Cited by 321Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsGenetics and Neurodevelopmental Disorders

The DOI matches its Crossref record; 136 of the 138 references it cites were found in a registry or an index.

Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP

Open access

Bourne, Jennifer N., Harris, Kristen M.·2011·Hippocampus

DOI 10.1002/hipo.20768PMC PMC2891364

Open this paper in CoChat — free account

Abstract

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1002/hipo.20768

Cites

136 of 136 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332
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
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 2,483
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
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · cited 1×
“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).”
Method
Dendritic spine changes associated with hippocampal long-term synaptic plasticity
Engert, F., & Bonhoeffer, T. (1999) · Nature · doi:10.1038/19978 · Cited by 1,412
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 1,340
Untitled work
(1976) · Medical Entomology and Zoology · Cited by 1,328
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
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
Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation
Larson, J., Wong, D., & Lynch, G. (1986) · Brain Research · doi:10.1016/0006-8993(86)90579-2 · Cited by 1,037
Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation [published erratum appears in J Neurosci 1992 Aug;12(8):following table of contents]
Harris, K. M., Jensen, F. E., & Tsao, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02685.1992 · Cited by 1,023
Self-citation
Rapid Dendritic Morphogenesis in CA1 Hippocampal Dendrites Induced by Synaptic Activity
Maletic-Savatic, M., Malinow, R., & Svoboda, K. (1999) · Science · doi:10.1126/science.283.5409.1923 · Cited by 1,009
Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells
Megı́as, M., Emri, Z., Freund, T. F., & Gulyás, A. I. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00496-6 · Cited by 950
Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study
Colonnier, M. (1968) · Brain Research · doi:10.1016/0006-8993(68)90234-5 · Cited by 946
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
Self-citation
Reconstruct : 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 889
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
Self-citation
Macromolecular 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
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
Signal-Processing Machines at the Postsynaptic Density
Kennedy, M. B. (2000) · Science · doi:10.1126/science.290.5492.750 · Cited by 788
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
Self-citation
Protein synthesis at synaptic sites on dendrites.
Steward, O., & Schuman, E. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.299 · Cited by 731
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
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
Genesis of dendritic spines: insights from ultrastructural and imaging studies
Yuste, R., & Bonhoeffer, T. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1300 · Cited by 657
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
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 635
Locally dynamic synaptic learning rules in pyramidal neuron dendrites
Harvey, C. D., & Svoboda, K. (2007) · Nature · doi:10.1038/nature06416 · Cited by 625
Neurotoxicity of excitatory amino acids
Guidotti, A. (1990) · Raven Press eBooks · Cited by 619
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×
“…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).”
BackgroundInfluential
The 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
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
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
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 601
Three-Dimensional Organization of Smooth Endoplasmic Reticulum in Hippocampal CA1 Dendrites and Dendritic Spines of the Immature and Mature Rat
Spacek, J., & Harris, K. M. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00190.1997 · Cited by 599
Self-citation
Compartmentalized 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
The molecular sociology of the cell
Robinson, C. V., Šali, A., & Baumeister, W. P. (2007) · Nature · doi:10.1038/nature06523 · Cited by 553
Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice
Chang, F., & Greenough, W. T. (1984) · Brain Research · doi:10.1016/0006-8993(84)91008-4 · Cited by 523
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 523
Self-citation
Plasticity-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
Self-citation
CPEB-Mediated Cytoplasmic Polyadenylation and the Regulation of Experience-Dependent Translation of α-CaMKII mRNA at Synapses
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 · cited 1×
“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
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
Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus.
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
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
Polyribosomes Redistribute from Dendritic Shafts into Spines with Enlarged Synapses during LTP in Developing Rat Hippocampal Slices
Ostroff, L. E., Fiala, J. C., Allwardt, B., & Harris, K. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00785-7 · Cited by 461
Self-citation
Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area
Fifkova´, E., & Harreveld, A. V. (1977) · Journal of Neurocytology · doi:10.1007/bf01261506 · Cited by 452
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
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
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
Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough
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
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
Synapse elimination and indelible memory
Lichtman, J. W., & Colman, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)80893-4 · Cited by 380
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 362
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
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 353
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 350
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
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
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 279
Self-citation
Calcineurin-Mediated LTD of GABAergic Inhibition Underlies the Increased Excitability of CA1 Neurons Associated with LTP
Lu, Y. M., Mansuy, I. M., Kandel, E. R., & Roder, J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81150-2 · Cited by 276
Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus
Desmond, N. L., & Levy, W. B. (1983) · Brain Research · doi:10.1016/0006-8993(83)91329-x · Cited by 276
Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities
Geinisman, Y., deToledo‐Morrell, L., & Morrell, F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91683-r · Cited by 269
Endosomal Compartments Serve Multiple Hippocampal Dendritic Spines from a Widespread Rather Than a Local Store of Recycling Membrane
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
Self-citation
Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses.
Buchs, P., & Müller, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.8040 · Cited by 267
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 258
Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation
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
Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation.
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
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 243
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
Strength through Diversity
Nelson, S. B., & Turrigiano, G. G. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.020 · Cited by 233
Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: A serial electron-microscopic study
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
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 226
Visualization of the Distribution of Autophosphorylated Calcium/Calmodulin-Dependent Protein Kinase II after Tetanic Stimulation in the CA1 Area of the Hippocampus
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 225
Self-citation
Synaptic tagging — who's it?
Martin, K. C., & Kosik, K. S. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn942 · Cited by 224
Spatiotemporal 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
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
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
Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus.Preprint
Nguyen, P., & Kandel, E. R. (1997) · Learning & Memory · doi:10.1101/lm.4.2.230 · Cited by 215
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 212
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 211
Self-citation
Changes 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
Changes in the numerical density of synaptic contacts with long‐term potentiation in the hippocampal dentate gyrus
Desmond, N. L., & Levy, W. B. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530404 · Cited by 207
Spine Loss and Other Persistent Alterations of Hippocampal Pyramidal Cell Dendrites in a Model of Early-Onset Epilepsy
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
Structural synaptic correlate of long‐term potentiation: Formation of axospinous synapses with multiple, completely partitioned transmission zones
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
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
Self-citation
Local 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 195
Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer
Fifkova´, E., & Anderson, C. L. (1981) · Experimental Neurology · doi:10.1016/0014-4886(81)90197-7 · Cited by 195
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 194
Self-citation
Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP
Hosokawa, T., Rusakov, D., Bliss, T., & Fine, A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05560.1995 · Cited by 187
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 186
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
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
Self-citation
Plasticity of dendritic function
Magee, J. C., & Johnston, D. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.013 · Cited by 180
Protracted 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
Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring
Sutherland, R. J., McDonald, R. J., & Savage, D. D. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 178
Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus
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
Self-citation
Competing for Memory
Fonseca, R., Nägerl, U. V., Morris, R., & Bonhoeffer, T. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.033 · Cited by 167
Expression of Long-Term Plasticity at Individual Synapses in Hippocampus Is Graded, Bidirectional, and Mainly Presynaptic: Optical Quantal Analysis
Enoki, R., Hu, Y.-L., Hamilton, D. C., & Fine, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.026 · Cited by 166
Local 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
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
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
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
Self-citation
Different 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 138
Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro
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
Self-citation
Experience-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
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 126
Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation(ltp): A serial section electron micrograph study in the dentate gyrus in the anaesthetised rat
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 121
Synaptogenesis on mature hippocampal dendrites occurs via filopodia and immature spines during blocked synaptic transmission
Petrak, L. J., Harris, K. M., & Kirov, S. A. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20468 · Cited by 117
Self-citation
Structural changes at synapses after delayed perfusion fixation in different regions of the mouse brain
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
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 116
Long-term potentiation is associated with new excitatory spine synapses on rat dentate granule cells.Preprint
Trommald, M., Hulleberg, G., & Andersen, P. N. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.218 · Cited by 113
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
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
Morphological correlates of long‐term potentiation imply the modification of existing synapses, not synaptogenesis, in the hippocampal dentate gyrus
Desmond, N. L., & Levy, W. B. (1990) · Synapse · doi:10.1002/syn.890050208 · Cited by 103
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
Heterosynaptic Molecular Dynamics: Locally Induced Propagating Synaptic Accumulation of CaM Kinase II
Rose, J. K., Jin, S., & Craig, A. M. (2009) · Neuron · doi:10.1016/j.neuron.2008.12.030 · Cited by 98
Preservation of neuronal ultrastructure in hippocampal slices using rapid microwave-enhanced fixation
Jensen, F. E., & Harris, K. M. (1989) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(89)90146-5 · Cited by 93
Self-citation
Chemically induced long‐term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices
Stewart, 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
Age-dependence in the homeostatic upregulation of hippocampal dendritic spine number during blocked synaptic transmission
Kirov, S. A., Goddard, C. A., & Harris, K. M. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.039 · Cited by 93
Self-citation
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 91
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
Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices
Bourne, J. N., Sorra, K. E., Hurlburt, J. L., & Harris, K. M. (2006) · Hippocampus · doi:10.1002/hipo.20238 · Cited by 70
Self-citation
Ultrastructural study of cholecystokinin‐immunoreactive cells and processes in area CA1 of the rat hippocampus
Harris, K. M., Marshall, P. E., & Landis, D. M. D. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902330202 · Cited by 70
Self-citation
Differential Trafficking of AMPA and NMDA Receptors during Long-Term Potentiation in Awake Adult Animals
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 69
Shared calcium signaling pathways in the induction of long-term potentiation and synaptic disinhibition in CA1 pyramidal cell dendrites
Wang, J., & Stelzer, A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.4.1687 · Cited by 65
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
Warmer preparation of hippocampal slices prevents synapse proliferation that might obscure LTP-related structural plasticity
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
Self-citation
Layer‐specific pyramidal cell oscillations evoked by tetanic stimulation in the rat hippocampal area CA1 in vitro and in vivo
Vreugdenhil, M., Bracci, E., & Jefferys, J. G. R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.075390 · Cited by 34
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 30
Different requirements for action potentials in the induction of different forms of long‐term potentiation
Raymond, C. R. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.151035 · Cited by 22
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
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

Flagged first, then by citations

2 of the 138 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

10.1016/S0896-6273(04)00713-5 · DOI

Sorted by citations

Local translation in neurons: visualization and function
Holt, C., Martin, K. C., & Schuman, E. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0263-5 · Cited by 463
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 449
Self-citation
Impermanence 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
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 419
Self-citation
The 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 all 321

Authors: Bourne, J. N., & Harris, K. M.
Affiliations: The University of Texas at Austin (US)
Corresponding author: Harris, Kristen M.
ORCID: Bourne, Jennifer N.
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
DOI: 10.1002/hipo.20768
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
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

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

Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks