Science · doi:10.1126/science.283.5409.1923 · Cited by 1,189 · see citing works
Transient and persistent dendritic spines in the neocortex in vivo
Holtmaat, A. J. G. D., Trachtenberg, J. T., Wilbrecht, L., Shepherd, G. M., Zhang, X., Knott, G. W., & Svoboda, K. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.003 · Cited by 1,131 · see citing works
Larson, J., Wong, D., & Lynch, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)90579-2 · Cited by 1,037 · see citing works
Harris, K. M., Jensen, F. E., & Tsao, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02685.1992 · Cited by 990 · see citing works
Self-citationMegı́as, M., Emri, Z., Freund, T. F., & Gulyás, A. I. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00496-6 · Cited by 950 · see citing works
Colonnier, M. (1968) · Brain Research · doi:10.1016/0006-8993(68)90234-5 · Cited by 946 · see citing works
Balancing Structure and Function at Hippocampal Dendritic Spines
Bourne, J. N., & Harris, K. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125646 · Cited by 916 · see citing works
Self-citationReconstruct : a free editor for serial section microscopy
Fiala, J. C. (2005) · Journal of Microscopy · doi:10.1111/j.1365-2818.2005.01466.x · Cited by 884 · 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
Self-citationMacromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography
Medalia, O., Weber, I. T., Frangakis, A. S., Nicastro, D., Gerisch, G., & Baumeister, W. P. (2002) · Science · doi:10.1126/science.1076184 · Cited by 841 · see citing works
Computational subunits in thin dendrites of pyramidal cells
Polsky, A., Mel, B. W., & Schiller, J. (2004) · Nature Neuroscience · doi:10.1038/nn1253 · Cited by 817 · see citing works
Signal-Processing Machines at the Postsynaptic Density
Kennedy, M. B. (2000) · Science · doi:10.1126/science.290.5492.750 · Cited by 788 · see citing works
Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal Area CA1
Fiala, J. C., Feinberg, M., Popov, V., & Harris, K. M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08900.1998 · Cited by 758 · see citing works
Self-citationProtein Synthesis at Synaptic Sites on Dendrites
Steward, O., & Schuman, E. M. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.299 · Cited by 690 · see citing works
Activation of CaMKII in single dendritic spines during long-term potentiation
Lee, S.-J. R., Escobedo-Lozoya, Y., Szatmari, E. M., & Yasuda, R. (2009) · Nature · doi:10.1038/nature07842 · Cited by 685 · see citing works
Development of long-term dendritic spine stability in diverse regions of cerebral cortex
Zuo, Y., Lin, A., Chang, P., & Gan, W.-B. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.001 · Cited by 684 · see citing works
Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons
Losonczy, A., & Magee, J. C. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.016 · Cited by 641 · see citing works
Genesis of dendritic spines: insights from ultrastructural and imaging studies
Yuste, R., & Bonhoeffer, T. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1300 · Cited by 628 · see citing works
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625 · see citing works
Neurotoxicity of excitatory amino acids
Guidotti, A. (1990) · Raven Press eBooks · Cited by 619 · see citing works
Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines
Tanaka, J.-I., Horiike, Y., Matsuzaki, M., Miyazaki, T., Ellis-Davies, G. C. R., & Kasai, H. (2008) · Science · doi:10.1126/science.1152864 · Cited by 615 · cited 4× · see citing works
“…experiments have aimed to understand whether an individual dendritic spine can undergo structural plasticity in response to localized chemical induction (Engert and Bonhoeffer, 1999), glutamate uncaging (Matsuzaki et al., 2004; Tanaka et al., 2008), or minimal stimulation (Lang et al., 2004).”
BackgroundInfluentialThe Dynamics of Dendritic Structure in Developing Hippocampal Slices
Dailey, M. E., & Smith, S. J. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-02983.1996 · Cited by 611 · see citing works
Dynamic visualization of local protein synthesis in hippocampal neurons
Aakalu, G., Smith, W. B., Nguyen, N., Jiang, C., & Schuman, E. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00295-1 · Cited by 611 · see citing works
Bidirectional Activity-Dependent Morphological Plasticity in Hippocampal Neurons
Nägerl, U. V., Eberhorn, N., Cambridge, S. B., & Bonhoeffer, T. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.016 · Cited by 602 · see citing works
Silent synapses and the emergence of a postsynaptic mechanism for LTP
Kerchner, G. A., & Nicoll, R. A. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2501 · Cited by 602 · see citing works
Spacek, J., & Harris, K. M. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00190.1997 · Cited by 599 · see citing works
Self-citationCompartmentalized dendritic plasticity and input feature storage in neurons
Losonczy, A., Makara, J. K., & Magee, J. C. (2008) · Nature · doi:10.1038/nature06725 · Cited by 598 · see citing works
Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue
Poirazi, P., & Mel, B. W. (2001) · Neuron · doi:10.1016/s0896-6273(01)00252-5 · Cited by 592 · see citing works
The molecular sociology of the cell
Robinson, C. V., Šali, A., & Baumeister, W. P. (2007) · Nature · doi:10.1038/nature06523 · Cited by 533 · see citing works
Chang, F., & Greenough, W. T. (1984) · Brain Research · doi:10.1016/0006-8993(84)91008-4 · Cited by 523 · see citing works
Structure, development, and plasticity of dendritic spines
Harris, K. M. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80050-6 · Cited by 515 · see citing works
Self-citationPlasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes
Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M., & Ehlers, M. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.040 · Cited by 493 · see citing works
Self-citationWu, 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 · cited 1× · see citing works
“The transient elevation of polyribosomes in spines with large synapses at 5 min after TBS-LTP suggests that local mRNAs were immediately unmasked at existing strong synapses (Wu et al., 1998; Wells et al., 2000).”
Glutamate Receptor Exocytosis and Spine Enlargement during Chemically Induced Long-Term Potentiation
Kopec, C. D., Li, B., Wei, W., Boehm, J., & Malinow, R. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3918-05.2006 · Cited by 486 · see citing works
Neurotrophins and Time: Different Roles for TrkB Signaling in Hippocampal Long-Term Potentiation
Kang, H., Welcher, A. A., Shelton, D., & Schuman, E. M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80378-5 · Cited by 481 · see citing works
Lee, K. S., Schottler, F., Oliver, M. E., & LYNCH, G. S. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.44.2.247 · Cited by 473 · see citing works
PSD-95 is required for activity-driven synapse stabilization.
Ehrlich, I., Klein, M., Rumpel, S., & Malinow, R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609307104 · Cited by 470 · see citing works
Ostroff, L. E., Fiala, J. C., Allwardt, B., & Harris, K. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00785-7 · Cited by 461 · see citing works
Self-citationFifkova´, E., & Harreveld, A. V. (1977) · Journal of Neurocytology · doi:10.1007/bf01261506 · Cited by 452 · see citing works
Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice
Knott, G. W., Quairiaux, C., Genoud, C., & Welker, E. (2002) · Neuron · doi:10.1016/s0896-6273(02)00663-3 · Cited by 438 · see citing works
Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex
Zuo, Y., Yang, G., Kwon, E., & Gan, W.-B. (2005) · Nature · doi:10.1038/nature03715 · Cited by 436 · see citing works
The Spread of Ras Activity Triggered by Activation of a Single Dendritic Spine
Harvey, C. D., Yasuda, R., Zhong, H., & Svoboda, K. (2008) · Science · doi:10.1126/science.1159675 · Cited by 434 · see citing works
Hyman, J. M., Wyble, B., Goyal, V., Rossi, C. A., & Hasselmo, M. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-37-11725.2003 · Cited by 404 · see citing works
TRPV1 Channels Mediate Long-Term Depression at Synapses on Hippocampal Interneurons
Gibson, H. E., Edwards, J. G., Page, R. S., Van Hook, M. J., & Kauer, J. A. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.027 · Cited by 388 · see citing works
Synapse elimination and indelible memory
Lichtman, J. W., & Colman, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)80893-4 · Cited by 380 · see citing works
LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1
Grosshans, D. R., Clayton, D. A., Coultrap, S. J., & Browning, M. D. (2001) · Nature Neuroscience · doi:10.1038/nn779 · Cited by 357 · see citing works
A clustered plasticity model of long-term memory engrams.
Govindarajan, A., Kelleher, R. J., & Tonegawa, S. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1937 · Cited by 355 · see citing works
Stable hippocampal long-term potentiation elicited by ‘theta’ pattern stimulation
Staubli, U. V., & LYNCH, G. S. (1987) · Brain Research · doi:10.1016/0006-8993(87)91605-2 · Cited by 345 · see citing works
Rapid Redistribution of Synaptic PSD-95 in the Neocortex In Vivo
Gray, N. W., Weimer, R. M., Bureau, I., & Svoboda, K. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040370 · Cited by 338 · see citing works
Visualization of changes in presynaptic function during long-term synaptic plasticity
Zakharenko, S. S., Zablow, L., & Siegelbaum, S. A. (2001) · Nature Neuroscience · doi:10.1038/89498 · Cited by 305 · see citing works
Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance
Gaïarsa, J., Caillard, O., & Ben‐Ari, Y. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02269-5 · Cited by 300 · see citing works
Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats
Kirov, S. A., Sorra, K. E., & Harris, K. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02876.1999 · Cited by 287 · see citing works
Self-citationLu, Y. M., Mansuy, I. M., Kandel, E. R., & Roder, J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81150-2 · Cited by 280 · see citing works
Desmond, N. L., & Levy, W. B. (1983) · Brain Research · doi:10.1016/0006-8993(83)91329-x · Cited by 276 · see citing works
Geinisman, Y., deToledo‐Morrell, L., & Morrell, F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91683-r · Cited by 270 · see citing works
Cooney, J. R., Hurlburt, J. L., Selig, D. K., Harris, K. M., & Fiala, J. C. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02215.2002 · Cited by 269 · see citing works
Self-citationBuchs, P., & Müller, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.8040 · Cited by 267 · see citing works
Otmakhov, N., Tao-Cheng, J.-H., Carpenter, S., Asrican, B., Dosemeci, A., Reese, T. S., & Lisman, J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2350-04.2004 · Cited by 258 · see citing works
Remodeling of Synaptic Structure in Sensory Cortical AreasIn Vivo
Majewska, A. K., Newton, J. R., & Sur, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4454-05.2006 · Cited by 246 · see citing works
Lang, C., Barco, A., Zablow, L., Kandel, E. R., Siegelbaum, S. A., & Zakharenko, S. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407581101 · Cited by 245 · see citing works
Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation
Chen, G., Kolbeck, R., Barde, Y., Bonhoeffer, T., & Kossel, A. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07983.1999 · Cited by 244 · see citing works
A Unified Model of the Presynaptic and Postsynaptic Changes During LTP at CA1 Synapses
Lisman, J., & Raghavachari, S. (2006) · Science's STKE · doi:10.1126/stke.3562006re11 · Cited by 241 · see citing works
Nelson, S. B., & Turrigiano, G. G. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.020 · Cited by 233 · see citing works
Yankova, M. P., Hart, S. A., & Woolley, C. S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051624598 · Cited by 232 · see citing works
Ouyang, Y., Kantor, D. B., Harris, K. M., Schuman, E. M., & Kennedy, M. B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05416.1997 · Cited by 227 · see citing works
Self-citationSpatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice
Whittington, M. A., Stanford, I. M., Colling, S. B., Jefferys, J. G. R., & Traub, R. D. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.591bj.x · Cited by 224 · see citing works
LTP Promotes a Selective Long-Term Stabilization and Clustering of Dendritic Spines
De Roo, M., Klauser, P., & Muller, D. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060219 · Cited by 223 · 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
GluR1 Links Structural and Functional Plasticity at Excitatory Synapses
Kopec, C. D., Réal, É., Kessels, H. W. H. G., & Malinow, R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3503-07.2007 · Cited by 220 · see citing works
Martin, K. C., & Kosik, K. S. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn942 · Cited by 219 · see citing works
Constitutive sharing of recycling synaptic vesicles between presynaptic boutons
Darcy, K., Staras, K., Collinson, L., & Goda, Y. (2006) · Nature Neuroscience · doi:10.1038/nn1640 · Cited by 216 · see citing works
Nguyen, P., & Kandel, E. R. (1997) · Learning & Memory · doi:10.1101/lm.4.2.230 · Cited by 215 · see citing works
Uniform Serial Sectioning for Transmission Electron Microscopy
Harris, K. M., Perry, E., Bourne, J. N., Feinberg, M. D., Ostroff, L. E., & Hurlburt, J. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3994-06.2006 · Cited by 208 · see citing works
Self-citationChanges in the postsynaptic density with long‐term potentiation in the dentate gyrus
Desmond, N. L., & Levy, W. B. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530405 · Cited by 207 · see citing works
Desmond, N. L., & Levy, W. B. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530404 · Cited by 207 · see citing works
Jiang, M., Lee, C. L., Smith, K. L., & Swann, J. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08356.1998 · Cited by 207 · see citing works
Geinisman, Y., Detoledo‐Morrell, L., Morrell, F., Heller, R. E., Rossi, M. A., & Parshall, R. F. (1993) · Hippocampus · doi:10.1002/hipo.450030405 · Cited by 206 · see citing works
Extending Unbiased Stereology of Brain Ultrastructure to Three-dimensional Volumes
Fiala, J. C., & Harris, K. M. (2001) · Journal of the American Medical Informatics Association · doi:10.1136/jamia.2001.0080001 · Cited by 203 · see citing works
Self-citationFifkova´, E., & Anderson, C. L. (1981) · Experimental Neurology · doi:10.1016/0014-4886(81)90197-7 · Cited by 195 · 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
Self-citationLocal translational control in dendrites and its role in long‐term synaptic plasticity
Sutton, M. A., & Schuman, E. M. (2005) · Journal of Neurobiology · doi:10.1002/neu.20152 · Cited by 188 · see citing works
Post-translational protein modification as the substrate for long-lasting memory
Routtenberg, A., & Rekart, J. L. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.11.006 · Cited by 188 · see citing works
Hosokawa, T., Rusakov, D., Bliss, T., & Fine, A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05560.1995 · Cited by 187 · see citing works
Hippocampal Interneurons Express a Novel Form of Synaptic Plasticity
McMahon, L. L., & Kauer, J. A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80269-x · Cited by 182 · see citing works
Stability in Synapse Number and Size at 2 Hr after Long-Term Potentiation in Hippocampal Area CA1
Sorra, K. E., & Harris, K. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-02-00658.1998 · Cited by 181 · see citing works
Self-citationProtracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons
Nägerl, U. V., Köstinger, G., Anderson, J. C., Martin, K. A. C., & Bonhoeffer, T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0511-07.2007 · Cited by 178 · see citing works
Plasticity of dendritic function
Magee, J. C., & Johnston, D. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.013 · Cited by 174 · see citing works
Kirov, S. A., Petrak, L. J., Fiala, J. C., & Harris, K. M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.04.053 · Cited by 172 · see citing works
Self-citationLocal Sharing as a Predominant Determinant of Synaptic Matrix Molecular Dynamics
Tsuriel, S., Geva, R., Zamorano, P. L., Dresbach, T., Boeckers, T. M., Gundelfinger, E. D., Garner, C. C., & Ziv, N. E. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040271 · Cited by 164 · see citing works
Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures
Richards, D. A., Mateos, J. M., Hugel, S., de Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501881102 · Cited by 161 · see citing works
Fonseca, R., Nägerl, U. V., Morris, R., & Bonhoeffer, T. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.033 · Cited by 160 · see citing works
Enoki, R., Hu, Y.-L., Hamilton, D. C., & Fine, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.026 · Cited by 158 · see citing works
Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus
Raymond, C. R., & Redman, S. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.098947 · Cited by 151 · see citing works
Cylindrical diameters method for calibrating section thickness in serial electron microscopy
Fiala, J. C., & Harris, K. M. (2001) · Journal of Microscopy · doi:10.1046/j.1365-2818.2001.00926.x · Cited by 144 · see citing works
Self-citationDifferent Calcium Sources Are Narrowly Tuned to the Induction of Different Forms of LTP
Raymond, C. R., & Redman, S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.1.249 · Cited by 137 · see citing works
Fiala, J. C., Kirov, S. A., Feinberg, M. D., Petrak, L. J., George, P., Goddard, C. A., & Harris, K. M. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10825 · Cited by 134 · see citing works
Self-citationExperience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons
Makara, J. K., Losonczy, A., Wen, Q., & Magee, J. C. (2009) · Nature Neuroscience · doi:10.1038/nn.2428 · Cited by 126 · see citing works
Subcellular Dynamics of Type II PKA in Neurons
Zhong, H., Sia, G.-M., Sato, T., Gray, N. W., Mao, T., Khuchua, Z. A., Huganir, R. L., & Svoboda, K. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.013 · Cited by 125 · see citing works
Popov, V. I., Davies, H. A., Rogachevsky, V. V., Patrushev, I., Errington, M. L., Gabbott, P. L. A., Bliss, T. V. P., & Stewart, M. G. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.029 · Cited by 122 · see citing works
Tao-Cheng, J.-H., Gallant, P. E., Brightman, M., Döṣemeci, A., & Reese, T. S. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21276 · Cited by 116 · see citing works
Trommald, M., Hulleberg, G., & Andersen, P. N. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.218 · Cited by 113 · see citing works
Electrical Stimuli Patterned After the Theta-Rhythm Induce Multiple Forms of LTP
Morgan, S. L., & Teyler, T. J. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.3.1289 · Cited by 113 · see citing works
Petrak, L. J., Harris, K. M., & Kirov, S. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20468 · Cited by 112 · see citing works
Self-citationSelective immunolesions of hippocampal cholinergic input fail to impair spatial working memory
McMahan, R. W., Sobel, T. J., & Baxter, M. G. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 109 · see citing works
Molecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment
Wells, D. G., Richter, J. D., & Fallon, J. R. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00050-1 · Cited by 108 · see citing works
Long-term potentiation induced by physiologically relevant stimulus patterns
Buzsáki, G., Haas, H. L., & Anderson, E. G. (1987) · Brain Research · doi:10.1016/0006-8993(87)91618-0 · Cited by 108 · see citing works
Desmond, N. L., & Levy, W. B. (1990) · Synapse · doi:10.1002/syn.890050208 · Cited by 103 · see citing works
On the Synchronizing Mechanisms of Tetanically Induced Hippocampal Oscillations
Bracci, E., Vreugdenhil, M., Hack, S. P., & Jefferys, J. G. R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-08104.1999 · Cited by 101 · see citing works
Rose, J. K., Jin, S., & Craig, A. M. (2009) · Neuron · doi:10.1016/j.neuron.2008.12.030 · Cited by 100 · see citing works
Jensen, F. E., & Harris, K. M. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90146-5 · Cited by 93 · see citing works
Self-citationStewart, M. G., Medvedev, N. I., Popov, V. I., Schoepfer, R., Davies, H. A., Murphy, K., Dallérac, G. M., Kraev, I., & Rodríguez, J. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04174.x · Cited by 93 · see citing works
Two opposing plasticity mechanisms pulling a single synapse
Rabinowitch, I., & Segev, I. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.05.005 · Cited by 90 · see citing works
Kirov, S. A., Goddard, C. A., & Harris, K. M. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.039 · Cited by 87 · see citing works
Self-citationCompeting for MemoryHippocampal LTP under Regimes of Reduced Protein Synthesis
Fonseca, R., Nägerl, U. V., MORRIS, R., & Bonhoeffer, T. (2004) · Neuron · doi:10.1016/s0896-6273(04)00713-5 · Cited by 77 · see citing works
The Fine Structure of the Nervous System: The Neurons and Supporting Cells
Doyle, D. (1978) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.41.2.191-c · Cited by 71 · see citing works
Bourne, J. N., Sorra, K. E., Hurlburt, J. L., & Harris, K. M. (2006) · Hippocampus · doi:10.1002/hipo.20238 · Cited by 70 · see citing works
Self-citationHarris, K. M., Marshall, P. E., & Landis, D. M. D. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902330202 · Cited by 70 · see citing works
Self-citationWang, J., & Stelzer, A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.4.1687 · Cited by 65 · see citing works
Williams, J. M., Guévremont, D., Mason‐Parker, S. E., Luxmanan, C., Tate, W. P., & Abraham, W. C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2348-07.2007 · Cited by 64 · see citing works
Experience-Dependent, Rapid Structural Changes in Hippocampal Pyramidal Cell Spines
Kitanishi, T., Ikegaya, Y., Matsuki, N., & Yamada, M. K. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp012 · Cited by 42 · see citing works
Bourne, J. N., Kirov, S. A., Sorra, K. E., & Harris, K. M. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.020 · Cited by 40 · see citing works
Self-citationVreugdenhil, M., Bracci, E., & Jefferys, J. G. R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.075390 · Cited by 34 · see citing works
Long-Term Potentiation in Isolated Dendritic Spines
Corera, A. T., Doucet, G., & Fon, E. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006021 · Cited by 28 · see citing works
Raymond, C. R. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.151035 · Cited by 21 · see citing works
Differential induction of long term synaptic plasticity in inhibitory synapses of the hippocampus
Mendoza, E., Galarraga, E., Tapia, D., Laville, A., Hernández, E., & Bargas, J. (2006) · Synapse · doi:10.1002/syn.20331 · Cited by 11 · see citing works
Behaviorally evoked transient reorganization of hippocampal spines
Kitanishi, T., Ikegaya, Y., & Matsuki, N. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06860.x · Cited by 8 · see citing works
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Local translation in neurons: visualization and function
Holt, C. E., Martin, K. C., & Schuman, E. M. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0263-5 · Cited by 515 · see citing works
Ultrastructure of Synapses in the Mammalian BrainPreprint
Harris, K. M., & Weinberg, R. J. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005587 · Cited by 423 · see citing works
Self-citationImpermanence of dendritic spines in live adult CA1 hippocampus
Attardo, A., Fitzgerald, J. E., & Schnitzer, M. J. (2015) · Nature · doi:10.1038/nature14467 · Cited by 399 · see citing works
Structural Components of Synaptic Plasticity and Memory ConsolidationPreprint
Bailey, C. H., Kandel, E. R., & Harris, K. M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021758 · Cited by 393 · see citing works
Self-citationThe single dendritic branch as a fundamental functional unit in the nervous system
Branco, T., & Häusser, M. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.07.009 · Cited by 355 · see citing works
Identification of an elaborate complex mediating postsynaptic inhibition
Uezu, A., Kanak, D. J., Bradshaw, T. W. A., Soderblom, E. J., Catavero, C. M., Burette, A. C., Weinberg, R. J., & Soderling, S. H. (2016) · Science · doi:10.1126/science.aag0821 · Cited by 354 · see citing works
Structural and synaptic plasticity in stress-related disorders
Christoffel, D. J., Golden, S. A., & Russo, S. J. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.044 · Cited by 334 · see citing works
The right time to learn: Mechanisms and optimization of spaced learning
Smolen, P., Zhang, Y., & Byrne, J. H. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.18 · Cited by 326 · see citing works
Nanoconnectomic upper bound on the variability of synaptic plasticity
Bartol, T. M., Bromer, C., Kinney, J. P., Chirillo, M. A., Bourne, J. N., Harris, K. M., & B, T. J. S. A. (2015) · eLife · doi:10.7554/elife.10778 · Cited by 319 · see citing works
Self-citationSynaptic circuit remodelling by matrix metalloproteinases in health and disease
Huntley, G. W. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3320 · Cited by 282 · see citing works
Fiete, I., Senn, W., Wang, C. Z.-H., & Hahnloser, R. H. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.003 · Cited by 269 · see citing works
The dialectic of Hebb and homeostasis
Turrigiano, G. G. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0258 · Cited by 242 · see citing works
Specht, C. G., Izeddin, I., Rodriguez, P. C., Beheiry, M. E., Rostaing, P., Darzacq, X., Dahan, M., & Triller, A. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.013 · Cited by 232 · see citing works
Computational principles of memory
Chaudhuri, R., & Fiete, I. (2016) · Nature Neuroscience · doi:10.1038/nn.4237 · Cited by 213 · see citing works
Keck, T., Toyoizumi, T., Chen, L., Doiron, B., Feldman, D. E., Fox, K. D., Wulfram Gerstner, B., Haydon, P. G., Hübener, M., Lee, H., et al. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0158 · Cited by 206 · see citing works
Reconstruction of neocortex: Organelles, compartments, cells, circuits, and activity
Turner, N. L., Macrina, T., Bae, J. A., Yang, R., Wilson, A. M., Schneider-Mizell, C., Lee, K., Lu, R., Wu, J., Bodor, A. L., et al. (2022) · Cell · doi:10.1016/j.cell.2022.01.023 · Cited by 206 · see citing works
The temporal paradox of Hebbian learning and homeostatic plasticity
Zenke, F., Gerstner, W., & Ganguli, S. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.015 · Cited by 201 · see citing works
Locally coordinated synaptic plasticity of visual cortex neurons in vivo
El‐Boustani, S., Ip, J. P. K., Breton‐Provencher, V., Knott, G. W., Okuno, H., Bito, H., & Sur, M. (2018) · Science · doi:10.1126/science.aao0862 · Cited by 179 · see citing works
The CaMKII/NMDAR complex as a molecular memory
Sanhueza, M., & Lisman, J. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-10 · Cited by 166 · see citing works
Iascone, D. M., Li, Y., Sümbül, U., Doron, M., Chen, H., Andreu, V., Goudy, F., Blockus, H., Abbott, L. F., Segev, I., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.015 · Cited by 165 · see citing works
Thrombospondin receptor α2δ-1 promotes synaptogenesis and spinogenesis via postsynaptic Rac1
Risher, W. C., Kim, N., Koh, S., Choi, J.-E., Mitev, P., Spence, E. F., Pilaz, L., Wang, D., Feng, G., Silver, D. L., et al. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201802057 · Cited by 158 · see citing works
The interplay between Hebbian and homeostatic synaptic plasticity
Vitureira, N., & Goda, Y. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201306030 · Cited by 152 · see citing works
Corticosteroid-Induced Neural Remodeling Predicts Behavioral Vulnerability and Resilience
Gourley, S. L., Swanson, A. M., & Koleske, A. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2138-12.2013 · Cited by 156 · see citing works
Spatial and Working Memory Is Linked to Spine Density and Mushroom Spines
Mahmmoud, R. R., Sase, S., Aher, Y. D., Sase, A., Gröger, M., Mokhtar, M., Höger, H., & Lübec, G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139739 · Cited by 146 · see citing works
Heterosynaptic Structural Plasticity on Local Dendritic Segments of Hippocampal CA1 Neurons
Oh, W. C., Parajuli, L. K., & Zito, K. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.12.016 · Cited by 142 · see citing works
Smith, H., Bourne, J. N., Cao, G., Chirillo, M. A., Ostroff, L. E., Watson, D. J., & Harris, K. M. (2016) · eLife · doi:10.7554/elife.15275 · Cited by 146 · see citing works
Self-citationInhibitory synaptic plasticity: spike timing-dependence and putative network function
Vogels, T. P., Froemke, R. C., Doyon, N., Gilson, M., Haas, J. S., Liu, R., Maffei, A., Miller, P. C., Wierenga, C. J., Woodin, M. A., et al. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00119 · Cited by 137 · see citing works
LTP-Induced Long-Term Stabilization of Individual Nascent Dendritic Spines
Hill, T. C., & Zito, K. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1404-12.2013 · Cited by 129 · see citing works
Proteostasis in complex dendrites
Hanus, C., & Schuman, E. M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3546 · Cited by 130 · see citing works
Prox, J., Bernreuther, C., Altmeppen, H. C., Grendel, J., Glatzel, M., D’Hooge, R., Stroobants, S., Ahmed, T., Balschun, D., Willem, M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5910-12.2013 · Cited by 130 · see citing works
Nanoscale Subsynaptic Domains Underlie the Organization of the Inhibitory Synapse
Crosby, K. C., Gookin, S. E., Garcia, J. D., Zent, K. H., Dell’Acqua, M. L., & Smith, K. R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.070 · Cited by 126 · see citing works
Borczyk, M., Śliwińska, M. A., Cały, A., Bernaś, T., & Radwańska, K. (2019) · Scientific Reports · doi:10.1038/s41598-018-38412-7 · Cited by 120 · see citing works
Barnes, S. J., Franzoni, E., Jacobsen, R. I., Erdélyi, F., Szabó, G., Claudia Clopath, A., Keller, G. B., & Keck, T. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.052 · Cited by 118 · see citing works
Where is the error? Hierarchical predictive coding through dendritic error computation
Mikulasch, F. A., Rudelt, L., Wibral, M., & Priesemann, V. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.09.007 · Cited by 128 · see citing works
Pereira, A. C., Lambert, H. K., Grossman, Y. S., Dumitriu, D., Waldman, R., Jannetty, S. K., Calakos, K., Janssen, W. G., McEwen, B. S., & Morrison, J. H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421285111 · Cited by 116 · see citing works
Primed to Sleep: The Dynamics of Synaptic Plasticity Across Brain States
Seibt, J., & Frank, M. G. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00002 · Cited by 111 · see citing works
Cortés‐Mendoza, J., de León‐Guerrero, S. D., Pedraza‐Alva, G., & Pérez‐Martínez, L. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.04.003 · Cited by 110 · see citing works
Inferring learning rules from distributions of firing rates in cortical neurons
Lim, S., McKee, J. L., Woloszyn, L., Amit, Y., Freedman, D. J., Sheinberg, D. L., & Brunel, N. (2015) · Nature Neuroscience · doi:10.1038/nn.4158 · Cited by 112 · see citing works
Pennacchietti, F., Vascon, S., Nieus, T. R., Rosillo, C., Das, S., Tyagarajan, S. K., Diaspro, A., Bue, A. D., Petrini, E. M., Barberis, A., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0514-16.2016 · Cited by 112 · see citing works
Assembly of Excitatory Synapses in the Absence of Glutamatergic Neurotransmission
Sando, R. C., Bushong, E. A., Zhu, Y., Huang, M., Considine, C., Phan, S., Ju, S., Uytiepo, M., Ellisman, M. H., & Maximov, A. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.047 · Cited by 108 · see citing works
Cortical response selectivity derives from strength in numbers of synapses
Scholl, B., Thomas, C. I., Ryan, M. A., Kamasawa, N., & Fitzpatrick, D. (2020) · Nature · doi:10.1038/s41586-020-03044-3 · Cited by 100 · see citing works
The aging mouse brain: cognition, connectivity and calcium
Radulescu, C. I., Cerar, V., Haslehurst, P., Kopanitsa, M. V., & Barnes, S. J. (2021) · Cell Calcium · doi:10.1016/j.ceca.2021.102358 · Cited by 105 · see citing works
Keeping Your Brain in Balance: Homeostatic Regulation of Network Function
Wen, W., & Turrigiano, G. G. (2024) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092523-110001 · Cited by 115 · see citing works
Risher, M., Fleming, R. L., Risher, W. C., Miller, K. M., Klein, R. C., Wills, T., Acheson, S. K., Moore, S. D., Wilson, W. A., Eroglu, C., et al. (2015) · Alcoholism: Clinical and Experimental Research · doi:10.1111/acer.12725 · Cited by 104 · see citing works
Opposing Effects of Neuronal Activity on Structural Plasticity
Fauth, M. J., & Tetzlaff, C. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00075 · Cited by 99 · see citing works
Dendritic Spine Elimination: Molecular Mechanisms and Implications
Stein, I. S., & Zito, K. (2018) · The Neuroscientist · doi:10.1177/1073858418769644 · Cited by 102 · see citing works
Calì, C., Agus, M., Kare, K., Boges, D. J., Lehväslaiho, H., Hadwiger, M., & Magistretti, P. J. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.101696 · Cited by 99 · see citing works
Spano, G. M., Banningh, S. W., Marshall, W., de Vivo, L., Bellesi, M., Loschky, S. S., Tononi, G., & Cirelli, C. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0380-19.2019 · Cited by 96 · see citing works
McNamara, R. K. (2015) · World Journal of Psychiatry · doi:10.5498/wjp.v5.i1.15 · Cited by 88 · see citing works
Structural LTP: from synaptogenesis to regulated synapse enlargement and clustering
Harris, K. M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.04.009 · Cited by 87 · see citing works
Self-citationVezzoli, E., Calì, C., De Roo, M., Ponzoni, L., Sogne, E., Gagnon, N., Francolini, M., Braida, D., Sala, M., Muller, D., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhz226 · Cited by 79 · see citing works
Synapse rearrangements upon learning: from divergent–sparse connectivity to dedicated sub-circuits
Caroni, P., Chowdhury, A., & Lahr, M. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.011 · Cited by 85 · see citing works
Müllner, F. E., Wierenga, C. J., & Bonhoeffer, T. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.003 · Cited by 85 · see citing works
Chirillo, M. A., Waters, M. S., Lindsey, L. F., Bourne, J. N., & Harris, K. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-40520-x · Cited by 84 · see citing works
Self-citationCriticality meets learning: Criticality signatures in a self-organizing recurrent neural network
Papa, B. D., Priesemann, V., & Triesch, J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178683 · Cited by 83 · see citing works
Nanoscale analysis of structural synaptic plasticity
Bourne, J. N., & Harris, K. M. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.019 · Cited by 78 · see citing works
Self-citationSwanger, S. A., Yao, X., Groß, C., & Bassell, G. J. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-38 · Cited by 81 · see citing works
F‐actin patches associated with glutamatergic synapses control positioning of dendritic lysosomes
van Bommel, B., Konietzny, A., Kobler, O., Bär, J., & Mikhaylova, M. (2019) · The EMBO Journal · doi:10.15252/embj.2018101183 · Cited by 80 · see citing works
Galli, S., Lopes, D. M., Ammari, R., Kopra, J. J., Millar, S. E., Gibb, A. J., & Salinas, P. C. (2014) · Nature Communications · doi:10.1038/ncomms5992 · Cited by 80 · see citing works
Glasgow, S. D., Labrecque, S., Beamish, I. V., Aufmkolk, S., Gibon, J., Han, D. C., Harris, S. N., Dufresne, P., Wiseman, P. W., McKinney, R. A., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.028 · Cited by 80 · see citing works
ROCK1 and ROCK2 inhibition alters dendritic spine morphology in hippocampal neurons
Swanger, S. A., Mattheyses, A. L., Gentry, E. G., & Herskowitz, J. H. (2015) · Cellular Logistics · doi:10.1080/21592799.2015.1133266 · Cited by 80 · see citing works
Arc/Arg3.1 function in long‐term synaptic plasticity: Emerging mechanisms and unresolved issues
Zhang, H., & Bramham, C. R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14958 · Cited by 71 · see citing works
Wosiski‐Kuhn, M., Erion, J., Gómez-Sánchez, E. P., Gómez-Sánchez, C. E., & Stranahan, A. M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.01.020 · Cited by 76 · see citing works
New Views on the Misconstrued: Executioner Caspases and Their Diverse Non-apoptotic Roles
Unsain, N., & Barker, P. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.029 · Cited by 75 · see citing works
Shaping inhibition: activity dependent structural plasticity of GABAergic synapses
Flores, C. E., & Méndez, P. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00327 · Cited by 70 · see citing works
Bell, M. E., Bourne, J. N., Chirillo, M. A., Mendenhall, J. M., Kuwajima, M., & Harris, K. M. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23646 · Cited by 72 · see citing works
Self-citationSzepesi, Z., Bijata, M., Ruszczycki, B., Kaczmarek, L., & Włodarczyk, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063314 · Cited by 68 · see citing works
Kuwajima, M., Mendenhall, J. M., Lindsey, L. F., & Harris, K. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059573 · Cited by 70 · see citing works
Self-citationHebbian Learning in a Random Network Captures Selectivity Properties of the Prefrontal Cortex
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Diniz, C. R. A. F., & Crestani, A. P. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01931-x · Cited by 67 · see citing works
Matt, L., Kirk, L. M., Chenaux, G., Speca, D. J., Puhger, K. R., Pride, M. C., Qneibi, M., Haham, T., Plambeck, K. E., Stern-Bach, Y., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.026 · Cited by 66 · see citing works
Bourne, J. N., Chirillo, M. A., & Harris, K. M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23384 · Cited by 65 · see citing works
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Lin, Y., Yeckel, M. F., & Koleske, A. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4284-12.2013 · Cited by 63 · see citing works
Miner, D. C., & Triesch, J. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004759 · Cited by 63 · see citing works
Chapman, C. A., Nuwer, J. L., & Jacob, T. C. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.911020 · Cited by 62 · see citing works
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Hartmann, C., Lazăr, A., Nessler, B., & Triesch, J. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004640 · Cited by 60 · see citing works
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Cirelli, C. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.016 · Cited by 58 · see citing works
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Zheng, P., & Triesch, J. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2014.00066 · Cited by 58 · see citing works
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Triesch, J., Vo, A. D., & Hafner, A. (2018) · eLife · doi:10.7554/elife.37836 · Cited by 53 · see citing works
Biochemical principles underlying the stable maintenance of LTP by the CaMKII/NMDAR complex
Lisman, J. E., & Raghavachari, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.010 · Cited by 51 · see citing works
Harris, K. M., Špaček, J., Bell, M. E., Parker, P. H., Lindsey, L. F., Baden, A. D., Vogelstein, J. T., & Burns, R. C. (2015) · Scientific Data · doi:10.1038/sdata.2015.46 · Cited by 51 · see citing works
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Pinho, J., Marcut, C. F., & Fonseca, R. (2020) · IUBMB Life · doi:10.1002/iub.2261 · Cited by 47 · see citing works
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Cano-Astorga, N., DeFelipe, J., & Alonso-Nanclares, L. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab120 · Cited by 49 · see citing works
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Lee, K. J., Park, I., Kim, H., Greenough, W. T., Pak, D. T. S., & Rhyu, I. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0848-12.2013 · Cited by 49 · see citing works
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Bucher, M., Fanutza, T., & Mikhaylova, M. (2019) · Cytoskeleton · doi:10.1002/cm.21583 · Cited by 49 · see citing works
Yadav, A., Gao, Y. Z., Rodriguez, A., Dickstein, D. L., Wearne, S. L., Luebke, J. I., Hof, P. R., & Weaver, C. M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23070 · Cited by 47 · see citing works
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Wu, Y., Grebenyuk, S. E., McHugh, T. J., Rusakov, D. A., & Semyanov, A. V. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.03.007 · Cited by 45 · see citing works
Atkin, G., Moore, S. J., Lü, Y., Nelson, R. F., Tipper, N., Rajpal, G., Hunt, J. F. V., Tennant, W., Hell, J. W., Murphy, G. G., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3013-14.2015 · Cited by 46 · see citing works
Yang, Y., & Liu, J. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102534 · Cited by 47 · see citing works
Ravasenga, T., Ruben, M., Regio, V., Polenghi, A., Petrini, E. M., & Barberis, A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110347 · Cited by 47 · see citing works
Translational control of auditory imprinting and structural plasticity by eIF2α
Batista, G., Johnson, J. L., Dominguez, E. N., Costa‐Mattioli, M., & Peña, J. L. (2016) · eLife · doi:10.7554/elife.17197 · Cited by 46 · see citing works
Aziz, W., Kraev, I., Mizuno, K., Kirby, A. J., Fang, T., Rupawala, H., Kasbi, K., Rothe, S., Jozsa, F., Rosenblum, K., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.064 · Cited by 44 · see citing works
Kuwajima, M., Mendenhall, J. M., & Harris, K. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-137-0_15 · Cited by 45 · see citing works
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Kulik, Y. D., Watson, D. J., Cao, G., Kuwajima, M., & Harris, K. M. (2019) · eLife · doi:10.7554/elife.46356 · Cited by 45 · see citing works
Self-citationKuwajima, M., Špaček, J., & Harris, K. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.061 · Cited by 45 · see citing works
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Verbich, D., Prenosil, G., Chang, P. K. ‐., Murai, K. K., & McKinney, R. A. (2012) · Glia · doi:10.1002/glia.22335 · Cited by 44 · see citing works
- Authors
- Bourne, J. N., & Harris, K. M.
- Affiliations
- The University of Texas at Austin (US)
- Corresponding author
- Harris, Kristen M.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2011-03-28
- Volume
- 21
- Issue
- 4
- Pages
- 354-373
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC2891364
- OpenAlex
- W2135208959
- Cited by
- 318
- References
- 138
- Citations by year
- 2026: 17 · 2025: 21 · 2024: 17 · 2023: 10 · 2022: 22 · 2021: 18 · 2020: 27 · 2019: 29 · 2018: 18 · 2017: 24 · 2016: 19 · 2015: 33 · 2014: 17 · 2013: 21 · 2012: 13
- FWCI
- 5.95
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH095980, R01MH104319)
- National Institute of Neurological Disorders and Stroke (R01NS033574, R01NS021184, NS21184, R01NS074644, NS33574, R37NS021184)
- National Institute of Biomedical Imaging and Bioengineering (EB002170, R01EB002170)
- 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
- long-term potentiation, structural synaptic plasticity, dendritic spines, inhibitory synapses, excitatory synapses, hippocampal CA1, theta burst stimulation, local protein synthesis, polysomes, spinogenesis, synaptic loss, synaptic homeostasis, filopodia
- MeSH terms
- Animals, Male, Synaptic Transmission, Neurons, Synapses, Time Factors, Long-Term Potentiation, Rats, Long-Evans, Microscopy, Electron, Transmission, Dendritic Spines, Rats, CA1 Region, Hippocampal
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