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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The masking of membrane specializations is probably one of the reasons why many ultrastructural studies that used high concentrations of potassium ferrocyanide/ferricyanide (1.5-3.0%) provided no data on SS.
“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
The Serial electron microscopy methods report that tissue from two animals was treated with 1.5% potassium ferrocyanide, supporting the citation as an example of a study using the stated concentration range. The paper does not say that this treatment masked membrane specializations or caused an absence of SS data; it instead discusses possible staining or fixation limitations in visualizing smooth endoplasmic reticulum. (LLM, conf=0.80)
Experimental — accuracy not yet measuredGiven that each spine receives only one synaptic input, the data indicate that 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 theories.
“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]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe expression of AMPA receptors is controlled independently at the level of the individual spine.
“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]
The Serial electron microscopy section (p. 2983) proposes that constricted spine necks might limit diffusion to neighboring synapses, supporting the cited notion of a spine as a possible chemical compartment. The discussion of spine geometry and synaptic efficacy (page not specified in our copy) likewise treats compartmentation as a possibility. Neither passage establishes that AMPA-receptor expression is controlled independently at each spine. (LLM, conf=0.85)
Experimental — accuracy not yet measuredRegions of glutamate sensitivity tended to be asymmetrically localized to one portion of a spine.
“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]
The citation follows the sentence’s PSD explanation, while the asymmetric glutamate-sensitivity observation is presented as the citing paper’s own finding. In “Relationships between hippocampal spine geometry and,” Harris and Stevens describe PSDs as occupying only a small portion of spine surface and suggest that larger PSDs contain more receptors. Our copy does not establish that the receptors are specifically AMPA receptors or give the stated 0.1–0.5 μm PSD diameter. (LLM, conf=0.79)
Experimental — accuracy not yet measuredSyn1a-CFP puncta area correlated with pHuse area.
“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]
The Serial electron microscopy section reports that postsynaptic density area was proportional to presynaptic axonal varicosity volume, supporting a general relationship between bouton size and synaptic size. It does not report Syn1a-CFP puncta, pHuse area, or a correlation between those two fluorescence measurements. (LLM, conf=0.82)
Experimental — accuracy not yet measured
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.
“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
The Serial electron microscopy section reports that PSD area is proportional to the number of vesicles in the presynaptic axonal varicosity. The Relationships between hippocampal spine geometry and synaptic efficacy section infers that larger PSDs likely contain more receptors, but does not count them. Neither section establishes a correlation with the readily releasable transmitter pool. Page numbers are not available in the indexed passages. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe volume of the dendritic spine head is related to the size of the postsynaptic density, the number of presynaptic vesicles, and the number of vesicles adjacent to the presynaptic cleft.
“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
The Serial electron microscopy section reports that spine head volume correlates with postsynaptic density area and with the total number of vesicles in the presynaptic axonal varicosity. It says all vesicles in those varicosities were counted, but does not report a separate relationship for vesicles adjacent to the synaptic cleft. Page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe volume of the dendritic spine head is directly proportional to the strength of synaptic currents.
“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
The Discussion reports that spine-head dimensions are proportional to postsynaptic density area and presynaptic vesicle number. In “Relationships between hippocampal spine geometry and anatomical indicators of synaptic efficacy” (page not specified), the authors propose that head size might reflect synaptic efficacy. They do not establish that head volume is directly proportional to synaptic current strength; the paper says measurement of conductance at individual spine synapses was impossible. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe relationship between spine geometry and expression of functional AMPA receptors provides substantial support to the hypothesis that neuronal fine structures have functional correlates in the brain.
“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]
The data are consistent with the correlation between AMPA receptor immunoreactivity and the size of PSD, because the size of PSD is nearly proportional to the spine-head volume.
“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]
Spine head volume is correlated with the area of the postsynaptic density.
“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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- 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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