Superpriming of synaptic vesicles as a common basis for intersynapse variability and modulation of synaptic strength
Open accessAbstract
Significance: Short-term plasticity (STP) of synaptic connections underlies many basic signal processing capabilities of the brain, such as gain control, temporal filtering, and adaptation. Glutamatergic synapses, the predominant excitatory synapses in the brain, display large variability both in basal synaptic strength and in STP. We show that a small fraction of release-ready vesicles are released with much higher probability than other vesicles. The number of these “superprimed” vesicles is variable among synapses, but increases strongly after application of phorbol ester, an analogue of the second messenger diacylglycerol, and after inducing posttetanic potentiation. Thus, modulatory transmitter systems, acting through the phospholipase-C–diacylglycerol pathway, will be able to upregulate superprimed vesicles and thereby boost synaptic strength at the onset of burst-like activity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
These might be "superprimed" vesicles.
“These might be “superprimed” vesicles [84,85].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [85]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
RETRACTED: Protein kinase C is a calcium sensor for presynaptic short-term plasticity
Fioravante, D., Chu, Y., de Jong, A. P. H., Leitges, M., Kaeser, P. S., & Regehr, W. G. (2014) · eLife · doi:10.7554/elife.03011 · Cited by 17 · see citing works
RetractedShort-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068 · see citing works
Synaptic depression and cortical gain control
Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997) · Science · doi:10.1126/science.275.5297.221 · Cited by 1,690 · see citing works
Synaptic theory of working memory
Mongillo, G., Barak, O., & Tsodyks, M. (2008) · Science · doi:10.1126/science.1150769 · Cited by 1,253 · see citing works
Heterogeneity of release probability, facilitation, and depletion at central synapses
Dobrunz, L. E., & Stevens, C. F. (1997) · Neuron · doi:10.1016/s0896-6273(00)80338-4 · Cited by 1,183 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
An optimized fluorescent probe for visualizing glutamate neurotransmission
Marvin, J. S., Borghuis, B. G., Tian, L., Cichon, J., Harnett, M. T., Akerboom, J., Gordus, A. G., Renninger, S. L., Chen, T., Bargmann, C. I., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2333 · Cited by 1,006 · see citing works
Neuromodulation of Brain States
Lee, S., & Dan, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.012 · Cited by 666 · see citing works
Schneggenburger, R., Meyer, A. C., & Neher, E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80789-8 · Cited by 621 · see citing works
Self-citationThe probability of transmitter release at a mammalian central synapse
Hessler, N. A., Shirke, A. M., & Malinow, R. (1993) · Nature · doi:10.1038/366569a0 · Cited by 617 · see citing works
Nonuniform probability of glutamate release at a hippocampal synapse.
Rosenmund, C., Clements, J., & Westbrook, G. (1993) · Science · doi:10.1126/science.7901909 · Cited by 616 · see citing works
Debanne, D., Guérineau, N. C., Gähwiler, B. H., & Thompson, S. M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021204 · Cited by 613 · see citing works
Heterogeneous Release Properties of Visualized Individual Hippocampal Synapses
Murthy, V. N., B, T. J. S. A., & Stevens, C. F. (1997) · Neuron · doi:10.1016/s0896-6273(00)80301-3 · Cited by 596 · see citing works
Taschenberger, H., & von Gersdorff, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09162.2000 · Cited by 486 · see citing works
Self-citationPresynaptic Calcium Current Modulation by a Metabotropic Glutamate Receptor
Takahashi, T., Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M., & Onodera, K. (1996) · Science · doi:10.1126/science.274.5287.594 · Cited by 392 · see citing works
Short-term forms of presynaptic plasticity
Fioravante, D., & Regehr, W. G. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.003 · Cited by 375 · see citing works
Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse.
Sakaba, T., & Neher, E. (2001) · Neuron · doi:10.1016/s0896-6273(01)00543-8 · Cited by 355 · see citing works
Self-citationRIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone
Han, Y., Kaeser, P. S., Südhof, T. C., & Schneggenburger, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.014 · Cited by 354 · see citing works
Junge, H. J., Rhee, J.-S., Jahn, O., Varoqueaux, F., Spiess, J., Waxham, M. N., Rosenmund, C., & Brose, N. (2004) · Cell · doi:10.1016/j.cell.2004.06.029 · Cited by 290 · see citing works
A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?
Dulubova, I., Lou, X., Lu, J., Huryeva, I., Alam, A., Schneggenburger, R., Südhof, T. C., & Rizo, J. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600753 · Cited by 289 · see citing works
The Coupling between Synaptic Vesicles and Ca2+ Channels Determines Fast Neurotransmitter Release
Wadel, K., Neher, E., & Sakaba, T. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.021 · Cited by 248 · see citing works
Self-citationNeher, E. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.038 · Cited by 236 · see citing works
Self-citationMunc13-1 C1 Domain Activation Lowers the Energy Barrier for Synaptic Vesicle Fusion
Basu, J., Betz, A., Brose, N., & Rosenmund, C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4908-06.2007 · Cited by 226 · see citing works
Interdependence of PKC-Dependent and PKC-Independent Pathways for Presynaptic Plasticity
Wierda, K. D. B., Toonen, R. F. G., de Wit, H., Brussaard, A. B., & Verhage, M. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.001 · Cited by 225 · see citing works
Bassoon speeds vesicle reloading at a central excitatory synapse
Hallermann, S., Fejtova, A., Schmidt, H., Weyhersmüller, A., Silver, R. A., Gundelfinger, E. D., & Eilers, J. (2010) · Neuron · doi:10.1016/j.neuron.2010.10.026 · Cited by 223 · see citing works
Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity
Schlüter, O. M., Basu, J., Südhof, T. C., & Rosenmund, C. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3553-05.2006 · Cited by 199 · cited 5× · see citing works
“In hippocampal synapses, superpriming was shown to depend on the presence of at least one isoform of rab3 (32).”
BackgroundInfluentialRegulation of Membrane Fusion in Synaptic Excitation-Secretion Coupling: Speed and Accuracy Matter
Wojcik, S. M., & Brose, N. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.013 · Cited by 191 · see citing works
Synaptic depression in the localization of sound
Cook, D. L., Schwindt, P. C., Grande, L. A., & Spain, W. J. (2003) · Nature · doi:10.1038/nature01248 · Cited by 190 · see citing works
Magleby, K. L., & Zengel, J. E. (1976) · The Journal of Physiology · doi:10.1113/jphysiol.1976.sp011378 · Cited by 159 · see citing works
Kushmerick, C., Renden, R., & von Gersdorff, H. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3889-05.2006 · Cited by 156 · see citing works
Presynaptic Mechanism for Phorbol Ester-Induced Synaptic Potentiation
Hori, T., Takai, Y., & Takahashi, T. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07262.1999 · Cited by 145 · see citing works
Minimizing Synaptic Depression by Control of Release Probability
Brenowitz, S. D., & Trussell, L. O. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-01857.2001 · Cited by 144 · see citing works
Lou, X., Korogod, N., Brose, N., & Schneggenburger, R. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0550-08.2008 · Cited by 140 · see citing works
Sakaba, T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0182-06.2006 · Cited by 134 · see citing works
Short-Term Plasticity of a Thalamocortical Pathway Dynamically Modulated by Behavioral State
Castro‐Alamancos, M. A., & Connors, B. W. (1996) · Science · doi:10.1126/science.272.5259.274 · Cited by 129 · see citing works
Wölfel, M., Lou, X., & Schneggenburger, R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4471-06.2007 · Cited by 125 · see citing works
The medial nucleus of the trapezoid body: Comparative physiology
Kopp‐Scheinpflug, C., Tolnai, S., Malmierca, M. S., & Rübsamen, R. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.088 · Cited by 123 · see citing works
Schotten, S., Meijer, M., Walter, A. M., Huson, V., Mamer, L., Kalogreades, L., ter Veer, M. J. T., Ruiter, M., Brose, N., Rosenmund, C., et al. (2015) · eLife · doi:10.7554/elife.05531 · Cited by 102 · see citing works
Isaacson, J. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.3.1571 · Cited by 99 · see citing works
Hanse, E., & Gustafsson, B. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0481i.x · Cited by 96 · see citing works
Korogod, N., Lou, X., & Schneggenburger, R. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1295-05.2005 · Cited by 96 · see citing works
Presynaptic signal transduction pathways that modulate synaptic transmission
de Jong, A. P. H., & Verhage, M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.06.005 · Cited by 94 · see citing works
Superpriming of synaptic vesicles after their recruitment to the readily releasable pool
Lee, J. S., Ho, W., Neher, E., & Lee, S.-H. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1314427110 · Cited by 85 · see citing works
Self-citationSoftware-based correction of single compartment series resistance errors
Traynelis, S. F. (1998) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(98)00140-x · Cited by 84 · see citing works
Lee, J. S., Kim, M., Ho, W., & Lee, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2165-08.2008 · Cited by 80 · see citing works
von der Malsburg, C., & Bienenstock, E. (1986) · Springer eBooks · doi:10.1007/978-3-642-82657-3_26 · Cited by 72 · see citing works
Billups, B., Graham, B. P., Wong, A. Y. C., & Forsythe, I. D. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.086736 · Cited by 72 · see citing works
Wu, X., & Wu, L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-07928.2001 · Cited by 71 · see citing works
Munc18-1 is a dynamically regulated PKC target during short-term enhancement of transmitter release
Genç, Ö., Kochubey, O., Toonen, R. F. G., Verhage, M., & Schneggenburger, R. (2014) · eLife · doi:10.7554/elife.01715 · Cited by 69 · see citing works
Müller, M., Goutman, J., Kochubey, O., & Schneggenburger, R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4378-09.2010 · Cited by 67 · see citing works
Chang, S., Reim, K., Pedersen, M., Neher, E., Brose, N., & Taschenberger, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4841-14.2015 · Cited by 66 · see citing works
Self-citationGrande, G., & Wang, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0400-11.2011 · Cited by 62 · see citing works
Habets, R., & Borst, J. G. (2007) · Journal of Physiology · doi:10.1113/jphysiol.2006.127365 · Cited by 54 · see citing works
Modulation of Presynaptic Release Probability by the Vertebrate-Specific Protein Mover
Körber, C., Horstmann, H., Venkataramani, V., Herrmannsdörfer, F., Kremer, T., Kaiser, M., Schwenger, D. B., Ahmed, S., Dean, C., Dresbach, T., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.001 · Cited by 52 · see citing works
Banitt, Y., Martin, K. A. C., & Segev, I. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1640-07.2007 · Cited by 52 · see citing works
Facilitation, Augmentation, and Potentiation of Transmitter Release
Magleby, K. L. (1979) · Progress in brain research · doi:10.1016/s0079-6123(08)64631-2 · Cited by 49 · see citing works
Vesicle pool partitioning influences presynaptic diversity and weighting in rat hippocampal synapses
Waters, J., & Smith, S. J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013485 · Cited by 46 · see citing works
Hanse, E., & Gustafsson, B. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0141k.x · Cited by 45 · see citing works
Montesinos, M. S., Dong, W., Goff, K. M., Das, B., Guerrero‐Given, D., Schmalzigaug, R., Premont, R. T., Satterfield, R., Kamasawa, N., & Young, S. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.042 · Cited by 41 · see citing works
Ishiyama, S., Schmidt, H., Cooper, B. H., Brose, N., & Eilers, J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2060-14.2014 · Cited by 40 · see citing works
Yao, L., & Sakaba, T. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00685.2010 · Cited by 31 · see citing works
Augmentation controls the fast rebound from depression at excitatory hippocampal synapses.
García-Pérez, E., & Wesseling, J. F. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01348.2007 · Cited by 30 · see citing works
Translating neuronal activity at the synapse: presynaptic calcium sensors in short-term plasticity
de Jong, A. P. H., & Fioravante, D. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00356 · Cited by 27 · see citing works
Wang, T., Rusu, S. I., Hruskova, B., Tureček, R., & Borst, J. G. G. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.256875 · Cited by 19 · see citing works
Chanda, S., & Xu‐Friedman, M. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1193-11.2011 · Cited by 19 · see citing works
Dynamic aspects of presynaptic calcium currents mediating synaptic transmission
Takahashi, T. (2005) · Cell Calcium · doi:10.1016/j.ceca.2005.01.018 · Cited by 18 · see citing works
The functional landscape of a presynaptic nerve terminal
Cano, R., Ruiz, R., Shen, C., Tabares, L., & Betz, W. J. (2012) · Cell Calcium · doi:10.1016/j.ceca.2012.04.012 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dynamically Primed Synaptic Vesicle States: Key to Understand Synaptic Short-Term Plasticity
Neher, E., & Brose, N. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.024 · Cited by 210 · see citing works
Self-citationUltrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapses
Helassa, N., Dürst, C. D., Coates, C., Kerruth, S., Arif, U., Schulze, C., Wiegert, J. S., Geeves, M. A., Oertner, T. G., & Török, K. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720648115 · Cited by 149 · 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
Vandael, D., Borges-Merjane, C., Zhang, X., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.013 · Cited by 114 · see citing works
Munc13-1 and Munc18-1 together prevent NSF-dependent de-priming of synaptic vesicles
He, E., Wierda, K. D. B., van Westen, R., Broeke, J. H. P., Toonen, R. F. G., Cornelisse, L. N., & Verhage, M. (2017) · Nature Communications · doi:10.1038/ncomms15915 · Cited by 97 · see citing works
Lin, K., Taschenberger, H., & Neher, E. (2022) · bioRxiv · doi:10.1073/pnas.2207987119 · Cited by 57 · see citing works
Self-citationMiki, 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
Calcium-dependent docking of synaptic vesicles
Silva, M., Tran, V., & Marty, A. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.04.003 · Cited by 82 · see citing works
A C1–C2 Module in Munc13 Inhibits Calcium-Dependent Neurotransmitter Release
Michelassi, F., Liu, H.-W., Hu, Z.-T., & Dittman, J. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.015 · Cited by 72 · see citing works
Unc13: A multifunctional synaptic marvel
Dittman, J. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.12.011 · Cited by 78 · 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
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
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
Self-citationUltrastructural Correlates of Presynaptic Functional Heterogeneity in Hippocampal Synapses
Maus, L., Lee, C., Altas, B., Sertel, S. M., Weyand, K., Rizzoli, S. O., Rhee, J., Brose, N., Imig, C., & Cooper, B. H. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.083 · Cited by 67 · see citing works
Homozygous STXBP1 variant causes encephalopathy and gain-of-function in synaptic transmission
Lammertse, H. C. A., van Berkel, A. A., Iacomino, M., Toonen, R. F. G., Striano, P., Gambardella, A., Verhage, M., & Zara, F. (2019) · Brain · doi:10.1093/brain/awz391 · Cited by 64 · see citing works
Stange-Marten, A., Nabel, A. L., Sinclair, J. L., Fischl, M. J., Alexandrova, O., Wohlfrom, H., Kopp‐Scheinpflug, C., Pecka, M., & Grothe, B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1702290114 · Cited by 61 · 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
Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts
Raja, M. K., Preobraschenski, J., Olmo-Cabrera, S. D., Martínez-Turrillas, R., Jahn, R., Pérez‐Otaño, I., & Wesseling, J. F. (2019) · eLife · doi:10.7554/elife.40744 · Cited by 57 · see citing works
Calcium dependence of neurotransmitter release at a high fidelity synapse
Eshra, A., Schmidt, H., Eilers, J., & Hallermann, S. (2021) · bioRxiv · doi:10.7554/elife.70408 · Cited by 34 · see citing works
Kobbersmed, J. R., Grasskamp, A. T., Jusyte, M., Böhme, M. A., Ditlevsen, S., Sørensen, J. B., & Walter, A. M. (2020) · eLife · doi:10.7554/elife.51032 · Cited by 56 · see citing works
Munc13- and SNAP25-dependent molecular bridges play a key role in synaptic vesicle priming
Papantoniou, C., Laugks, U., Betzin, J., Capitanio, C., Ferrero, J. J., Sánchez‐Prieto, J., Schoch, S., Brose, N., Baumeister, W. P., Cooper, B. H., et al. (2023) · Science Advances · doi:10.1126/sciadv.adf6222 · Cited by 55 · see citing works
Some Subtle Lessons from the Calyx of Held Synapse
Neher, E. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2016.12.017 · Cited by 46 · see citing works
Self-citationLipstein, N., Chang, S., Lin, K., López-Murcia, F. J., Neher, E., Taschenberger, H., & Brose, N. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.054 · Cited by 52 · see citing works
Self-citationAldahabi, M., Balint, F., Holderith, N., Lorincz, A., Reva, M., & Nusser, Z. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.035 · Cited by 50 · see citing works
The Cerebellar Mossy Fiber Synapse as a Model for High-Frequency Transmission in the Mammalian CNS
Delvendahl, I., & Hallermann, S. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.09.006 · Cited by 50 · 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
Ortega, J. M., Genç, Ö., & Davis, G. W. (2018) · eLife · doi:10.7554/elife.40385 · Cited by 38 · see citing works
Chamberland, S., Timofeeva, Y., Evstratova, A., Volynski, K. E., & Tóth, K. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720659115 · Cited by 38 · see citing works
Apparent calcium dependence of vesicle recruitment
Ritzau‐Jost, A., Jablonski, L., Viotti, J., Lipstein, N., Eilers, J., & Hallermann, S. (2018) · The Journal of Physiology · doi:10.1113/jp275911 · Cited by 38 · see citing works
Variability in the Munc13-1 content of excitatory release sites.
Karlocai, M. R., Heredi, J., Benedek, T., Holderith, N., Lorincz, A., & Nusser, Z. (2021) · eLife · doi:10.7554/elife.67468 · Cited by 37 · see citing works
High-speed imaging of glutamate release with genetically encoded sensors
Dürst, C. D., Wiegert, J. S., Helassa, N., Kerruth, S., Coates, C., Schulze, C., Geeves, M. A., Török, K., & Oertner, T. G. (2019) · Nature Protocols · doi:10.1038/s41596-019-0143-9 · Cited by 37 · see citing works
Doc2-mediated superpriming supports synaptic augmentation
Xue, R., Ruhl, D. A., Briguglio, J. S., Figueroa, A. G., Pearce, R., & Chapman, E. (2018) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1802104115 · Cited by 29 · see citing works
Neher, E. (2023) · The Journal of General Physiology · doi:10.1085/jgp.202313454 · Cited by 34 · see citing works
Self-citationNeurosecretion: what can we learn from chromaffin cells
Neher, E. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-2051-6 · Cited by 34 · see citing works
Self-citationA two-step docking site model predicting different short-term synaptic plasticity patterns
Pulido, C., & Marty, A. (2018) · The Journal of General Physiology · doi:10.1085/jgp.201812072 · Cited by 33 · see citing works
Sakmann, B. J. (2017) · Experimental Physiology · doi:10.1113/ep085776 · Cited by 33 · see citing works
Cognitive synaptopathy: synaptic and dendritic spine dysfunction in age-related cognitive disorders
Barrantes, F. J. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1476909 · Cited by 31 · see citing works
Presynaptic Diversity Revealed by Ca 2+ -Permeable AMPA Receptors at the Calyx of Held Synapse
Lujan, B., Dagostin, A., & von Gersdorff, H. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2565-18.2019 · Cited by 30 · see citing works
Advances in Engineering and Application of Optogenetic Indicators for Neuroscience
Piatkevich, K. D., Murdock, M. H., & Subach, F. V. (2019) · Applied Sciences · doi:10.3390/app9030562 · Cited by 30 · see citing works
“Kiss-shrink-run” unifies mechanisms for synaptic vesicle exocytosis and hyperfast recycling
Tao, C.-L., Tian, C.-L., Liu, Y.-T., Lu, Z.-H., Qi, L., Li, X., Li, C., Shen, X., Gu, M., Huang, W.-L., et al. (2025) · Science · doi:10.1126/science.ads7954 · Cited by 29 · see citing works
Morphofunctional changes at the active zone during synaptic vesicle exocytosis
Radecke, J., Seeger, R., Kádková, A., Laugks, U., Khosrozadeh, A., Goldie, K. N., Lučić, V., Sørensen, J. B., & Zuber, B. (2023) · EMBO Reports · doi:10.15252/embr.202255719 · Cited by 29 · see citing works
Single Bursts of Individual Granule Cells Functionally Rearrange Feedforward Inhibition
Neubrandt, M., Oláh, V. J., Brunner, J., Marosi, E. L., Soltész, I., & Szabadics, J. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1595-17.2018 · Cited by 28 · see citing works
Platzer, K., Sticht, H., Bupp, C. P., Ganapathi, M., Pereira, E. M., Guyader, G. L., Bilan, F., Henderson, L. B., Lemke, J. R., Taschenberger, H., et al. (2022) · Annals of Neurology · doi:10.1002/ana.26485 · Cited by 27 · see citing works
Self-citationJusyte, M., Blaum, N., Böhme, M. A., Berns, M. M. M., Bonard, A. E., Vámosi, Á. B., Pushpalatha, K. V., Kobbersmed, J. R., & Walter, A. M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112541 · Cited by 27 · see citing works
Farsi, Z., Walde, M., Klementowicz, A. E., Paraskevopoulou, F., & Woehler, A. (2020) · iScience · doi:10.1016/j.isci.2020.101909 · Cited by 25 · see citing works
Self-citationTran, V., Miki, T., & Marty, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114469119 · Cited by 27 · see citing works
Butola, T., Alvanos, T., Hintze, A., Koppensteiner, P., Kleindienst, D., Shigemoto, R., Wichmann, C., & Moser, T. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0586-21.2021 · Cited by 22 · see citing works
Neher, E., & Taschenberger, H. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.10.012 · Cited by 15 · see citing works
Self-citationFully-primed slowly-recovering vesicles mediate presynaptic LTP at neocortical neurons
Weichard, I., Taschenberger, H., Gsell, F., Bornschein, G., Ritzau‐Jost, A., Schmidt, H., Kittel, R. J., Eilers, J., Neher, E., Hallermann, S., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2305460120 · Cited by 22 · see citing works
Self-citationUnc13 Aligns SNAREs and Superprimes Synaptic Vesicles
Palfreyman, M. T., & Jørgensen, E. M. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.017 · Cited by 23 · see citing works
Kinetics of transmitter release at the calyx of Held synapse
Sakaba, T. (2018) · Proceedings of the Japan Academy. Series B, Physical and biological sciences · doi:10.2183/pjab.94.010 · Cited by 17 · see citing works
Regulation of a subset of release-ready vesicles by the presynaptic protein Mover
Pofantis, E., Neher, E., & Dresbach, T. (2021) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2022551118 · Cited by 9 · see citing works
Self-citationPresynaptic GCaMP expression decreases vesicle release probability at the calyx of Held
Singh, M., Lujan, B., & Renden, R. (2018) · Synapse · doi:10.1002/syn.22040 · Cited by 18 · see citing works
Aldahabi, M., Neher, E., & Nusser, Z. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2322550121 · Cited by 15 · see citing works
Self-citationGuzman, G. A., Guzman, R. E., Jordan, N., & Hidalgo, P. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00125 · Cited by 16 · see citing works
Kim, O., Okamoto, Y., Kaufmann, W. A., Brose, N., Shigemoto, R., & Jonas, P. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002879 · Cited by 15 · see citing works
Exact Distribution of the Quantal Content in Synaptic Transmission
Rijal, K., Müller, N. I. C., Friauf, E., Singh, A., Prasad, A., & Das, D. (2024) · Physical Review Letters · doi:10.1103/physrevlett.132.228401 · Cited by 15 · see citing works
Distinct temporal filters in mitral cells and external tufted cells of the olfactory bulb
Vaaga, C. E., & Westbrook, G. L. (2017) · The Journal of Physiology · doi:10.1113/jp274608 · Cited by 15 · see citing works
Bera, M., Grushin, K. S., Sundaram, R. V. K., Hinzen, J. S., Chen, J., Chatterjee, A., Radhakrishnan, A., Lee, S., Padmanarayana, M., Coleman, J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-62420-7 · Cited by 15 · see citing works
Novel types of frequency filtering in the lateral perforant path projections to dentate gyrus
Quintanilla, J., Jia, Y., Lauterborn, J. C., Pruess, B. S., Le, A. A., Cox, C. D., Gall, C. M., LYNCH, G. S., & Gunn, B. G. (2022) · The Journal of Physiology · doi:10.1113/jp283012 · Cited by 14 · see citing works
Mechanistic insights into cAMP-mediated presynaptic potentiation at hippocampal mossy fiber synapses
Fukaya, R., Miyano, R., Hirai, H., & Sakaba, T. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1237589 · Cited by 13 · see citing works
Silva, M., Tran, V., & Marty, A. (2023) · eLife · doi:10.7554/elife.91087 · Cited by 14 · see citing works
Huson, V., Meijer, M., Dekker, M. P., ter Veer, M. J. T., Ruiter, M., van Weering, J. R. T., Verhage, M., & Cornelisse, L. N. (2020) · eLife · doi:10.7554/elife.55713 · Cited by 14 · see citing works
The M domain in UNC-13 regulates the probability of neurotransmitter release
Liu, H., Li, L., Sheoran, S., Yu, Y., Richmond, J. E., Xia, J., Tang, J., Liu, J., & Hu, Z. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108828 · Cited by 13 · see citing works
Gallimore, A. R., Hepburn, I., Georgiev, S. V., Rizzoli, S. O., & Schutter, E. D. (2025) · Science Advances · doi:10.1126/sciadv.adq6477 · Cited by 13 · see citing works
Molecular mechanisms of homeostatic plasticity in central pattern generator networks
Northcutt, A. J., & Schulz, D. J. (2019) · Developmental Neurobiology · doi:10.1002/dneu.22727 · Cited by 14 · see citing works
López-Murcia, F. J., Lin, K., Berns, M. M. M., Ranjan, M., Lipstein, N., Neher, E., Brose, N., Reim, K., & Taschenberger, H. (2024) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2320505121 · Cited by 13 · see citing works
Self-citationHigh Entrainment Constrains Synaptic Depression Levels of an In vivo Globular Bushy Cell Model
Rudnicki, M., & Hemmert, W. (2017) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2017.00016 · Cited by 12 · see citing works
Quantum propensities in the brain cortex and free will
Georgiev, D. D. (2021) · Biosystems · doi:10.1016/j.biosystems.2021.104474 · Cited by 12 · see citing works
Chipman, P. H., Lee, U., Orr, B. O., Fetter, R. D., & Davis, G. W. (2025) · Neuron · doi:10.1016/j.neuron.2025.05.030 · Cited by 11 · see citing works
Lin, K., Ranjan, M., Lipstein, N., Brose, N., Neher, E., & Taschenberger, H. (2025) · The Journal of Physiology · doi:10.1113/jp286282 · Cited by 11 · see citing works
Self-citationHu, H., Wang, X., Li, C., Li, Y., Hao, J.-F., Zhou, Y., Yang, X., Chen, P.-H., Shen, X.-F., & Zhang, S.-L. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.10.020 · Cited by 7 · see citing works
Kádková, A., Murach, J., Østergaard, M., Malsam, A., Malsam, J., Lolicato, F., Nickel, W., Söllner, T. H., & Sørensen, J. B. (2024) · eLife · doi:10.7554/elife.88619 · Cited by 10 · see citing works
Nestvogel, D., Merino, R. M., Leon-Pinzon, C., Schottdorf, M., Lee, C., Imig, C., Brose, N., & Rhee, J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.045 · Cited by 10 · see citing works
Morphofunctional changes at the active zone during synaptic vesicle exocytosisPreprint
Radecke, J., Seeger, R., Kádková, A., Laugks, U., Khosrozadeh, A., Goldie, K. N., Lučić, V., Sørensen, J. B., & Zuber, B. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.07.483217 · Cited by 10 · see citing works
SNARE Proteins in Synaptic Vesicle Fusion
Palfreyman, M. T., West, S. E., & Jørgensen, E. M. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-34229-5_4 · Cited by 10 · see citing works
Gustafsson, B., Ma, R., & Hanse, E. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00007 · Cited by 9 · see citing works
Wesseling, J. F. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00032 · Cited by 9 · see citing works
Hain, P. J. H., & Moser, T. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1351280 · Cited by 8 · see citing works
Modulation of Neural Microcircuits That Control Complex Dynamics in Olfactory Networks
Huang, Z., Tatti, R., Loeven, A. M., Conde, D. R. L., & Fadool, D. A. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.662184 · Cited by 7 · see citing works
A two-subpopulation model that reflects heterogeneity of large dense core vesicles in exocytosis
Qin, N., Chen, Z., & Xue, R. (2022) · Cell Cycle · doi:10.1080/15384101.2022.2026576 · Cited by 8 · see citing works
Species-Specific Adaptation for Ongoing High-Frequency Action Potential Generation in MNTB Neurons
Kladisios, N., Wicke, K. D., Pätz, C., & Felmy, F. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.2320-22.2023 · Cited by 8 · see citing works
Martín, R., Suárez-Pinilla, A. S., García-Font, N., Laguna-Luque, M. L., López, J. C., Oset‐Gasque, M. J., Gruart, A., Delgado-Garcia, J. M., Torres, M., & Sánchez‐Prieto, J. (2023) · Molecular Autism · doi:10.1186/s13229-023-00547-4 · Cited by 8 · see citing works
Lin, K., Taschenberger, H., & Neher, E. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4075232 · Cited by 8 · see citing works
Self-citationThe intracellular Ca 2+ sensitivity of transmitter release in glutamatergic neocortical boutons
Bornschein, G., Brachtendorf, S., Reinert, A., Eshra, A., Kraft, R., Hirrlinger, J., Eilers, J., Hallermann, S., & Schmidt, H. (2025) · Science · doi:10.1126/science.adp0870 · Cited by 6 · see citing works
Meijer, M., Öttl, M., Yang, J., Subkhangulova, A., Kumar, A., Feng, Z., van Voorst, T. W., Groffen, A., van Weering, J. V., Zhang, Y., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-46828-1 · Cited by 5 · see citing works
Tuning auditory synapses for resilience, reliability and precision
Lujan, B., & von Gersdorff, H. (2017) · The Journal of Physiology · doi:10.1113/jp273496 · Cited by 4 · see citing works
Ultrafast glutamate sensors resolve high-frequency release at Schaffer collateral synapsesPreprint
Helassa, N., Dürst, C. D., Coates, C., Kerruth, S., Arif, U., Schulze, C., Wiegert, J. S., Geeves, M., Oertner, T. G., & Török, K. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/233494 · Cited by 4 · see citing works
Ranjan, M., Lin, K., Mueller, B. D., Wojcik, S. M., Lohse, M., Südhof, T. C., Jørgensen, E. M., Neher, E., Lipstein, N., Brose, N., et al. (2026) · Science Advances · doi:10.1126/sciadv.aea0449 · Cited by 3 · see citing works
Self-citationSilva, M., Tran, V., & Marty, A. (2024) · eLife · doi:10.7554/elife.91087.3 · Cited by 1 · see citing works
Xue, R., Zhang, E., & Wang, Y. (2024) · Acta Physiologica · doi:10.1111/apha.14115 · Cited by 1 · see citing works
Eichler, A., Kruse, P., Schob, C., & Lenz, M. (2025) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2025.1724377 · Cited by 1 · see citing works
Synaptic vesicle undocking induces low-frequency depression
Silva, M., Trigo, F. F., Llano, I., & Marty, A. (2026) · eLife · doi:10.64898/2026.01.15.699619 · Cited by 1 · see citing works
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2026) · eLife · doi:10.7554/elife.102923.6 · Cited by 1 · see citing works
Synaptic Facilitation Enhances the Reliability and Precision of High-Frequency Neurotransmission
Bernal-Correa, A. M., Dagostin, A., von Gersdorff, H., & Kushmerick, C. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0570-25.2026 · Cited by 1 · see citing works
Functioning of Synaptic Vesicle Pools: Diversity and Organizational Principles
Gafurova, C. R., & Petrov, A. M. (2026) · Biochemistry (Moscow) · doi:10.1134/s0006297926600535 · Cited by 1 · see citing works
Undoing of firing rate adaptation enables invariant population codes
Brandão, S. C., Ramirez, L., Züfle, P., Walter, A. M., Silies, M., & Martelli, C. (2026) · Science Advances · doi:10.1126/sciadv.aeg3535 · Cited by 1 · see citing works
Electrophysiological Analysis of the Synaptic Vesicle Priming Process
Nestvogel, D. (2017) · doi:10.53846/goediss-6444 · Cited by 1 · see citing works
Correlating Synaptic Ultrastructure and Function at the NanoscalePreprint
Maus, L., Altas, B., Rhee, J., Brose, N., Imig, C., & Cooper, B. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/588848 · Cited by 1 · see citing works
- Authors
- Taschenberger, H., Woehler, A., & Neher, E.
- Affiliations
- Nanoscale Microscopy and Molecular Physiology of the Brain Cluster of Excellence 171 — DFG Research Center 103 (DE)
- Corresponding author
- Neher, Erwin
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2016-07-18
- Volume
- 113
- Issue
- 31
- Pages
- E4548-57
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4978258
- OpenAlex
- W2477973977
- Cited by
- 128
- References
- 67
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 13 · 2023: 18 · 2022: 10 · 2021: 12 · 2020: 8 · 2019: 15 · 2018: 13 · 2017: 16 · 2016: 1
- FWCI
- 8.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft (CNMPB)
- European Commission Directorate-General for Research and Innovation (FP7-HEALTH-F2-2009-241498)
- 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 › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- synaptic vesicles, short-term plasticity, post-tetanic potentiation, short-term depression, synaptic facilitation, phospholipase C, diacylglycerol, phorbol ester, glutamatergic synapses
- MeSH terms
- Algorithms, Animals, Animals, Newborn, Cells, Cultured, Electric Stimulation, Female, Male, Models, Neurological, Synaptic Transmission, Neuronal Plasticity, Synapses, Synaptic Vesicles, Signal Transduction, Rats, Wistar, Glutamic Acid, Excitatory Postsynaptic Potentials
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review