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Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics
Open accessAbstract
Serial electron microscopy and 3-D reconstructions of dendritic spines from hippocampal area CA 1 dendrites were obtained to evaluate 2 questions about relationships between spine geometry and synaptic efficacy. First, under what biophysical conditions are the spine necks likely to reduce the magnitude of charge transferred from the synapses on the spine heads to the recipient dendrite? Simulation software provided by Charles Wilson (1984) was used to determine that if synaptic conductance is 1 nS or less, only 1% of the hippocampal spine necks are sufficiently thin and long to reduce charge transfer by more than 10%. If synaptic conductance approaches 5 nS, however, 33% of the hippocampal spine necks are sufficiently thin and long to reduce charge transfer by more than 10%. Second, is spine geometry associated with other anatomical indicators of synaptic efficacy, including the area of the postsynaptic density and the number of vesicles in the presynaptic axon? Reconstructed spines were graphically edited into head and neck compartments, and their dimensions were measured, the areas of the postsynaptic densities (PSD) were measured, and all of the vesicles in the presynaptic axonal varicosities were counted. The dimensions of the spine head were well correlated with the area of PSD and the number of vesicles in the presynaptic axonal varicosity. Spine neck diameter and length were not correlated with PSD area, head volume, or the number of vesicles. These results suggest that the dimensions of the spine head, but not the spine neck, reflect differences in synaptic efficacy. We suggest that the constricted necks of hippocampal dendritic spines might reduce diffusion of activated molecules to neighboring synapses, thereby attributing specificity to activated or potentiated synapses.
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“This is probably one of the reasons why many ultrastructural studies that utilized high concentrations of potassium ferrocyanide/ferricyanide (1.5–3.0%) provided no data on SS (e.g., Harris and Stevens, 1989; Hayworth et al., 2014; Yakoubi et al., 2019a; Yin et al., 2020; Gour et al., 2021; Phelps et al., 2021; Peddie et al., 2022; Turner et al., 2022).”
From Unambiguous identification of asymmetric and symmetric synapses using volume electron microscopy (2024) · cites this paper as Harris and Stevens, 1989
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“Given that each spine receives only one synaptic input13, our data indicate the highest possible degree of freedom is available in synaptic connections in the dendrites, which has been assumed in the learning models of most neural network theories17.”
From Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons (2001) · cites this paper as [13]
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“This observation suggests that the expression of AMPA receptors is controlled independently at a level of the individual spine, consistent with the classical notion that a single spine may behave as an independent chemical compartment to regulate synaptic transmission13, 14.”
From Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons (2001) · cites this paper as [13]
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“Regions of glutamate sensitivity tended to be asymmetrically localized to one portion of a spine (Figs. 3h and 4c–j), consistent with the predominant localization of AMPA receptors within PSDs with a diameter of 0.1 to 0.5μm13, 19, 20.”
From Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons (2001) · cites this paper as [13]
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“Syn1a-CFP puncta area calculated as a measure of bouton area, which correlated with pHuse area, as expected42.”
From A trans-synaptic nanocolumn aligns neurotransmitter release to receptors (2016) · cites this paper as [42]
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“In turn, the size of the postsynaptic density is correlated with the number of presynaptic vesicles, the number of postsynaptic receptors and the ready-releasable pool of transmitter (Harris and Stevens, 1989; Nusser et al., 1998; Schikorski and Stevens, 1999, 2001; Arellano et al., 2007a).”
From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Harris and Stevens, 1989
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“Additionally, the volume of the dendritic spine head is related to the size of the postsynaptic density (Harris and Stevens, 1989; Schikorski and Stevens, 1997; Arellano et al., 2007b), the number of presynaptic vesicles, and the number of vesicles adjacent to the presynaptic cleft (Harris and Stevens, 1989).”
From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Harris and Stevens, 1989
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“Furthermore, the volume of the head is directly proportional to the strength of synaptic currents (Harris and Stevens, 1989; Schikorski and Stevens, 1997; Arellano et al., 2007a).”
From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Harris and Stevens, 1989
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“The relationship between spine geometry and expression of functional AMPA receptors demonstrated here provides substantial support to the hypothesis that neuronal fine structures have functional correlates in the brain13, 18, 21.”
From Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons (2001) · cites this paper as [13]
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“These data are consistent with the correlation between AMPA receptor immunoreactivity and the size of PSD19, 20, because the size of PSD is nearly proportional to the spine-head volume13.”
From Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons (2001) · cites this paper as [13]
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“whereas the spine head volume is correlated with the area of the postsynaptic density.”
From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Harris and Stevens, 1989
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Citations
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Gemin, O., Serna, P., Assendorp, N., Fossati, M., Rostaing, P., Triller, A., & Charrier, C. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.06.230722
Metadata
- Authors
- Harris, K., & Stevens, J.
- Affiliations
- Boston Children's Hospital (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1989-08-01
- Volume
- 9
- Issue
- 8
- Pages
- 2982-2997
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6569708
- OpenAlex
- W2117664079
- Cited by
- 1,073
- References
- 38
- Citations by year
- 2026: 17 · 2025: 26 · 2024: 35 · 2023: 33 · 2022: 31 · 2021: 50 · 2020: 39 · 2019: 43 · 2018: 47 · 2017: 33 · 2016: 40 · 2015: 48 · 2014: 44 · 2013: 50 · 2012: 42
- FWCI
- 5.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alfred P. Sloan Foundation
- National Institutes of Health (NS21184)
- Medical Research Council
- National Institute of Neurological Disorders and Stroke (NS21184, NS 20820)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655, P30HD-18655)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- dendritic spines, CA1 pyramidal neurons, hippocampus, synaptic efficacy, postsynaptic density, synaptic vesicles, charge transfer, synaptic conductance, dendritic spine morphology, synaptic specificity
- MeSH terms
- Animals, Axons, Biophysics, Dendrites, Electric Conductivity, Endoplasmic Reticulum, Hippocampus, Image Processing, Computer-Assisted, Male, Microscopy, Electron, Models, Neurological, Neurons, Purkinje Cells, Rats, Inbred Strains, Synapses, Rats, Biophysical Phenomena
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