Properties of Quantal Transmission at CA1 Synapses

Raghavachari, Sridhar; Lisman, John E.

doi:10.1152/jn.00258.2004

Cited by 197Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionCellular transport and secretion

Properties of Quantal Transmission at CA1 Synapses

Raghavachari, Sridhar, Lisman, John E.·2004·Journal of Neurophysiology

DOI 10.1152/jn.00258.2004

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Abstract

We have used Monte Carlo simulations to understand the generation of quantal responses at the single active zones of CA1 synapses. We constructed a model of AMPA channel activation that accounts for the responses to controlled glutamate application and a model of glutamate diffusion in the synaptic cleft. With no further adjustments to these models, we simulated the response to the release of glutamate from a single vesicle. The predicted response closely matches the rise time of observed responses, which recent measurements show is much faster (<100 micros) than previously thought. The simulations show that initial channel opening is driven by a brief (<100 micros) glutamate spike near the site of vesicle fusion, producing a hotspot of channel activation (diameter: approximately 250 nm) smaller than many synapses. Quantal size therefore depends more strongly on the density of channels than their number, a finding that has important implications for measuring synaptic strength. Recent measurements allow estimation of AMPA receptor density at CA1 synapses. Using this value, our simulations correctly predicts a quantal amplitude of approximately 10 pA. We have also analyzed the properties of excitatory postsynaptic currents (EPSCs) generated by the multivesicular release that can occur during evoked responses. We find that summation is nearly linear and that the existence of multiple narrow peaks in amplitude histograms can be accounted for. It has been unclear how to reconcile…

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The probability of AMPA receptor activation declines with distance from glutamate release sites.
“given that the probability of AMPAR activation declines with distance from glutamate release sites has previously been deduced3,16”
From A trans-synaptic nanocolumn aligns neurotransmitter release to receptors (2016) · cites this paper as [16]
The relationship between channel opening probability and distance from a release site is Po(r)=0.42e-r/88nm.
“Central to this approach is the relationship between channel opening probability and its distance from a release site, determined previously by stochastic modeling approaches3,16,47: (6)Po(r)=0.42e-r/88nm”
From A trans-synaptic nanocolumn aligns neurotransmitter release to receptors (2016) · cites this paper as [16]

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Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy.
Cingolani, L. A., & Goda, Y. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2373 · Cited by 831 · see citing works
A trans-synaptic nanocolumn aligns neurotransmitter release to receptors
Tang, A.-H., Chen, H., Li, T. P., Metzbower, S. R., MacGillavry, H. D., & Blanpied, T. A. (2016) · Nature · doi:10.1038/nature19058 · Cited by 677 · see citing works
Super-Resolution Imaging Reveals That AMPA Receptors Inside Synapses Are Dynamically Organized in Nanodomains Regulated by PSD95
Nair, D., Hosy, E., Petersen, J. D., Constals, A., Giannone, G., Choquet, D., & Sibarita, J.-B. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2381-12.2013 · Cited by 617 · see citing works
Nanoscale Scaffolding Domains within the Postsynaptic Density Concentrate Synaptic AMPA Receptors
MacGillavry, H. D., Song, Y., Raghavachari, S., & Blanpied, T. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.009 · Cited by 442 · see citing works
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Structural and Functional Architecture of AMPA-Type Glutamate Receptors and Their Auxiliary Proteins
Greger, I. H., Watson, J. F., & Cull-Candy, S. G. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.009 · Cited by 392 · see citing works
Glutamate receptor dynamics in dendritic microdomains.
Newpher, T. M., & Ehlers, M. D. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.030 · Cited by 356 · see citing works
Transcellular Nanoalignment of Synaptic Function
Biederer, T., Kaeser, P. S., & Blanpied, T. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.006 · Cited by 352 · see citing works
Single-Molecule Discrimination of Discrete Perisynaptic and Distributed Sites of Actin Filament Assembly within Dendritic Spines
Frost, N. A., Shroff, H., Kong, H., Betzig, E., & Blanpied, T. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.026 · Cited by 263 · see citing works
Structure and function of a neocortical synapse
Holler, S., Köstinger, G., Martin, K. A. C., Schuhknecht, G. F. P., & Stratford, K. J. (2021) · Nature · doi:10.1038/s41586-020-03134-2 · Cited by 249 · see citing works
Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity
Ehlers, M. D., Heine, M., Groc, L., Lee, M.-C., & Choquet, D. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.010 · Cited by 300 · see citing works
The sequence of events that underlie quantal transmission at central glutamatergic synapses
Lisman, J. E., Raghavachari, S., & Tsien, R. W. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2191 · Cited by 244 · see citing works
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A Unified Model of the Presynaptic and Postsynaptic Changes During LTP at CA1 Synapses
Lisman, J., & Raghavachari, S. (2006) · Science's STKE · doi:10.1126/stke.3562006re11 · Cited by 241 · see citing works
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Thinking Outside the Cleft to Understand Synaptic Activity: Contribution of the Cystine-Glutamate Antiporter (System xc−) to Normal and Pathological Glutamatergic Signaling
Bridges, R., Lutgen, V., Lobner, D., & Baker, D. A. (2012) · Pharmacological Reviews · doi:10.1124/pr.110.003889 · Cited by 205 · see citing works
From the stochasticity of molecular processes to the variability of synaptic transmission
Ribrault, C., Sekimoto, K., & Triller, A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3025 · Cited by 198 · see citing works
Pre-post synaptic alignment through neuroligin-1 tunes synaptic transmission efficiency
Haas, K. T., Compans, B., Letellier, M., Bartol, T. M., Grillo-Bosch, D., Sejnowski, T. J., Sainlos, M., Choquet, D., Thoumine, O., & Hosy, E. (2018) · eLife · doi:10.7554/elife.31755 · Cited by 183 · see citing works
Distance-Dependent Differences in Synapse Number and AMPA Receptor Expression in Hippocampal CA1 Pyramidal Neurons
Nicholson, D. A., Trana, R. E., Katz, Y., Kath, W. L., Spruston, N., & Geinisman, Y. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.022 · Cited by 188 · see citing works
SynCAM 1 Adhesion Dynamically Regulates Synapse Number and Impacts Plasticity and Learning
Robbins, E. M., Krupp, A. J., de Arce, K. P., Ghosh, A. K., Fogel, A. I., Boucard, A. A., Südhof, T. C., Stein, V., & Biederer, T. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.003 · Cited by 178 · see citing works
The Input-Output Transformation of the Hippocampal Granule Cells: From Grid Cells to Place Fields
de Almeida, L., Idiart, M., & Lisman, J. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6048-08.2009 · Cited by 167 · see citing works
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Glutamatergic synapses are structurally and biochemically complex because of multiple plasticity processes: long-term potentiation, long-term depression, short-term potentiation and scaling
Lisman, J. E. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0260 · Cited by 165 · see citing works
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The Unitary Event Underlying Multiquantal EPSCs at a Hair Cell's Ribbon Synapse
Li, G., Keen, E., Andor-Ardó, D., Hudspeth, A. J., & von Gersdorff, H. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0514-09.2009 · Cited by 164 · see citing works
Expression of Long-Term Plasticity at Individual Synapses in Hippocampus Is Graded, Bidirectional, and Mainly Presynaptic: Optical Quantal Analysis
Enoki, R., Hu, Y.-L., Hamilton, D. C., & Fine, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.026 · Cited by 158 · see citing works
Functional organization of postsynaptic glutamate receptors
Scheefhals, N., & MacGillavry, H. D. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.002 · Cited by 151 · see citing works
Multivesicular Release at Schaffer Collateral–CA1 Hippocampal Synapses
Christie, J. M., & Jahr, C. E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4307-05.2006 · Cited by 144 · see citing works
PTEN is recruited to the postsynaptic terminal for NMDA receptor‐dependent long‐term depression
Jurado, S., Benoist, M., Lario, A., Knafo, S., Petrok, C. N., & Esteban, J. A. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.160 · Cited by 146 · see citing works
Receptor Actions of Synaptically Released Glutamate: The Role of Transporters on the Scale from Nanometers to Microns
Zheng, K., Scimemi, A., & Rusakov, D. A. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.129874 · Cited by 143 · see citing works
Spine microdomains for postsynaptic signaling and plasticity
Newpher, T. M., & Ehlers, M. D. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.02.004 · Cited by 140 · see citing works
Structural plasticity with preserved topology in the postsynaptic protein network
Blanpied, T. A., Kerr, J. M., & Ehlers, M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711669105 · Cited by 133 · see citing works
Protein kinase Mζ enhances excitatory synaptic transmission by increasing the number of active postsynaptic AMPA receptors
Ling, D. S. F., Benardo, L. S., & Sacktor, T. C. (2006) · Hippocampus · doi:10.1002/hipo.20171 · Cited by 132 · see citing works
Optogenetic Control of Synaptic Composition and Function
Sinnen, B. L., Bowen, A. B., Forte, J. S., Hiester, B. G., Crosby, K. C., Gibson, E. S., Dell’Acqua, M. L., & Kennedy, M. J. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.037 · Cited by 124 · see citing works
Retrograde Synaptic Inhibition Is Mediated by α-Neurexin Binding to the α2δ Subunits of N-Type Calcium Channels
Tong, X.-J., Soto, E. J. L., Li, L., Liu, H., Nedelcu, D., Lipscombe, D., Hu, Z., & Kaplan, J. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.018 · Cited by 116 · see citing works
Synaptic transmission and plasticity require AMPA receptor anchoring via its N-terminal domain
Watson, J. F., Ho, H., & Greger, I. H. (2017) · eLife · doi:10.7554/elife.23024 · Cited by 117 · see citing works
Nanoscale co-organization and coactivation of AMPAR, NMDAR, and mGluR at excitatory synapses
Goncalves, J., Bartol, T. M., Camus, C., Levet, F., Menegolla, A. P., Sejnowski, T. J., Sibarita, J.-B., Vivaudou, M., Choquet, D., & Hosy, E. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1922563117 · Cited by 112 · see citing works
Shaping the synaptic signal: molecular mobility inside and outside the cleft
Rusakov, D. A., Savtchenko, L. P., Zheng, K., & Henley, J. M. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.002 · Cited by 105 · see citing works
AMPA Receptors as Therapeutic Targets for Neurological Disorders
Lee, K., Goodman, L., Fourie, C., Schenk, S., Leitch, B., & Montgomery, J. M. (2015) · Advances in protein chemistry and structural biology · doi:10.1016/bs.apcsb.2015.10.004 · Cited by 102 · see citing works
Unveiling the Extracellular Space of the Brain: From Super-resolved Microstructure toIn VivoFunction
Hrabětová, S., Cognet, L., Rusakov, D. A., & Nägerl, U. V. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1664-18.2018 · Cited by 98 · see citing works
Modulation of Synaptic Plasticity by Glutamatergic Gliotransmission: A Modeling Study
Pittà, M. D., & Brunel, N. (2016) · Neural Plasticity · doi:10.1155/2016/7607924 · Cited by 96 · see citing works
Fast AMPAR trafficking for a high‐frequency synaptic transmission
Choquet, D. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07350.x · Cited by 93 · see citing works
The ubiquitous nature of multivesicular release
Rudolph, S., Tsai, M., von Gersdorff, H., & Wadiche, J. I. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.05.008 · Cited by 95 · see citing works
Subsynaptic positioning of AMPARs by LRRTM2 controls synaptic strength
Ramsey, A. M., Tang, A., LeGates, T. A., Gou, X., Carbone, B. E., Thompson, S. M., Biederer, T., & Blanpied, T. A. (2021) · Science Advances · doi:10.1126/sciadv.abf3126 · Cited by 90 · see citing works
Synapse‐to‐synapse variation in mean synaptic vesicle size and its relationship with synaptic morphology and function
Qu, L., Akbergenova, Y., Hu, Y., & Schikorski, T. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22007 · Cited by 93 · see citing works
Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity
Pittà, M. D., Volman, V., Berry, H., Parpura, V., Volterra, A., & Ben‐Jacob, E. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00098 · Cited by 91 · see citing works
Subsynaptic AMPA Receptor Distribution Is Acutely Regulated by Actin-Driven Reorganization of the Postsynaptic Density
Kerr, J. M., & Blanpied, T. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2927-11.2012 · Cited by 91 · see citing works
Asynchronous release sites align with NMDA receptors in mouse hippocampal synapses
Li, S., Raychaudhuri, S., Lee, S. A., Brockmann, M. M., Wang, J., Kusick, G. F., Prater, C. M., Syed, S., Falahati, H., Ramos, R., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21004-x · Cited by 89 · see citing works
Scaffolding Proteins of the Post-synaptic Density Contribute to Synaptic Plasticity by Regulating Receptor Localization and Distribution: Relevance for Neuropsychiatric Diseases
Iasevoli, F., Tomasetti, C., & de Bartolomeis, A. (2012) · Neurochemical Research · doi:10.1007/s11064-012-0886-y · Cited by 88 · see citing works
Acceleration of AMPA receptor kinetics underlies temperature‐dependent changes in synaptic strength at the rat calyx of Held
Postlethwaite, M., Hennig, M. H., Steinert, J. R., Graham, B. P., & Forsythe, I. D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.123612 · Cited by 87 · see citing works
Loss of neuronal GSK3β reduces dendritic spine stability and attenuates excitatory synaptic transmission via β-catenin
Ochs, S. M., Dorostkar, M. M., Aramuni, G., Schön, C., Filser, S., Pöschl, J., Kremer, A., Leuven, F. V., Ovsepian, S. V., & Herms, J. W. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.55 · Cited by 86 · see citing works
Synapse Geometry and Receptor Dynamics Modulate Synaptic Strength
Freche, D., Pannasch, U., Rouach, N., & Holcman, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025122 · Cited by 86 · see citing works
A Low-Affinity Antagonist Reveals Saturation and Desensitization in Mature Synapses in the Auditory Brain Stem
Chanda, S., & Xu‐Friedman, M. A. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00751.2009 · Cited by 82 · see citing works
Diversity of Glutamatergic Synaptic Strength in Lateral Prefrontal versus Primary Visual Cortices in the Rhesus Monkey
Medalla, M., & Luebke, J. I. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3426-14.2015 · Cited by 71 · see citing works
Electric Fields Due to Synaptic Currents Sharpen Excitatory Transmission
Sylantyev, S., Savtchenko, L. P., Niu, Y., Ivanov, A., Jensen, T. P., Kullmann, D. M., Xiao, M., & Rusakov, D. A. (2008) · Science · doi:10.1126/science.1154330 · Cited by 73 · see citing works
Dynamics of nascent and active zone ultrastructure as synapses enlarge during long‐term potentiation in mature hippocampus
Bell, M. E., Bourne, J. N., Chirillo, M. A., Mendenhall, J. M., Kuwajima, M., & Harris, K. M. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23646 · Cited by 72 · see citing works
The Effects of NR2 Subunit-Dependent NMDA Receptor Kinetics on Synaptic Transmission and CaMKII Activation
Santucci, D. M., & Raghavachari, S. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000208 · Cited by 71 · see citing works
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Perisynaptic astroglial processes: dynamic processors of neuronal information
Ghézali, G., Dallérac, G. M., & Rouach, N. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1070-3 · Cited by 69 · see citing works
Synaptic Vesicle Docking: Sphingosine Regulates Syntaxin1 Interaction with Munc18
Camoletto, P. G., Vara, H., Morando, L., Connell, E., Marletto, F. P., Giustetto, M., Sassoé‐Pognetto, M., Veldhoven, P. P. V., & Ledesma, M. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005310 · Cited by 70 · see citing works
Neuron-Specific Regulation of Associative Learning and Memory by MAGI-1 in C. elegans
Steták, A., Hoerndli, F. J., Maricq, A. V., van den Heuvel, S., & Hajnal, A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006019 · Cited by 69 · see citing works
Comparative ultrastructural features of excitatory synapses in the visual and frontal cortices of the adult mouse and monkey
Hsu, A., Luebke, J. I., & Medalla, M. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24196 · Cited by 68 · see citing works
Structural mechanisms of activation and desensitization in neurotransmitter-gated ion channels
Plested, A. J. R. (2016) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3214 · Cited by 66 · see citing works
Lateral organization of the postsynaptic density
MacGillavry, H. D., Kerr, J. M., & Blanpied, T. A. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2011.09.001 · Cited by 64 · see citing works
Mechanisms of Neuronal Silencing After Cortical Spreading Depression
Sawant-Pokam, P., Suryavanshi, P. S., Méndez, J. M., Dudek, F. E., & Brennan, K. C. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv328 · Cited by 65 · see citing works
Protein Crowding within the Postsynaptic Density Can Impede the Escape of Membrane Proteins
Li, T. P., Song, Y., MacGillavry, H. D., Blanpied, T. A., & Raghavachari, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3154-15.2016 · Cited by 63 · see citing works
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Quantal Fluctuations in Central Mammalian Synapses: Functional Role of Vesicular Docking Sites
Pulido, C., & Marty, A. (2017) · Physiological Reviews · doi:10.1152/physrev.00032.2016 · Cited by 60 · see citing works
Independent Regulation of Basal Neurotransmitter Release Efficacy by Variable Ca2+ Influx and Bouton Size at Small Central Synapses
Ermolyuk, Y. S., Alder, F. G., Henneberger, C., Rusakov, D. A., Kullmann, D. M., & Volynski, K. E. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001396 · Cited by 59 · see citing works
Functional Indicators of Glutamate Transport in Single Striatal Astrocytes and the Influence of Kir4.1 in Normal and Huntington Mice
Dvorzhak, A., Vagner, T., Kirmse, K., & Grantyn, R. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0316-16.2016 · Cited by 61 · see citing works
Axospinous synaptic subtype‐specific differences in structure, size, ionotropic receptor expression, and connectivity in apical dendritic regions of rat hippocampal CA1 pyramidal neurons
Nicholson, D. A., & Geinisman, Y. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21896 · Cited by 57 · see citing works
AMPA receptor nanoscale dynamic organization and synaptic plasticities
Choquet, D., & Hosy, E. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.04.003 · Cited by 59 · see citing works
Evaluation of glutamate concentration transient in the synaptic cleft of the rat calyx of Held
Budisantoso, T., Harada, H., Kamasawa, N., Fukazawa, Y., Shigemoto, R., & Matsui, K. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.241398 · Cited by 59 · see citing works
Creating diverse synapses from the same molecules
Nusser, Z. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.001 · Cited by 63 · see citing works
Nanoscale rules governing the organization of glutamate receptors in spine synapses are subunit specific
Hruska, M., Cain, R. E., & Dalva, M. B. (2022) · Nature Communications · doi:10.1038/s41467-022-28504-4 · Cited by 56 · see citing works
Mechanisms Underlying Signal Filtering at a Multisynapse Contact
Budisantoso, T., Matsui, K., Kamasawa, N., Fukazawa, Y., & Shigemoto, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5243-11.2012 · Cited by 56 · see citing works
Functional consequences of pre- and postsynaptic expression of synaptic plasticity
Costa, R. P., Mizusaki, B. E. P., Sjöström, P. J., & van Rossum, M. C. W. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0153 · Cited by 57 · see citing works
Nanoscale architecture of synaptic vesicles and scaffolding complexes revealed by cryo-electron tomography
Held, R. G., Liang, J., & Brünger, A. T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2403136121 · Cited by 51 · see citing works
Genetic inhibition of CaMKII in dorsal striatal medium spiny neurons reduces functional excitatory synapses and enhances intrinsic excitability
Klug, J. R., Mathur, B. N., Kash, T. L., Wang, H.-D., Matthews, R. T., Robison, A. J., Anderson, M. E., Deutch, A. Y., Lovinger, D. M., Colbran, R. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045323 · Cited by 49 · see citing works
Heterogeneity of glutamatergic synapses: cellular mechanisms and network consequences
Wichmann, C., & Kuner, T. (2021) · Physiological Reviews · doi:10.1152/physrev.00039.2020 · Cited by 59 · see citing works
Specificity of Primate Amygdalar Pathways to Hippocampus
Wang, J., & Barbas, H. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1267-18.2018 · Cited by 48 · see citing works
Vesicle Pool Size at the Salamander Cone Ribbon Synapse
Bartoletti, T. M., Babai, N. Z., & Thoreson, W. B. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00718.2009 · Cited by 49 · see citing works
Neurexin-3 subsynaptic densities are spatially distinct from Neurexin-1 and essential for excitatory synapse nanoscale organization in the hippocampus
Lloyd, B. A., Han, Y., Roth, R., Zhang, B., & Aoto, J. N. (2023) · Nature Communications · doi:10.1038/s41467-023-40419-2 · Cited by 42 · see citing works
Nano-Organization at the Synapse: Segregation of Distinct Forms of Neurotransmission
Guzikowski, N. J., & Kavalali, E. T. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.796498 · Cited by 45 · see citing works
A network of autism linked genes stabilizes two pools of synaptic GABAA receptors
Tong, X.-J., Hu, Z., Liu, Y., Anderson, D. C., & Kaplan, J. M. (2015) · eLife · doi:10.7554/elife.09648 · Cited by 44 · see citing works
The organization of AMPA receptor subunits at the postsynaptic membrane
Jacob, A., & Weinberg, R. J. (2014) · Hippocampus · doi:10.1002/hipo.22404 · Cited by 40 · see citing works
Matched Pre- and Post-Synaptic Changes Underlie Synaptic Plasticity over Long Time Scales
Loebel, A., Bé, J.-V. L., Richardson, M. J. E., Markram, H., & Herz, A. V. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3740-12.2013 · Cited by 35 · see citing works
Ultrastructural and functional changes at the tripartite synapse during epileptogenesis in a model of temporal lobe epilepsy
Clarkson, C., Smeal, R. M., Hasenoehrl, M. G., White, J. A., Rubio, M. E., & Wilcox, K. S. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113196 · Cited by 38 · see citing works
AMPA receptor anchoring at CA1 synapses is determined by N-terminal domain and TARP γ8 interactions
Watson, J. F., Pinggera, A., Ho, H., & Greger, I. H. (2021) · Nature Communications · doi:10.1038/s41467-021-25281-4 · Cited by 38 · see citing works
Neuroligin-3 confines AMPA receptors into nanoclusters, thereby controlling synaptic strength at the calyx of Held synapses
Han, Y., Cao, R., Qin, L., Chen, L. Y., Tang, A., Südhof, T. C., & Zhang, B. (2022) · Science Advances · doi:10.1126/sciadv.abo4173 · Cited by 37 · see citing works
S-nitrosylation-dependent proteasomal degradation restrains Cdk5 activity to regulate hippocampal synaptic strength
Zhang, P., Fu, W., Fu, A. K. Y., & Ip, N. Y. (2015) · Nature Communications · doi:10.1038/ncomms9665 · Cited by 36 · see citing works
Asymmetry Between Pre- and Postsynaptic Transient Nanodomains Shapes Neuronal Communication
Heine, M., & Holcman, D. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.01.005 · Cited by 34 · see citing works
The glutamatergic synapse: a complex machinery for information processing
Maio, V. D. (2021) · Cognitive Neurodynamics · doi:10.1007/s11571-021-09679-w · Cited by 34 · see citing works
The single place fields of CA3 cells: A two‐stage transformation from grid cells
de Almeida, L., Idiart, M., & Lisman, J. E. (2010) · Hippocampus · doi:10.1002/hipo.20882 · Cited by 32 · see citing works
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Deorphanization of novel biogenic amine-gated ion channels identifies a new serotonin receptor for learning
Morud, J., Hardege, I., Liu, H., Wu, T., Choi, M.-K., Basu, S., Zhang, Y., & Schafer, W. R. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.036 · Cited by 32 · see citing works
The Pre/Post LTP Debate
Lisman, J. E. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.020 · Cited by 31 · see citing works
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The internal architecture of dendritic spines revealed by super-resolution imaging: What did we learn so far?
MacGillavry, H. D., & Hoogenraad, C. C. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.02.024 · Cited by 31 · see citing works
The number and distribution of AMPA receptor channels containing fast kinetic GluA3 and GluA4 subunits at auditory nerve synapses depend on the target cells
Rubio, M. E., Matsui, K., Fukazawa, Y., Kamasawa, N., Harada, H., Itakura, M., Molnár, E., Abe, M., Sakimura, K., & Shigemoto, R. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1408-0 · Cited by 31 · see citing works
Re-examination of the determinants of synaptic strength from the perspective of superresolution imaging
Gou, X., Ramsey, A. M., & Tang, A. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102540 · Cited by 30 · see citing works
The expression of long-term potentiation: reconciling the preists and the postivists
MacDougall, M. J., & Fine, A. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0135 · Cited by 30 · see citing works
Control of Transmembrane Protein Diffusion within the Postsynaptic Density Assessed by Simultaneous Single-Molecule Tracking and Localization Microscopy
Li, T. P., & Blanpied, T. A. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00019 · Cited by 29 · see citing works
Realistic modelling of receptor activation in hippocampal excitatory synapses: analysis of multivesicular release, release location, temperature and synaptic cross-talk
Boucher, J., Kröger, H., & Attila Gabor, S. I. K. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0273-x · Cited by 28 · see citing works
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Authors: Raghavachari, S., & Lisman, J. E.
Affiliations: Brandeis University (US)
ORCID: Lisman, John E.
Venue: Journal of Neurophysiology
Publisher: American Physiological Society
Published: 2004-10
Volume: 92
Issue: 4
Pages: 2456-2467
ISSN: 0022-3077 (ISSN-L)
1522-1598
DOI: 10.1152/jn.00258.2004
OpenAlex: W2115645299
Cited by: 197
References: 96
Citations by year: 2026: 3 · 2025: 9 · 2024: 11 · 2023: 9 · 2022: 7 · 2021: 15 · 2020: 8 · 2019: 7 · 2018: 10 · 2017: 13 · 2016: 10 · 2015: 13 · 2014: 5 · 2013: 8 · 2012: 13
FWCI: 1.52
Type: journal article
Language: en
Open access: closed
Locations: Journal of Neurophysiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01ns035083-04)
National Institute of Neurological Disorders and Stroke (R01NS027337, R01 NS27337, R01 NS35083)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords: CA1 synapses, AMPA receptors, glutamate diffusion, synaptic cleft, vesicle fusion, miniature EPSCs, multivesicular release, synaptic efficacy, channel density, rise time
MeSH terms: Benzothiadiazines, Computer Simulation, Diuretics, Hippocampus, Kinetics, Monte Carlo Method, Synaptic Transmission, Stochastic Processes, Synapses, Neural Networks, Computer, Receptors, AMPA, Glutamic Acid, Excitatory Postsynaptic Potentials

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Properties of Quantal Transmission at CA1 Synapses

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