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 accessAbstract
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 density45 and the presynaptic active zone44.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [45]
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“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 the citing paper
“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
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The Classical Complement Cascade Mediates CNS Synapse Elimination
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Synaptic tagging and long-term potentiation
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“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 1,412
A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons
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(1976) · Medical Entomology and Zoology · Cited by 1,328
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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-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
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-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
Metadata
- 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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