The Number and Organization of Ca 2+ Channels in the Active Zone Shapes Neurotransmitter Release from Schaffer Collateral Synapses
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Fast synaptic transmission requires tight colocalization of Ca 2+ channels and neurotransmitter vesicles. It is generally thought that Ca 2+ channels are expressed abundantly in presynaptic active zones, that vesicles within the same active zone have similar release properties, and that significant vesicle depletion only occurs at synapses with high release probability. Here we show, at excitatory CA3→CA1 synapses in mouse hippocampus, that release from individual vesicles is generally triggered by only one Ca 2+ channel and that only few functional Ca 2+ channels may be spread in the active zone at variable distances to neighboring neurotransmitter vesicles. Using morphologically realistic Monte Carlo simulations, we show that this arrangement leads to a widely heterogeneous distribution of release probability across the vesicles docked at the active zone, and that depletion of the vesicles closest to Ca 2+ channels can account for the Ca 2+ dependence of short-term plasticity at these synapses. These findings challenge the prevailing view that efficient synaptic transmission requires numerous presynaptic Ca 2+ channels in the active zone, and indicate that the relative arrangement of Ca 2+ channels and vesicles contributes to the heterogeneity of release probability within and across synapses and to vesicle depletion at small central synapses with low average release probability.
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Observations in small CNS synapses of both clustered and random distribution of Ca2+ channels, and emerging evidence for channel mobility as an equalizer of Pr for vesicles independent of channel positioning, suggest that their precise distribution may not be the sole determinant of the active zone release likelihood landscape.
“However, observations in small CNS synapses of both clustered24,25 and random distribution of Ca2+ channels26, and emerging evidence for channel mobility as an equalizer of Pr for vesicles independent of channel positioning27 suggest that their precise distribution may not be the sole determinant of the AZ release likelihood landscape.”
From A trans-synaptic nanocolumn aligns neurotransmitter release to receptors (2016) · cites this paper as [26]
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- Authors
- Scimemi, A., & Diamond, J. S.
- Affiliations
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-12-12
- Volume
- 32
- Issue
- 50
- Pages
- 18157-18176
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3553858
- OpenAlex
- W1978630448
- Cited by
- 85
- References
- 61
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 5 · 2023: 5 · 2022: 4 · 2021: 5 · 2020: 7 · 2019: 11 · 2018: 5 · 2017: 4 · 2016: 9 · 2015: 8 · 2014: 10 · 2013: 2
- FWCI
- 2.64
- 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
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (ZIANS002986, Z01NS002986)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- calcium channels, active zone, neurotransmitter release, Schaffer collateral synapses, CA3-CA1 synapses, hippocampus, vesicle depletion, short-term plasticity, vesicle docking, synaptic transmission, Monte Carlo simulation
- MeSH terms
- Animals, Mice, Inbred C57BL, Models, Neurological, Monte Carlo Method, Synaptic Transmission, Neurons, Synapses, Synaptic Vesicles, Calcium Channels, Neurotransmitter Agents, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Mice, CA1 Region, Hippocampal, CA3 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.
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