Release probability of hippocampal glutamatergic terminals scales with the size of the active zone
Open accessAbstract
Cortical synapses have structural, molecular and functional heterogeneity; our knowledge regarding the relationship between their ultrastructural and functional parameters is still fragmented. Here we asked how the neurotransmitter release probability and presynaptic [Ca(2+)] transients relate to the ultrastructure of rat hippocampal glutamatergic axon terminals. Two-photon Ca(2+) imaging-derived optical quantal analysis and correlated electron microscopic reconstructions revealed a tight correlation between the release probability and the active-zone area. Peak amplitude of [Ca(2+)] transients in single boutons also positively correlated with the active-zone area. Freeze-fracture immunogold labeling revealed that the voltage-gated calcium channel subunit Cav2.1 and the presynaptic protein Rim1/2 are confined to the active zone and their numbers scale linearly with the active-zone area. Gold particles labeling Cav2.1 were nonrandomly distributed in the active zones. Our results demonstrate that the numbers of several active-zone proteins, including presynaptic calcium channels, as well as the number of docked vesicles and the release probability, scale linearly with the active-zone area.
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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 [24]
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Experimental — accuracy not yet measuredThe number of fusion events must be correlated with the size of presynaptic terminals for successful exo-endocytosis coupling.
“Thus, the number of fusion events must be correlated with the size of presynaptic terminals61 for successful exo-endocytosis coupling.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [61]
The Results ('Large variability in release probability and short-term plasticity of axon terminals'; page unavailable) report a significant positive correlation between release probability and bouton volume. Release probability is not the number of fusion events, and the paper does not establish that such a correlation is necessary for successful exo-endocytosis coupling. (LLM, conf=0.85)
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Cites
Quantal components of the end‐plate potential
del Castillo, J., & Katz, B. (1954) · The Journal of Physiology · doi:10.1113/jphysiol.1954.sp005129 · Cited by 2,201 · see citing works
Matsuzaki, M., Ellis-Davies, G. C. R., Nemoto, T., Miyashita, Y., Iino, M., & Kasai, H. (2001) · Nature Neuroscience · doi:10.1038/nn736 · Cited by 1,563 · see citing works
The role of calcium in neuromuscular facilitation
Katz, B., & Miledi, R. (1968) · The Journal of Physiology · doi:10.1113/jphysiol.1968.sp008469 · Cited by 1,347 · see citing works
Harris, K., & Stevens, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02982.1989 · Cited by 1,073 · see citing works
Neher, E. (1998) · Neuron · doi:10.1016/s0896-6273(00)80983-6 · Cited by 1,010 · see citing works
Quantitative ultrastructural analysis of hippocampal excitatory synapses
Schikorski, T., & Stevens, C. F. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05858.1997 · Cited by 997 · see citing works
Roles of N-Type and Q-Type Ca 2+ Channels in Supporting Hippocampal Synaptic Transmission
Wheeler, D. B., Randall, A. D., & Tsien, R. W. (1994) · Science · doi:10.1126/science.7832825 · Cited by 954 · see citing works
Microdomains of High Calcium Concentration in a Presynaptic Terminal
Llinas, R. H., Sugimori, M., & Silver, R. B. (1992) · Science · doi:10.1126/science.1350109 · Cited by 839 · see citing works
Cell Type and Pathway Dependence of Synaptic AMPA Receptor Number and Variability in the Hippocampus
Nusser, Z., Lujan, R., Laube, G., Roberts, J. D. B., Molnar, E., & Somogyi, P. (1998) · Neuron · doi:10.1016/s0896-6273(00)80565-6 · Cited by 804 · see citing works
Self-citationIntracellular calcium dependence of transmitter release rates at a fast central synapse
Schneggenburger, R., & Neher, E. (2000) · Nature · doi:10.1038/35022702 · Cited by 785 · see citing works
Target-cell-specific facilitation and depression in neocortical circuits
Reyes, A., Lujan, R., Rozov, A., Burnashev, N., Somogyi, P., & Sakmann, B. (1998) · Nature Neuroscience · doi:10.1038/1092 · Cited by 716 · see citing works
Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse
Llinas, R. H., Steinberg, I. Z., & Walton, K. D. (1981) · Biophysical Journal · doi:10.1016/s0006-3495(81)84899-0 · Cited by 706 · see citing works
Different modes of expression of AMPA and NMDA receptors in hippocampal synapses
Takumi, Y., Ramírez-León, V., Laake, P., Rinvik, E., & Ottersen, O. P. (1999) · Nature Neuroscience · doi:10.1038/10172 · Cited by 675 · see citing works
Inactivity produces increases in neurotransmitter release and synapse size
Murthy, V. N., Schikorski, T., Stevens, C. F., & Zhu, Y. (2001) · Neuron · doi:10.1016/s0896-6273(01)00500-1 · Cited by 612 · see citing works
Hefft, S., & Jonas, P. (2005) · Nature Neuroscience · doi:10.1038/nn1542 · Cited by 583 · see citing works
Calcium Sensitivity of Glutamate Release in a Calyx-Type Terminal
Bollmann, J. H., Sakmann, B. J., & Borst, J. G. G. (2000) · Science · doi:10.1126/science.289.5481.953 · Cited by 507 · see citing works
Shepherd, G. M. G., & Harris, K. M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08300.1998 · Cited by 502 · see citing works
Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses
Eggermann, E., Bucurenciu, I., Goswami, S. P., & Jonas, P. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3125 · Cited by 500 · see citing works
Estimating Intracellular Calcium Concentrations and Buffering without Wavelength Ratioing
Maravall, M., Mainen, Z. F., Sabatini, B. L., & Svoboda, K. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76809-3 · Cited by 416 · see citing works
Rozov, A., Burnashev, N., Sakmann, B., & Neher, E. (2001) · Journal of Physiology · doi:10.1111/j.1469-7793.2001.0807h.x · Cited by 392 · see citing works
Diversification of synaptic strength: presynaptic elements
Atwood, H. L., & Karunanithi, S. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn876 · Cited by 346 · see citing works
Facilitation at single synapses probed with optical quantal analysis
Oertner, T. G., Sabatini, B. L., Nimchinsky, E. A., & Svoboda, K. (2002) · Nature Neuroscience · doi:10.1038/nn867 · Cited by 324 · see citing works
Xu‐Friedman, M. A., Harris, K. M., & Regehr, W. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06666.2001 · Cited by 313 · see citing works
RIM-Binding Protein, a Central Part of the Active Zone, Is Essential for Neurotransmitter Release
Liu, K. S. Y., Siebert, M., Mertel, S., Knoche, E., Wegener, S., Wichmann, C., Matkovic, T., Muhammad, K., Depner, H., Mettke, C., et al. (2011) · Science · doi:10.1126/science.1212991 · Cited by 306 · see citing works
NMDA Receptor Content of Synapses in Stratum Radiatum of the Hippocampal CA1 Area
Racca, C., Stephenson, F. A., Streit, P., Roberts, J. D. B., & Somogyi, P. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02512.2000 · Cited by 304 · see citing works
Developmental Transformation of the Release Modality at the Calyx of Held Synapse
Fedchyshyn, M. J., & Wang, L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0350-05.2005 · Cited by 298 · see citing works
Molecular Identity of Dendritic Voltage-Gated Sodium Channels
Lőrincz, A., & Nusser, Z. (2010) · Science · doi:10.1126/science.1187958 · Cited by 297 · see citing works
Self-citationCalcium Secretion Coupling at Calyx of Held Governed by Nonuniform Channel–Vesicle Topography
Meinrenken, C., Borst, J. G., & Sakmann, B. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01648.2002 · Cited by 290 · see citing works
Koester, H. J., & Sakmann, B. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00625.x · Cited by 288 · see citing works
Bucurenciu, I., Kulik, A., Schwaller, B., Frotscher, M., & Jonas, P. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.026 · Cited by 274 · see citing works
Thomson, A. M. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.131bl.x · Cited by 270 · see citing works
Ultrafast Exocytosis Elicited by Calcium Current in Synaptic Terminals of Retinal Bipolar Neurons
Mennerick, S. J., & Matthews, G. (1996) · Neuron · doi:10.1016/s0896-6273(00)80254-8 · Cited by 259 · see citing works
Gulyás, A. I., Szabo, G. G., Ulbert, I., Holderith, N. B., Monyer, H., Erdélyi, F., Szabó, G., Freund, T. F., & Hájos, N. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4104-10.2010 · Cited by 257 · see citing works
Self-citationLong-term potentiation: outstanding questions and attempted synthesis
Lisman, J. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1242 · Cited by 240 · see citing works
The Number of Glutamate Receptors Opened by Synaptic Stimulation in Single Hippocampal Spines
Nimchinsky, E. A., Yasuda, R., Oertner, T. G., & Svoboda, K. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5066-03.2004 · Cited by 224 · see citing works
Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses
Koester, H. J., & Johnston, D. (2005) · Science · doi:10.1126/science.1100815 · Cited by 222 · see citing works
Wu, L., & Saggau, P. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05613.1994 · Cited by 217 · see citing works
Korn, H., Mallet, A., Triller, A., & Faber, D. S. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.48.3.679 · Cited by 196 · see citing works
Mechanisms contributing to synaptic Ca 2+ signals and their heterogeneity in hair cells
Frank, T., Khimich, D., Neef, A., & Moser, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813213106 · Cited by 195 · see citing works
Number and Density of AMPA Receptors in Single Synapses in Immature Cerebellum
Tanaka, J., Matsuzaki, M., Tarusawa, E., Momiyama, A., Molnár, E., Kasai, H., & Shigemoto, R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4256-04.2005 · Cited by 171 · see citing works
Kulik, Á., Vida, I., Fukazawa, Y., Guetg, N., Kasugai, Y., Marker, C. L., Rigato, F., Bettler, B., Wickman, K. D., Frotscher, M., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4178-05.2006 · Cited by 141 · see citing works
Losonczy, A., Zhang, L., Shigemoto, R., Somogyi, P., & Nusser, Z. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.020024 · Cited by 129 · see citing works
Self-citationA small number of open Ca2+ channels trigger transmitter release at a central GABAergic synapse
Bucurenciu, I., Bischofberger, J., & Jónás, P. (2009) · Nature Neuroscience · doi:10.1038/nn.2461 · Cited by 125 · see citing works
Propst, J., & Ko, C. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-11-03654.1987 · Cited by 112 · see citing works
Ca2+-dependent enhancement of release by subthreshold somatic depolarization
Christie, J. M., Chiu, D. N., & Jahr, C. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2718 · Cited by 110 · see citing works
High-resolution quantitative visualization of glutamate and GABA receptors at central synapses.
Masugi-Tokita, M., & Shigemoto, R. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.012 · Cited by 109 · see citing works
Reid, C. A., Clements, J. D., & Bekkers, J. M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-08-02738.1997 · Cited by 99 · see citing works
Ohana, O., & Sakmann, B. J. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.135by.x · Cited by 93 · see citing works
Hagiwara, A., Fukazawa, Y., Deguchi‐Tawarada, M., Ohtsuka, T., & Shigemoto, R. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20633 · Cited by 90 · see citing works
Kulik, Á., Nakadate, K., Hagiwara, A., Fukazawa, Y., Luján, R., Saito, H., 昇, 鈴., Futatsugi, A., Mikoshiba, K., Frotscher, M., et al. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03319.x · Cited by 90 · see citing works
DiGregorio, D. A., Peskoff, A., & Vergara, J. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07846.1999 · Cited by 89 · see citing works
Miyazaki, T., Yamasaki, M., Hashimoto, K., Yamazaki, M., Abe, M., Usui, H., Kano, M., Sakimura, K., & Watanabe, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2755-11.2012 · Cited by 83 · see citing works
Self-citationBranco, T., Marra, V., & Staras, K. (2009) · Journal of Structural Biology · doi:10.1016/j.jsb.2009.10.014 · Cited by 68 · see citing works
Atwood, H. L., & Marin, L. (1983) · Cell and Tissue Research · doi:10.1007/bf00215778 · Cited by 63 · see citing works
Synaptic Morphology and Differences in Sensitivity
Fields, R. D., & Ellisman, M. H. (1985) · Science · doi:10.1126/science.3975637 · Cited by 49 · see citing works
Lőrincz, A., Rózsa, B. J., Katona, G., Vizi, E. S., & Tamás, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605412104 · Cited by 47 · see citing works
Self-citation
Flagged first, then by citations
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Sorted by citations
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
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
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
Sleep Drive Is Encoded by Neural Plastic Changes in a Dedicated Circuit
Liu, S., Liu, Q., Tabuchi, M., & Wu, M. N. (2016) · Cell · doi:10.1016/j.cell.2016.04.013 · Cited by 308 · see citing works
Synaptic vesicle recycling: steps and principles
Rizzoli, S. O. (2014) · The EMBO Journal · doi:10.1002/embj.201386357 · Cited by 317 · see citing works
Super-Resolution Imaging of the Extracellular Space in Living Brain Tissue
Tønnesen, J., Inavalli, V. V. G. K., & Nägerl, U. V. (2018) · Cell · doi:10.1016/j.cell.2018.02.007 · Cited by 293 · see citing works
Synaptic mechanisms of pattern completion in the hippocampal CA3 network
Guzman, S. J., Schlögl, A., Frotscher, M., & Jónás, P. (2016) · Science · doi:10.1126/science.aaf1836 · Cited by 281 · see citing works
Shaping Neuronal Fate: Functional Heterogeneity of Direct Microglia-Neuron Interactions
Cserép, C., Pósfai, B., & Dénes, Á. (2021) · Neuron · doi:10.1016/j.neuron.2020.11.007 · Cited by 256 · see citing works
The Synaptic Vesicle Cycle Revisited: New Insights into the Modes and Mechanisms
Chanaday, N. L., Cousin, M. A., Milosevic, I., Watanabe, S., & Morgan, J. R. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1158-19.2019 · Cited by 255 · 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
Nakamura, Y., Harada, H., Kamasawa, N., Matsui, K., Rothman, J. S., Shigemoto, R., Silver, R. A., DiGregorio, D. A., & Takahashi, T. (2015) · Neuron · doi:10.1016/j.neuron.2014.11.019 · Cited by 245 · see citing works
Neher, E. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.038 · Cited by 236 · see citing works
Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states
Ehmann, N., van de Linde, S., Alon, A., Ljaschenko, D., Keung, X. Z., Holm, T., Rings, A., DiAntonio, A., Hallermann, S., Ashery, U., et al. (2014) · Nature Communications · doi:10.1038/ncomms5650 · Cited by 233 · see citing works
Cell-specific STORM super-resolution imaging reveals nanoscale organization of cannabinoid signaling
Dudok, B., Barna, L., Ledri, M., Szabó, S. I., Szabadits, E., Pintér, B., Woodhams, S. G., Henstridge, C. M., Balla, G. Y., Nyilas, R., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3892 · Cited by 227 · see citing works
Self-citationSensory Processing at Ribbon Synapses in the Retina and the Cochlea
Moser, T., Grabner, C. P., & Schmitz, F. (2019) · Physiological Reviews · doi:10.1152/physrev.00026.2018 · Cited by 206 · see citing works
Intracellular cAMP Sensor EPAC: Physiology, Pathophysiology, and Therapeutics Development
Robichaux, W. G., & Cheng, X. (2018) · Physiological Reviews · doi:10.1152/physrev.00025.2017 · Cited by 208 · see citing works
SNAP-25, a Known Presynaptic Protein with Emerging Postsynaptic Functions
Antonucci, F., Corradini, I., Fossati, G., Tomasoni, R., Menna, E., & Matteoli, M. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00007 · Cited by 175 · see citing works
Synaptic diversity enables temporal coding of coincident multisensory inputs in single neurons
Chabrol, F. P., Arenz, A., Wiechert, M. T., Margrie, T. W., & DiGregorio, D. A. (2015) · Nature Neuroscience · doi:10.1038/nn.3974 · Cited by 189 · see citing works
The Diversity of Cortical Inhibitory Synapses
Kubota, Y., Karube, F., Nomura, M., & Kawaguchi, Y. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00027 · Cited by 180 · see citing works
Spontaneous Activity Drives Local Synaptic Plasticity In Vivo
Winnubst, J., Cheyne, J. E., Niculescu, D., & Lohmann, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.029 · Cited by 180 · see citing works
Altered synaptic dynamics during normal brain aging.
Mostany, R., Anstey, J. E., Crump, K. L., Maco, B., Knott, G., & Portera-Cailliau, C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4825-12.2013 · Cited by 179 · see citing works
Bassoon Specifically Controls Presynaptic P/Q-type Ca2+ Channels via RIM-Binding Protein
Davydova, D., Marini, C., King, C., Klueva, J., Bischof, F., Romorini, S., Montenegro‐Venegas, C., Heine, M., Schneider, R., Schröder, M. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.012 · Cited by 172 · see citing works
The interplay between Hebbian and homeostatic synaptic plasticity
Vitureira, N., & Goda, Y. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201306030 · Cited by 152 · see citing works
Calcium Channels and Short-term Synaptic Plasticity
Catterall, W. A., Leal, K., & Nanou, E. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.r112.411645 · Cited by 146 · see citing works
Differential triggering of spontaneous glutamate release by P/Q-, N- and R-type Ca2+ channels
Ermolyuk, Y. S., Alder, F. G., Surges, R., Pavlov, I. Y., Timofeeva, Y., Kullmann, D. M., & Volynski, K. E. (2013) · Nature Neuroscience · doi:10.1038/nn.3563 · Cited by 148 · see citing works
Synaptic vesicles transiently dock to refill release sites
Kusick, G. F., Chin, M., Raychaudhuri, S., Lippmann, K., Adula, K. P., Hujber, E. J., Vu, T., Davis, M. W., Jorgensen, E. M., & Watanabe, S. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00716-1 · Cited by 138 · see citing works
Wu, Y., Huo, L., Maeder, C. I., Feng, W., & Shen, K. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.035 · Cited by 144 · see citing works
Ohn, T., Rutherford, M. A., Jing, Z., Jung, S., Duque-Afonso, C. J., Hoch, G., Picher, M. M., Scharinger, A., Strenzke, N., & Moser, T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1605737113 · Cited by 144 · see citing works
Fusion Competent Synaptic Vesicles Persist upon Active Zone Disruption and Loss of Vesicle Docking
Wang, S. S. H., Held, R. G., Wong, M. Y., Liu, C., Karakhanyan, A., & Kaeser, P. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.005 · Cited by 143 · see citing works
Reddy‐Alla, S., Böhme, M. A., Reynolds, E., Beis, C., Grasskamp, A. T., Mampell, M. M., Maglione, M., Jusyte, M., Rey, U., Babikir, H. A., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.016 · Cited by 141 · see citing works
Indriati, D. W., Kamasawa, N., Matsui, K., Meredith, A. L., Watanabe, M., & Shigemoto, R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2921-12.2013 · Cited by 140 · see citing works
Self-citationRebola, N., Reva, M., Kirizs, T., Szoboszlay, M., Lőrincz, A., Moneron, G., Nusser, Z., & DiGregorio, D. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.014 · Cited by 136 · see citing works
Self-citationSingle excitatory axons form clustered synapses onto CA1 pyramidal cell dendrites
Bloss, E. B., Cembrowski, M. S., Karsh, B., Colonell, J. I., Fetter, R. D., & Spruston, N. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0084-6 · Cited by 125 · see citing works
Rapid active zone remodeling consolidates presynaptic potentiation
Böhme, M. A., McCarthy, A. W., Grasskamp, A. T., Beuschel, C. B., Goel, P., Jusyte, M., Laber, D., Huang, S., Rey, U., Petzoldt, A. G., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08977-6 · Cited by 127 · see citing works
Recurrent synapses and circuits in the CA3 region of the hippocampus: an associative network
Duigou, C. L., Simonnet, J., Teleńczuk, M. T., Fricker, D., & Miles, R. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00262 · Cited by 134 · see citing works
The control of release probability at nerve terminals
Dittman, J. S., & Ryan, T. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0111-3 · Cited by 122 · see citing works
Quantitative optical nanophysiology of Ca2+ signaling at inner hair cell active zones
Neef, J., Urban, N. T., Ohn, T., Frank, T., Jean, P., Hell, S. W., Willig, K. I., & Moser, T. (2018) · Nature Communications · doi:10.1038/s41467-017-02612-y · Cited by 119 · see citing works
Vesicle Tethering on the Surface of Phase-Separated Active Zone Condensates
Wu, X., Ganzella, M., Zhou, J., Zhu, S., Jahn, R., & Zhang, M. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.10.029 · Cited by 119 · see citing works
Mitochondrial Ultrastructure Is Coupled to Synaptic Performance at Axonal Release Sites
Cserép, C., Pósfai, B., Schwarcz, A. D., & Dénes, Á. (2018) · eNeuro · doi:10.1523/eneuro.0390-17.2018 · Cited by 106 · see citing works
Molnár, G., Rózsa, M., Baka, J., Holderith, N., Barzó, P., Nusser, Z., & Tamás, G. (2016) · eLife · doi:10.7554/elife.18167 · Cited by 111 · see citing works
Self-citationThe Bruchpilot cytomatrix determines the size of the readily releasable pool of synaptic vesicles
Matkovic, T., Siebert, M., Knoche, E., Depner, H., Mertel, S., Owald, D., Schmidt, M., Thomas, U., Sickmann, A., Kamin, D., et al. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201301072 · Cited by 110 · see citing works
Akbergenova, Y., Zhang, Y. V., Weiss, S., Cunningham, K. L., & Littleton, J. T. (2018) · eLife · doi:10.7554/elife.38268 · Cited by 112 · see citing works
Mobility of Calcium Channels in the Presynaptic Membrane
Schneider, R., Hosy, E., Kohl, J., Klueva, J., Choquet, D., Thomas, U., Voigt, A., & Heine, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.050 · Cited by 108 · see citing works
Early remodeling of the neocortex upon episodic memory encoding
Bero, A. W., Meng, J., Cho, S., Shen, A. H., Canter, R. G., Ericsson, M., & Tsai, L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408378111 · Cited by 106 · see citing works
Nanoscale-Targeted Patch-Clamp Recordings of Functional Presynaptic Ion Channels
Novák, P., Gorelik, J., Vivekananda, U., Shevchuk, A., Ermolyuk, Y. S., Bailey, R. J., Bushby, A. J., Moss, G. W. J., Rusakov, D. A., Klenerman, D., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.012 · Cited by 105 · see citing works
RIM-BPs Mediate Tight Coupling of Action Potentials to Ca 2+ -Triggered Neurotransmitter Release
Acuna, C., Liu, X., Gonzalez-Suarez, A. D., & Südhof, T. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.027 · Cited by 104 · see citing works
Chindemi, G., Abdellah, M., Amsalem, O., Benavides-Piccione, R., Delattre, V., Doron, M., Ecker, A., Jaquier, A. T., King, J., Kumbhar, P., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30214-w · Cited by 102 · see citing works
Gratz, S. J., Goel, P., Bruckner, J. J., Hernandez, R. X., Khateeb, K., Macleod, G. T., Dickman, D. K., & O’Connor-Giles, K. M. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.3068-18.2019 · Cited by 102 · see citing works
Grauel, M., Maglione, M., Reddy-Alla, S., Willmes, C., Brockmann, M. M., Trimbuch, T., Rosenmund, T., Pangalos, M., Vardar, G., Stumpf, A., et al. (2016) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1605256113 · Cited by 89 · see citing works
Nanodomain Coupling at an Excitatory Cortical Synapse
Schmidt, H., Brachtendorf, S., Arendt, O., Hallermann, S., Ishiyama, S., Bornschein, G., Gall, D., Schiffmann, S. N., Heckmann, M., & Eilers, J. (2012) · Current Biology · doi:10.1016/j.cub.2012.12.007 · Cited by 99 · 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
Control of neuronal voltage-gated calcium ion channels from RNA to protein
Lipscombe, D., Allen, S. E., & Toro, C. P. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.06.008 · Cited by 92 · see citing works
Montero‐Crespo, M., Domínguez-Álvaro, M., Alonso‐Nanclares, L., DeFelipe, J., & Blázquez‐Llorca, L. (2020) · Brain · doi:10.1093/brain/awaa406 · Cited by 88 · see citing works
Nanoscale Structural Plasticity of the Active Zone Matrix Modulates Presynaptic Function
Glebov, O. O., Jackson, R. E., Winterflood, C. M., Owen, D. M., Barker, E. A., Doherty, P., Ewers, H., & Burrone, J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.064 · Cited by 88 · see citing works
Kádková, A., Radecke, J., & Sørensen, J. B. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.09.020 · Cited by 89 · see citing works
Szabo, G. G., Lenkey, N., Holderith, N. B., Andrási, T., Nusser, Z., & Hájos, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-14.2014 · Cited by 87 · see citing works
Self-citationThe functional organization of motor nerve terminals
Slater, C. R. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.09.004 · Cited by 83 · see citing works
Spatiotemporal Regulation of Synaptic Vesicle Fusion Sites in Central Synapses
Maschi, D., & Klyachko, V. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.006 · Cited by 86 · see citing works
Transient Confinement of CaV2.1 Ca2+-Channel Splice Variants Shapes Synaptic Short-Term Plasticity
Heck, J., Parutto, P., Ciuraszkiewicz, A., Bikbaev, A. F., Freund, R., Mitlöhner, J., Andres‐Alonso, M., Fejtová, A., Holcman, D., & Heine, M. (2019) · Neuron · doi:10.1016/j.neuron.2019.04.030 · Cited by 85 · see citing works
Revealing nanostructures in brain tissue via protein decrowding by iterative expansion microscopy
Sarkar, D., Kang, J., Wassie, A. T., Schroeder, M. E., Peng, Z., Tarr, T. B., Tang, A., Niederst, E. D., Young, J. Z., Su, H., et al. (2022) · Nature Biomedical Engineering · doi:10.1038/s41551-022-00912-3 · Cited by 86 · see citing works
Scimemi, A., & Diamond, J. S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3827-12.2012 · Cited by 85 · see citing works
Marra, V., Burden, J. J., Thorpe, J. R., Smith, I. T., Smith, S. L., Häusser, M., Branco, T., & Staras, K. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.042 · Cited by 85 · see citing works
Miki, T., Kaufmann, W. A., Malagón, G., Gomez, L. C., Tabuchi, K., Watanabe, M., Shigemoto, R., & Marty, A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1704470114 · Cited by 84 · see citing works
Self-citationα-Neurexins Together with α2δ-1 Auxiliary Subunits Regulate Ca 2+ Influx through Ca v 2.1 Channels
Brockhaus, J., Schreitmüller, M., Repetto, D., Klatt, O., Reißner, C., Elmslie, K. S., Heine, M., & Missler, M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0511-18.2018 · Cited by 82 · see citing works
Parajuli, L. K., Nakajima, C., Kulik, Á., Matsui, K., Schneider, T., Shigemoto, R., & Fukazawa, Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1142-12.2012 · Cited by 79 · see citing works
Kubota, Y., Kondo, S., Nomura, M., Hatada, S., Yamaguchi, N., Mohamed, A. A., Karube, F., Lübke, J. H. R., & Kawaguchi, Y. (2015) · eLife · doi:10.7554/elife.07919 · Cited by 79 · see citing works
A carbon nanotube tape for serial-section electron microscopy of brain ultrastructure
Kubota, Y., Sohn, J., Hatada, S., Sievers, M., Straehle, J., Gour, A., Neujahr, R., Miki, T., Mikula, S., & Kawaguchi, Y. (2018) · Nature Communications · doi:10.1038/s41467-017-02768-7 · Cited by 75 · see citing works
Subsynaptic spatial organization as a regulator of synaptic strength and plasticity
Chen, H., Tang, A., & Blanpied, T. A. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.05.004 · Cited by 84 · see citing works
Three-dimensional analysis of synapses in the transentorhinal cortex of Alzheimer’s disease patients
Domínguez-Álvaro, M., Montero-Crespo, M., Blazquez-Llorca, L., Insausti, R., DeFelipe, J., & Alonso-Nanclares, L. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0520-6 · Cited by 79 · see citing works
Zhou, K., Stawicki, T. M., Goncharov, A., & Jin, Y. (2013) · eLife · doi:10.7554/elife.01180 · Cited by 79 · see citing works
Homeostatic scaling of active zone scaffolds maintains global synaptic strength
Goel, P., Bergeron, D. D., Böhme, M. A., Nunnelly, L. F., Lehmann, M., Buser, C., Walter, A. M., Sigrist, S. J., & Dickman, D. K. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201807165 · Cited by 75 · see citing works
Toward large-scale connectome reconstructions
Plaza, S. M., Scheffer, L. K., & Chklovskii, D. B. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.019 · Cited by 78 · see citing works
Presynaptic origins of distinct modes of neurotransmitter release
Chanaday, N. L., & Kavalali, E. T. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.03.005 · Cited by 78 · see citing works
Newman, Z. L., Bakshinskaya, D. E., Schultz, R., Kenny, S. J., Moon, S., Aghi, K., Stanley, C., Marnani, N., Li, R., Bleier, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27815-2 · Cited by 71 · see citing works
Dong, W., Radulović, T., Goral, R. O., Thomas, C. I., Montesinos, M. S., Guerrero‐Given, D., Hagiwara, A., Putzke, T., Hida, Y., Abe, M., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.024 · Cited by 70 · see citing works
Molecular Machines Regulating the Release Probability of Synaptic Vesicles at the Active Zone
Körber, C., & Kuner, T. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00005 · Cited by 72 · see citing works
SNAP-25 regulates spine formation through postsynaptic binding to p140Cap
Tomasoni, R., Repetto, D., Morini, R., Elia, C., Gardoni, F., Di Luca, M., Turco, E., Defilippi, P., & Matteoli, M. (2013) · Nature Communications · doi:10.1038/ncomms3136 · Cited by 71 · see citing works
Dynamical Organization of Syntaxin-1A at the Presynaptic Active Zone
Ullrich, A., Böhme, M. A., Schöneberg, J., Depner, H., Sigrist, S. J., & Noé, F. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004407 · Cited by 72 · see citing works
Local Efficacy of Glutamate Uptake Decreases with Synapse Size
Herde, M. K., Bohmbach, K., Domingos, C., Vana, N., Komorowska‐Müller, J. A., Passlick, S., Schwarz, I., Jackson, C. J., Dietrich, D., Schwarz, M. K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108182 · Cited by 71 · see citing works
Presynaptic Active Zone Plasticity Encodes Sleep Need in Drosophila
Huang, S., Piao, C., Beuschel, C. B., Götz, T., & Sigrist, S. J. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.019 · Cited by 70 · see citing works
Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function
Muhammad, K., Reddy‐Alla, S., Driller, J. H., Schreiner, D., Rey, U., Böhme, M. A., Hollmann, C., Ramesh, N., Depner, H., Lützkendorf, J., et al. (2015) · Nature Communications · doi:10.1038/ncomms9362 · Cited by 67 · see citing works
Fekete, Á., Nakamura, Y., Yang, Y., Herlitze, S., Mark, M. D., DiGregorio, D. A., & Wang, L. (2019) · Nature Communications · doi:10.1038/s41467-019-08452-2 · Cited by 69 · see citing works
Takács, V. T., Szőnyi, A., Freund, T. F., Nyíri, G., & Gulyás, A. I. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0692-6 · Cited by 69 · see citing works
Miki, T., Nakamura, Y., Malagon, G., Neher, E., & Marty, A. (2018) · Nature Communications · doi:10.1038/s41467-018-06336-5 · Cited by 53 · see citing works
Presynaptic morphogenesis, active zone organization and structural plasticity in Drosophila
Vactor, D. V., & Sigrist, S. J. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.003 · Cited by 67 · see citing works
Rodriguez-Moreno, J., Rollenhagen, A., Arlandis, J., Santuy, A., Merchán-Pérez, Á., DeFelipe, J., Lübke, J. H. R., & Clascá, F. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx187 · Cited by 65 · see citing works
A Modular Organization of LRR Protein-Mediated Synaptic Adhesion Defines Synapse Identity.
Schroeder, A., Vanderlinden, J., Vints, K., Ribeiro, L. F., Vennekens, K. M., Gounko, N. V., Wierda, K. D., & de Wit, J. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.026 · Cited by 60 · see citing works
SNARE Regulatory Proteins in Synaptic Vesicle Fusion and Recycling
Sauvola, C. W., & Littleton, J. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.733138 · Cited by 53 · see citing works
Ariel, P., Hoppa, M. B., & Ryan, T. A. (2013) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2012.00009 · Cited by 67 · see citing works
Synapse-Level Determination of Action Potential Duration by K + Channel Clustering in Axons
Rowan, M. J. M., DelCanto, G., Yu, J. J., Kamasawa, N., & Christie, J. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.035 · Cited by 66 · see citing works
Prichard, K. L., O’Brien, N. S., Murcia, S. R., Baker, J. R., & McCluskey, A. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.754110 · Cited by 67 · see citing works
Fife organizes synaptic vesicles and calcium channels for high-probability neurotransmitter release
Bruckner, J. J., Zhan, H., Gratz, S., Rao, M., Ukken, F. P., Zilberg, G., & O'Connor-Giles, K. M. (2017) · Journal of Cell Biology · doi:10.1083/jcb.201601098 · Cited by 55 · see citing works
Bourne, J. N., Chirillo, M. A., & Harris, K. M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23384 · Cited by 65 · see citing works
Santuy, A., Rodríguez, J., DeFelipe, J., & Merchán-Pérez, Á. (2018) · eNeuro · doi:10.1523/eneuro.0377-17.2017 · Cited by 61 · see citing works
Vesicular Release Statistics and Unitary Postsynaptic Current at Single GABAergic Synapses
Pulido, C., Trigo, F. F., Llano, I., & Marty, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.12.006 · Cited by 58 · see citing works
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
The SNARE Proteins SNAP25 and Synaptobrevin Are Involved in Endocytosis at Hippocampal Synapses
Zhang, Z., Wang, D., Sun, T., Xu, J., Chiang, H., Shin, W., & Wu, L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0301-13.2013 · Cited by 61 · see citing works
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
Rodriguez-Moreno, J., Porrero, C., Rollenhagen, A., Rubio-Teves, M., Casas-Torremocha, D., Alonso‐Nanclares, L., Yakoubi, R., Santuy, A., Merchán-Pérez, Á., DeFelipe, J., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2886-19.2020 · Cited by 60 · see citing works
Three-dimensional synaptic organization of the human hippocampal CA1 field
Montero-Crespo, M., Dominguez-Alvaro, M., Rondon-Carrillo, P., Alonso-Nanclares, L., DeFelipe, J., & Blazquez-Llorca, L. (2020) · eLife · doi:10.7554/elife.57013 · Cited by 60 · see citing works
- Authors
- Holderith, N., Lorincz, A., Katona, G., Rózsa, B., Kulik, A., Watanabe, M., & Nusser, Z.
- Affiliations
- HUN-REN Institute of Experimental Medicine (HU)
- Hokkaido University (JP)
- Venue
- Nature Neuroscience
- Published
- 2012-06-10
- Volume
- 15
- Issue
- 7
- Pages
- 988-997
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3386897
- OpenAlex
- W2093514926
- Cited by
- 405
- References
- 56
- Citations by year
- 2026: 3 · 2025: 15 · 2024: 29 · 2023: 29 · 2022: 30 · 2021: 32 · 2020: 38 · 2019: 28 · 2018: 39 · 2017: 24 · 2016: 30 · 2015: 36 · 2014: 34 · 2013: 32 · 2012: 6
- FWCI
- 14.24
- Type
- journal article
- Language
- en
- Update notices
- erratum (2015-12-29)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Wellcome Trust (083484, 090197, 094513, 083484/Z/07/Z, 090197/Z/09/Z, 094513/Z/10/Z)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- release probability, active zone, glutamatergic synapses, CA3 pyramidal cells, voltage-gated calcium channels, Cav2.1, docked vesicles, synaptic ultrastructure, two-photon calcium imaging
- MeSH terms
- Action Potentials, Animals, Hippocampus, Male, Random Allocation, Synaptic Vesicles, Rats, Wistar, Presynaptic Terminals, Calcium Channels, N-Type, Rats
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