Different priming states of synaptic vesicles underlie distinct release probabilities at hippocampal excitatory synapses
Open accessAbstract
A stunning example of synaptic diversity is the postsynaptic target cell-type-dependent difference in synaptic efficacy in cortical networks. Here, we show that CA1 pyramidal cell (PC) to fast spiking interneuron (FSIN) connections have 10-fold larger release probability (P v ) than those on oriens lacunosum-moleculare (O-LM) interneurons. Freeze-fracture immunolabeling revealed that different nano-topologies and coupling distances between Ca 2+ channels and release sites (RSs) are not responsible for the distinct P v . Although [Ca 2+ ] transients are 40% larger in FSINs innervating boutons, when [Ca 2+ ] entry is matched in the two bouton populations, EPSCs in O-LM cells are still 7-fold smaller. However, application of a phorbol ester analog resulted in a ∼2.5-fold larger augmentation at PC – O-LM compared to PC – FSIN synapses, suggesting incomplete docking or priming of vesicles. Similar densities of docked vesicles rule out distinct RS occupancies and demonstrate that incompletely primed, but docked, vesicles limit the output of PC – O-LM synapses.
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?
The corresponding active zone membrane association can be detected by freeze-fracture replica labeling.
“The corresponding AZ membrane association can be detected by FRL [23,61,66,67].”
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 [23]
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
(1996) · Cited by 20,179 · see citing works
Computer visualization of three-dimensional image data using IMOD.
Kremer, J. R., Mastronarde, D., & Mcintosh, J. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0013 · Cited by 5,770 · see citing works
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
Intracellular 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 · cited 1× · see citing works
“…somatostatin(Som)/mGluR1 a -expressing IN(e.g. oriensla-cunosum-moleculare [O-LM] cells in the hippocampus), the P v is low and the postsynaptic response displays robust short-term facilitation (Ali et al., 1998; Ali and Thomson, 1998; Reyes et al., 1998; Scanziani et al., 1998; Sun et al., 2005).”
Rhee, J.-S., Betz, A., Pyott, S., Reim, K., Varoqueaux, F., Augustin, I., Hesse, D., Südhof, T. C., Takahashi, M., Rosenmund, C., et al. (2002) · Cell · doi:10.1016/s0092-8674(01)00635-3 · Cited by 500 · see citing works
Tests of 'Randomness' for Spatial Point Patterns
Ripley, B. D. (1979) · Journal of the Royal Statistical Society Series B (Statistical Methodology) · doi:10.1111/j.2517-6161.1979.tb01091.x · Cited by 484 · see citing works
Gulyás, A. I., Megı́as, M., Emri, Z., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-22-10082.1999 · Cited by 476 · see citing works
Routing of spike series by dynamic circuits in the hippocampus
Pouille, F., & Scanziani, M. (2004) · Nature · doi:10.1038/nature02615 · Cited by 434 · see citing works
Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release
Betz, A., Ashery, U., Rickmann, M., Augustin, I., Neher, E., Südhof, T. C., Rettig, J., & Brose, N. (1998) · Neuron · doi:10.1016/s0896-6273(00)80520-6 · Cited by 425 · see citing works
Mammalian Homologues of Caenorhabditis elegans unc-13 Gene Define Novel Family of C2-domain Proteins
Brose, N., Hofmann, K., Hata, Y., & Südhof, T. C. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.42.25273 · Cited by 412 · see citing works
Release probability of hippocampal glutamatergic terminals scales with the size of the active zone
Holderith, N., Lorincz, A., Katona, G., Rózsa, B., Kulik, A., Watanabe, M., & Nusser, Z. (2012) · Nature Neuroscience · doi:10.1038/nn.3137 · Cited by 405 · see citing works
Self-citationShigemoto, R., Kulik, A., Roberts, J. D. B., Ohishi, H., Nusser, Z., Kaneko, T., & Somogyi, P. (1996) · Nature · doi:10.1038/381523a0 · Cited by 400 · see citing works
Self-citationRozov, 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
The Morphological and Molecular Nature of Synaptic Vesicle Priming at Presynaptic Active Zones
Imig, C., Min, S.-W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T. C., Rhee, J., Brose, N., & Cooper, B. H. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.009 · Cited by 389 · see citing works
Munc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex
Ma, C., Li, W., Xu, Y., & Rizo, J. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2047 · Cited by 363 · see citing works
OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons
Leão, R. N., Mikulovic, S., Leão, K. E., Munguba, H., Gezelius, H., Enjin, A., Patra, K., Eriksson, A., Loew, L. M., Tort, A. B. L., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3235 · Cited by 359 · see citing works
Differential Control of Vesicle Priming and Short-Term Plasticity by Munc13 Isoforms
Rosenmund, C., Sigler, A., Augustin, I., Reim, K., Brose, N., & Rhee, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00568-8 · Cited by 346 · see citing works
Three-Dimensional Architecture of Presynaptic Terminal Cytomatrix
Siksou, L., Rostaing, P., Lechaire, J., Boudier, T., Ohtsuka, T., Fejtová, A., Kao, H., Greengard, P., Gundelfinger, E. D., Triller, A., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1773-07.2007 · Cited by 329 · 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-citationAllosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion
Lou, X., Scheuß, V., & Schneggenburger, R. (2005) · Nature · doi:10.1038/nature03568 · Cited by 289 · see citing works
RIM Proteins Activate Vesicle Priming by Reversing Autoinhibitory Homodimerization of Munc13
Deng, L., Kaeser, P. S., Xu, W., & Südhof, T. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.005 · Cited by 287 · see citing works
Modulation of transmitter release by presynaptic resting potential and background calcium levels.
Awatramani, G., Price, G., & Trussell, L. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.038 · Cited by 285 · 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
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
Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis
Shin, O.-H., Lu, J., Rhee, J.-S., Tomchick, D. R., Pang, Z. P., Wojcik, S. M., Camacho-Perez, M., Brose, N., Machius, M., Rizo, J., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1758 · Cited by 243 · see citing works
Synaptic weight set by Munc13-1 supramolecular assemblies
Sakamoto, H., Ariyoshi, T., Kimpara, N., Sugao, K., Taiko, I., Takikawa, K., Asanuma, D., Namiki, S., & Hirose, K. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0041-9 · Cited by 235 · see citing works
Munc13-1 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
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
Mechanism of neurotransmitter release coming into focus
Rizo, J. (2018) · Protein Science · doi:10.1002/pro.3445 · Cited by 210 · cited 1× · see citing works
“It is now generally accepted that Munc13 molecules are the master regulators of SV priming at central synapses (reviewed by Rizo, 2018).”
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
Ali, A. B., & Thomson, A. M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.185bu.x · Cited by 202 · see citing works
Ali, A. B., Deuchars, J., Pawelzik, H., & Thomson, A. M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.201bu.x · Cited by 180 · see citing works
Target cell-specific modulation of transmitter release at terminals from a single axon
Scanziani, M., Gähwiler, B. H., & Charpak, S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.12004 · Cited by 167 · see citing works
Actin- and Myosin-Dependent Vesicle Loading of Presynaptic Docking Sites Prior to Exocytosis
Miki, T., Malagón, G., Pulido, C., Llano, I., Neher, E., & Marty, A. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.033 · Cited by 160 · see citing works
Elfn1 Regulates Target-Specific Release Probability at CA1-Interneuron Synapses
Sylwestrak, E. L., & Ghosh, A. (2012) · Science · doi:10.1126/science.1222482 · Cited by 151 · 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
Rebola, 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-citationTaschenberger, H., Woehler, A., & Neher, E. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606383113 · Cited by 128 · 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
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
Elfn1 recruits presynaptic mGluR7 in trans and its loss results in seizures
Tomioka, N. H., Yasuda, H., Miyamoto, H., Hatayama, M., Morimura, N., Matsumoto, Y., Suzuki, T., Odagawa, M., Odaka, Y. S., Iwayama, Y., et al. (2014) · Nature Communications · doi:10.1038/ncomms5501 · Cited by 113 · 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
Membrane bridging by Munc13-1 is crucial for neurotransmitter release
Quade, B., Camacho, M., Zhao, X., Orlando, M., Trimbuch, T., Xu, J., Li, W., Nicastro, D., Rosenmund, C., & Rizo, J. (2019) · eLife · doi:10.7554/elife.42806 · Cited by 108 · 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
Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses
Biró, Á. A., Holderith, N. B., & Nusser, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3688-04.2005 · Cited by 96 · see citing works
Self-citationHeterodimerization of Munc13 C2A domain with RIM regulates synaptic vesicle docking and priming
Camacho, M., Basu, J., Trimbuch, T., Chang, S., Pulido-Lozano, C., Chang, S.-S., Duluvova, I., Abo-Rady, M., Rizo, J., & Rosenmund, C. (2017) · Nature Communications · doi:10.1038/ncomms15293 · Cited by 95 · 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
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
Calcium Sensitivity of Neurotransmitter Release Differs at Phasic and Tonic Synapses
Millar, A. G., Zucker, R. S., Ellis‐Davies, G. C. R., Charlton, M. P., & Atwood, H. L. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4717-04.2005 · Cited by 82 · see citing works
The Binomial Model in Fluctuation Analysis of Quantal Neurotransmitter Release
Quastel, D. M. J. (1997) · Biophysical Journal · doi:10.1016/s0006-3495(97)78709-5 · Cited by 81 · see citing works
Millar, A. G., Bradacs, H., Charlton, M. P., & Atwood, H. L. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09661.2002 · Cited by 73 · see citing works
Losonczy, A., Somogyi, P., & Nusser, Z. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00842.2002 · Cited by 72 · see citing works
Self-citationA 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
Stachniak, T. J., Sylwestrak, E., Scheiffele, P., Hall, B. J., & Ghosh, A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2276-18.2019 · Cited by 72 · 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
Ultrastructural 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
Imig, C., López-Murcia, F. J., Maus, L., García-Plaza, I. H., Mortensen, L. S., Schwark, M., Schwarze, V., Angibaud, J., Nägerl, U. V., Taschenberger, H., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.004 · Cited by 66 · see citing works
Sun, H. Y., Lyons, S. A., & Dobrunz, L. E. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.093948 · Cited by 64 · see citing works
Munc13-Independent Vesicle Priming at Mouse Photoreceptor Ribbon Synapses
Cooper, B. H., Hemmerlein, M., Ammermüller, J., Imig, C., Reim, K., Lipstein, N., Kalla, S., Kawabe, H., Brose, N., Brandstätter, J. H., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4240-11.2012 · Cited by 63 · see citing works
Identification of a Munc13-sensitive step in chromaffin cell large dense-core vesicle exocytosis
Man, K. N. M., Imig, C., Walter, A. M., Pinheiro, P. S., Stevens, D. R., Rettig, J., Sørensen, J. B., Cooper, B. H., Brose, N., & Wojcik, S. M. (2015) · eLife · doi:10.7554/elife.10635 · Cited by 63 · see citing works
Lübbert, M., Goral, R. O., Keine, C., Thomas, C. I., Guerrero‐Given, D., Putzke, T., Satterfield, R., Kamasawa, N., & Young, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.028 · Cited by 58 · see citing works
Keller, D. X., Babai, N. Z., Kochubey, O., Han, Y., Markram, H., Schürmann, F., & Schneggenburger, R. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004253 · Cited by 57 · see citing works
Lin, K., Taschenberger, H., & Neher, E. (2022) · bioRxiv · doi:10.1073/pnas.2207987119 · Cited by 57 · see citing works
An Excess-Calcium-Binding-Site Model Predicts Neurotransmitter Release at the Neuromuscular Junction
Dittrich, M., Pattillo, J. M., King, J. D., Cho, S., Stiles, J. R., & Meriney, S. D. (2013) · Biophysical Journal · doi:10.1016/j.bpj.2013.05.023 · Cited by 54 · see citing works
Éltes, T., Kirizs, T., Nusser, Z., & Holderith, N. B. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2024-16.2017 · Cited by 52 · see citing works
Self-citationLuo, F., Dittrich, M., Stiles, J. R., & Meriney, S. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1394-11.2011 · Cited by 50 · 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
Lenkey, N., Kirizs, T., Holderith, N., Máté, Z., Szabó, G., Vizi, E. S., Hájos, N., & Nusser, Z. (2015) · Nature Communications · doi:10.1038/ncomms7557 · Cited by 45 · see citing works
Self-citationIncomplete vesicular docking limits synaptic strength under high release probability conditions
Malagón, G., Miki, T., Tran, V., Gomez, L. C., & Marty, A. (2020) · eLife · doi:10.7554/elife.52137 · Cited by 44 · 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
Self-citationCalcium 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
Tran, V., Miki, T., & Marty, A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2114469119 · Cited by 27 · see citing works
Li, L., Liu, H., Hall, Q., Wang, W., Yu, Y., Kaplan, J. M., & Hu, Z. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.018 · Cited by 23 · see citing works
Objective quantification of nanoscale protein distributions
Szoboszlay, M., Kirizs, T., & Nusser, Z. (2017) · Scientific Reports · doi:10.1038/s41598-017-15695-w · Cited by 17 · see citing works
Self-citationHolderith, N. B., Aldahabi, M., & Nusser, Z. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.773209 · Cited by 9 · see citing works
Self-citationLin, K., Taschenberger, H., & Neher, E. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4075232 · Cited by 8 · see citing works
Flagged first, then by citations
2 of the 81 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Neher, E. (2023) · The Journal of General Physiology · doi:10.1085/jgp.202313454 · Cited by 34 · see citing works
Jusyte, 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
Differential nanoscale organization of excitatory synapses onto excitatory vs. inhibitory neurons
Dharmasri, P. A., Levy, A. D., & Blanpied, T. A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2315379121 · Cited by 23 · see citing works
Fully-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
Koppensteiner, P., Bhandari, P., Önal, C., Borges-Merjane, C., Monnier, E. L., Roy, U., Nakamura, Y., Sadakata, T., Sanbo, M., Hirabayashi, M., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301449121 · Cited by 24 · see citing works
Synaptic and dendritic architecture of different types of hippocampal somatostatin interneurons
Takács, V. T., Bardóczi, Z., Orosz, Á., Major, Á., Tar, L., Berki, P., Papp, P., Mayer, M. I., Sebők, H., Zsolt, L., et al. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002539 · 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-citationTrans-synaptic molecular context of NMDA receptor nanodomains
Anderson, M. C., Dharmasri, P. A., Damenti, M., Metzbower, S. R., Laghaei, R., Blanpied, T. A., & Levy, A. D. (2025) · Nature Communications · doi:10.1038/s41467-025-62766-y · 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
“Although recent work demonstrated the feasibility of such a technically demanding approach [23], rigorous correlated biophysical and morphological analysis of defined glutamatergic synapses at the single-synapse level to resolve the nanoscale changes during presynaptic plasticity induction is…”
Distinct dendritic integration strategies control dynamics of inhibition in the neocortex
Morabito, A., Zerlaut, Y., Dhanasobhon, D., Berthaux, E., Pinho, C. M., Tzilivaki, A., Moneron, G., Cathala, L., Poirazi, P., Bacci, A., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.05.029 · Cited by 19 · see citing works
Medeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2024) · eLife · doi:10.7554/elife.88412.3 · 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
Martín‐Belmonte, A., Aguado, C., Alfaro‐Ruiz, R., Kulik, Á., de la Ossa, L., Moreno‐Martínez, A. E., Alberquilla, S., García‐Carracedo, L., Fernández, M., Fajardo‐Serrano, A., et al. (2024) · Brain Pathology · doi:10.1111/bpa.13279 · Cited by 10 · see citing works
Blaum, N., Ghelani, T., Götz, T., Chronister, K. S., Bengochea, M., Ceresnova, L., Christensen, C., Moulin, T. C., Kern, H. B., Thomas, U., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2514151122 · Cited by 9 · see citing works
Input/Output Relationships for the Primary Hippocampal Circuit
Gunn, B. G., Pruess, B. S., Gall, C. M., & LYNCH, G. S. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0130-24.2024 · Cited by 8 · see citing works
Rapid presynaptic maturation in naturally regenerating axons of the adult mouse olfactory nerve
Browne, L., Crespo, A., & Grubb, M. S. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111750 · Cited by 8 · see citing works
Loss of postsynaptic NMDARs drives nanoscale reorganization of Munc13-1 and PSD-95Preprint
Dharmasri, P. A., DeMarco, E. M., Anderson, M. C., Levy, A. D., & Blanpied, T. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.12.574705 · Cited by 8 · see citing works
Medeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2023) · eLife · doi:10.7554/elife.88412 · Cited by 23 · see citing works
Midorikawa, M., Sakamoto, H., Nakamura, Y., Hirose, K., & Miyata, M. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114770 · Cited by 7 · see citing works
A dendritic substrate for temporal diversity of cortical inhibitionPreprint
Morabito, A., Zerlaut, Y., Dhanasobhon, D., Berthaux, E., Tzilivaki, A., Moneron, G., Cathala, L., Poirazi, P., Bacci, A., DiGregorio, D. A., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.09.602783 · Cited by 7 · see citing works
Pre- versus Post-synaptic Forms of LTP in Two Branches of the Same Hippocampal Afferent
Quintanilla, J., Jia, Y., Pruess, B. S., Chavez, J., Gall, C. M., LYNCH, G. S., & Gunn, B. G. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1449-23.2024 · Cited by 7 · see citing works
Dynamic nanoscale architecture of synaptic vesicle fusion in mouse hippocampal neurons
Kroll, J., Kravčenko, U., Sadeghi, M., Diebolder, C. A., Ivanov, L., Lubas, M., Sprink, T., Schacherl, M., Kudryashev, M., & Rosenmund, C. (2025) · Nature Communications · doi:10.1038/s41467-025-67291-6 · Cited by 5 · see citing works
An Exact Transient Solution Characterizing Stochastic Dynamics of Neuronal Synaptic TransmissionPreprint
Singh, A. (2023) · doi:10.31219/osf.io/fdq3c · Cited by 5 · see citing works
Medeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2023) · eLife · doi:10.7554/elife.88412.1 · Cited by 5 · see citing works
Lőrincz, A., Ashaber, M., & Nusser, Z. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0645-25.2025 · Cited by 4 · see citing works
Self-citationMedeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.02.535290 · Cited by 4 · see citing works
Luján, R., Turégano-López, M., Aguado, C., & Merchán-Pérez, Á. (2024) · Advanced technology in neuroscience . · doi:10.4103/atn.atn-d-24-00009 · Cited by 3 · see citing works
Koppensteiner, P., Bhandari, P., Önal, C., Borges-Merjane, C., Monnier, E. L., Nakamura, Y., Sadakata, T., Sanbo, M., Hirabayashi, M., Brose, N., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.28.514202 · Cited by 3 · see citing works
Chanaday, N. L. (2026) · Advances in neurobiology · doi:10.1007/978-3-032-12594-1_3 · Cited by 2 · see citing works
Fekete, Z., Weisz, F., Karlócai, M. R., Veres, J. M., Andrási, T., & Hájos, N. (2024) · The Journal of Physiology · doi:10.1113/jp286284 · Cited by 2 · see citing works
Kim, H. S., Santana, G. M. T., Sancer, G., Emonet, T., & Jeanne, J. M. (2024) · Current Biology · doi:10.1016/j.cub.2025.05.051 · Cited by 3 · see citing works
Kim, O., Okamoto, Y., Brose, N., Shigemoto, R., & Jónás, P. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.04.569907 · Cited by 2 · see citing works
Medeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2024) · eLife · doi:10.7554/elife.88412.2 · Cited by 2 · 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
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2025) · eLife · doi:10.7554/elife.102923.1 · Cited by 1 · see citing works
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2025) · eLife · doi:10.7554/elife.102923 · Cited by 1 · see citing works
Synaptic and dendritic architecture of different types of hippocampal somatostatin interneuronsPreprint
Takács, V. T., Bardóczi, Z., Orosz, Á., Major, Á., Tar, L., Berki, P., Papp, P., Mayer, M. I., Sebők, H., Zsolt, L., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.14.540675
Medeiros, A. T., Gratz, S. J., Delgado, A., Ritt, J. T., & O’Connor-Giles, K. M. (2024) · eLife · doi:10.7554/elife.88412.2.sa0
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2025) · eLife · doi:10.7554/elife.102923.2
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2025) · eLife · doi:10.7554/elife.102923.3
Polyadic synapses introduce unique wiring architectures in T5 cells of DrosophilaPreprint
Samara, E., & Borst, A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.04.668437
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2025) · eLife · doi:10.7554/elife.102923.4
Polyadic synapses introduce unique wiring architectures in T5 cells of Drosophila
Samara, E., & Borst, A. (2025) · PLoS ONE · doi:10.1371/journal.pone.0334925
Shin, J., Lee, S. Y., Kim, Y., & Lee, S. (2026) · eLife · doi:10.7554/elife.102923.5
Selective, genetically induced increase in synaptic vesicle priming
Aldahabi, M., Bálint, F., Lőrincz, A., Lipstein, N., Brose, N., & Nusser, Z. (2026) · Science Advances · doi:10.1126/sciadv.aee6848
Self-citationUltrastructural and molecular analysis of cortico-striatal dopamine hub synapses
Lapios, P. (2024) · theses.fr (ABES) · doi:10.70675/527646a6zd9b5z4935z80ebz0950bba9d08e
The Primary Hippocampal Circuit: New Lessons about an Old Network
Gunn, B. G., & LYNCH, G. S. (2026) · The Neuroscientist · doi:10.1177/10738584261476032
- Authors
- Aldahabi, M., Balint, F., Holderith, N., Lorincz, A., Reva, M., & Nusser, Z.
- Affiliations
- Semmelweis University (HU)
- Centre National de la Recherche Scientifique (FR)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2022-12
- Volume
- 110
- Issue
- 24
- Pages
- 4144-4161.e7
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC9796815
- OpenAlex
- W4306748254
- Cited by
- 50
- References
- 81
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 20 · 2023: 9 · 2022: 2
- FWCI
- 4.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- H2020 European Research Council (787157)
- 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 › Memory and Neural Mechanisms
- Keywords
- synaptic vesicle priming, release probability, hippocampal CA1, pyramidal neurons, fast-spiking interneurons, oriens-lacunosum moleculare interneurons, synaptic diversity, calcium transients, vesicle docking, phorbol ester, synaptic transmission
- MeSH terms
- Hippocampus, Interneurons, Probability, Synapses, Synaptic Vesicles
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