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

DOI 10.1002/hipo.20768PMC PMC2891364

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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.

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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

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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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