Structural determinants of transmission at large hippocampal mossy fiber synapses
Open accessAbstract
Synapses are the key elements for signal processing and plasticity in the brain. To determine the structural factors underlying the unique functional properties of the hippocampal mossy fiber synapse, the complete quantitative geometry was investigated, using electron microscopy of serial ultrathin sections followed by computer-assisted three-dimensional reconstruction. In particular, parameters relevant for transmitter release and synaptic plasticity were examined. Two membrane specializations were found: active zones (AZs), transmitter release sites, and puncta adherentia, putative adhesion complexes. Individual boutons had, on average, 25 AZs (range, 7–45) that varied in shape and size (mean, 0.1 μm 2 ; range, 0.07–0.17 μm 2 ). The mean distance between individual AZs was 0.45 μm. Mossy fiber boutons and their target structures were mostly ensheathed by astrocytes, but fine glial processes never reached the active zones. Two structural factors are likely to promote synaptic cross talk: the short distance between AZs and the absence of fine glial processes at AZs. Thus, synaptic cross talk may contribute to the efficacy of hippocampal mossy fiber synapses. On average, a bouton contained 20,400 synaptic vesicles; ∼900 vesicles were located within 60 nm from the active zone, ∼4400 between 60 and 200 nm, and the remaining beyond 200 nm, suggesting large readily releasable, recycling, and reserve pools. The organization of the different pools may be a key structural correlate of presynaptic plasticity at this synapse. Thus, the mossy fiber bouton differs fundamentally in structure and function from the calyx of Held and other central 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?
Proper synapse formation during childhood provides a substrate for cognition, whereas improper formation or functionality leads to neuro-developmental disorders including mental retardation and autism.
“Proper synapse formation during childhood provides a substrate for cognition, whereas improper formation or functionality leads to neuro-developmental disorders including mental retardation and autism”
From Human Brain/Cloud Interface (2019) · cites this paper as Rollenhagen et al., 2007
The Introduction (pp. 10434–10444) links hippocampal mossy fiber synapses to processing, storage, and recall of spatial information, supporting a general connection between synapses and cognition. It does not establish that synapse formation during childhood provides that substrate or that improper formation or function leads to mental retardation or autism; searches for those developmental and disorder terms found no supporting passage. (LLM, conf=0.79)
Experimental — accuracy not yet measuredThe mossy fiber-CA3 PN synapse is accessible to quantitative structural analysis by electron microscopy, high-pressure freezing, and freeze-fracture replica labeling.
“Finally, it is accessible to quantitative structural analysis by EM [34,35], high-pressure freezing (HPF) [36–38], and freeze-fracture replica labeling (FRL) [39].”
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 [34]
Under control conditions, the estimated RRP size is 1.6 vesicles per AZ.
“Under control conditions, we estimate an RRP size of 1.6 vesicles per AZ (S4 Table; assuming that a typically sized MFB contains 29 AZs) [34].”
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 [34]
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
Estimation of nuclear population from microtome sections
Abercrombie, M. (1946) · The Anatomical Record · doi:10.1002/ar.1090940210 · Cited by 4,363 · see citing works
Danbolt, N. C. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00067-8 · Cited by 4,068 · see citing works
Definition of the readily releasable pool of vesicles at hippocampal synapses.
Rosenmund, C., & Stevens, C. (1996) · Neuron · doi:10.1016/s0896-6273(00)80146-4 · Cited by 1,084 · 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
Rizzoli, S. O., & Betz, W. J. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1583 · Cited by 975 · see citing works
Verstreken, P., Ly, C. V., Venken, K. J. T., Koh, T.-W., Zhou, Y., & Bellen, H. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.018 · Cited by 841 · see citing works
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
Acsády, L., Kamondi, A., Sı́k, A., Freund, T., & Buzsáki, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03386.1998 · Cited by 741 · see citing works
Synaptic plasticity at hippocampal mossy fibre synapses
Nicoll, R. A., & Schmitz, D. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1786 · Cited by 653 · 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
Relating Hippocampal Circuitry to Function
Lisman, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)81085-5 · Cited by 607 · see citing works
Amaral, D. G., & Dent, J. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950106 · Cited by 606 · see citing works
Geiger, J. R. P., & Jónás, P. (2000) · Neuron · doi:10.1016/s0896-6273(00)00164-1 · Cited by 605 · see citing works
Mitochondria as all‐round players of the calcium game
Rizzuto, R., Bernardi, P., & Pozzan, T. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00037.x · Cited by 562 · see citing works
Chapter 1 Chapter Neurons, numbers and the hippocampal network
Amaral, D. G., Ishizuka, N., & Claiborne, B. J. (1990) · Progress in brain research · doi:10.1016/s0079-6123(08)61237-6 · Cited by 523 · see citing works
Morphological correlates of functionally defined synaptic vesicle populations
Schikorski, T., & Stevens, C. F. (2001) · Nature Neuroscience · doi:10.1038/86042 · Cited by 516 · see citing works
Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo
Henze, D. A., Wittner, L., & Buzsáki, G. (2002) · Nature Neuroscience · doi:10.1038/nn887 · Cited by 480 · see citing works
Distinct short-term plasticity at two excitatory synapses in the hippocampus
Salin, P. A., Scanziani, M., Malenka, R. C., & Nicoll, R. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.23.13304 · Cited by 438 · see citing works
Chicurel, M. E., & Harris, K. M. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903250204 · Cited by 417 · see citing works
Blackstad, T. W., & Kjærheim, Å. (1961) · The Journal of Comparative Neurology · doi:10.1002/cne.901170202 · Cited by 386 · see citing works
Sätzler, K., Söhl, L. F., Bollmann, J. H., Borst, J. G. G., Frotscher, M., Sakmann, B. J., & Lübke, J. H. R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10567.2002 · Cited by 364 · see citing works
Self-citationVesicle pools and short-term synaptic depression: lessons from a large synapse
Schneggenburger, R., Sakaba, T., & Neher, E. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02139-2 · Cited by 361 · see citing works
Combined Analog and Action Potential Coding in Hippocampal Mossy Fibers
Alle, H., & Geiger, J. R. P. (2006) · Science · doi:10.1126/science.1119055 · Cited by 348 · see citing works
The Structural Organization of the Readily Releasable Pool of Synaptic Vesicles
Rizzoli, S. O., & Betz, W. J. (2004) · Science · doi:10.1126/science.1094682 · Cited by 340 · 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
Barbour, B., & Häusser, M. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)20050-5 · Cited by 307 · see citing works
Differential Mechanisms of Transmission at Three Types of Mossy Fiber Synapse
Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E., & McBain, C. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08279.2000 · Cited by 262 · see citing works
The fine structure of the mossy fibre endings in the hippocampus of the rabbit.
Hamlyn, L. H. (1962) · PubMed · Cited by 243 · see citing works
Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse
Saviane, C., & Silver, R. A. (2006) · Nature · doi:10.1038/nature04509 · Cited by 240 · see citing works
Sun, J., & Wu, L. (2001) · Neuron · doi:10.1016/s0896-6273(01)00271-9 · Cited by 231 · see citing works
DiGregorio, D. A., Nusser, Z., & Silver, R. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00787-0 · Cited by 231 · see citing works
Engel, D., & Jónás, P. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.048 · Cited by 190 · see citing works
Specialized Synapse-Associated Structures within the Calyx of Held
Rowland, K. C., Irby, N. K., & Spirou, G. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09135.2000 · Cited by 187 · see citing works
A large pool of releasable vesicles in a cortical glutamatergic synapse
Hallermann, S., Pawlu, C., Jonas, P., & Heckmann, M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1432836100 · Cited by 181 · see citing works
Derouiche, A., & Frotscher, M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90103-3 · Cited by 164 · see citing works
Self-citationGalimberti, I., Gogolla, N., Alberi, S., Santos, A. F., Müller, D., & Caroni, P. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.026 · Cited by 163 · see citing works
Timing and Efficacy of Ca2+Channel Activation in Hippocampal Mossy Fiber Boutons
Bischofberger, J., Geiger, J. R. P., & Jónás, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10593.2002 · Cited by 158 · see citing works
Analysis of synaptic ultrastructure without fixative using high‐pressure freezing and tomography
Rostaing, P., Réal, É., Siksou, L., Lechaire, J. P., Boudier, T., Boeckers, T. M., Gertler, F. B., Gundelfinger, E. D., Triller, A., & Marty, S. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05234.x · Cited by 152 · see citing works
Ultrastructural Contributions to Desensitization at Cerebellar Mossy Fiber to Granule Cell Synapses
Xu‐Friedman, M. A., & Regehr, W. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02182.2003 · Cited by 142 · see citing works
Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus
Lawrence, J. J., Grinspan, Z. M., & McBain, C. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049551 · Cited by 125 · see citing works
Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network
Bischofberger, J., Engel, D., Frotscher, M., & Jónás, P. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0093-2 · Cited by 117 · see citing works
Self-citationKobayashi, K., & Poo, M. (2004) · Neuron · doi:10.1016/s0896-6273(03)00873-0 · Cited by 109 · see citing works
Honda, T., Sakisaka, T., Yamada, T., Kumazawa-Manita, N., Hoshino, T., Kajita, M., Kayahara, T., Ishizaki, H., Tanaka, M., Mizoguchi, A., et al. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.10.002 · Cited by 105 · see citing works
Nicol, M. J., & Walmsley, B. D. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012972 · Cited by 105 · see citing works
Giant miniature EPSCs at the hippocampal mossy fiber to CA3 pyramidal cell synapse are monoquantal.
Henze, D., Mcmahon, D., Harris, K., & Barrionuevo, G. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00394.2001 · Cited by 105 · see citing works
The morphology of excitatory central synapses: from structure to function.
Rollenhagen, A., & Lübke, J. H. R. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0288-z · Cited by 99 · see citing works
Self-citationGlial modulation of synaptic transmission: Insights from the supraoptic nucleus of the hypothalamus
Oliet, S. H. R., Piet, R., Poulain, D. A., & Theodosis, D. T. (2004) · Glia · doi:10.1002/glia.20032 · Cited by 98 · see citing works
Wimmer, V. C., Horstmann, H., Groh, A., & Kuner, T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3268-05.2006 · Cited by 93 · see citing works
Davis, N. T., Veenstra, J. A., Feyereisen, R., & Hildebrand, J. G. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970825)385:2 · Cited by 82 · see citing works
Divergence of hippocampal mossy fibers
Frotscher, M., Soriano, E., & Misgeld, U. (1994) · Synapse · doi:10.1002/syn.890160208 · Cited by 77 · see citing works
Self-citationQuantal components of the excitatory postsynaptic currents at a rat central auditory synapse
Sahara, Y., & Takahashi, T. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00189.x · Cited by 72 · see citing works
Synapses formed by normal and abnormal hippocampal mossy fibers
Frotscher, M., Jónás, P., & Sloviter, R. S. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0269-2 · Cited by 71 · see citing works
Self-citationUltrastructural correlates of vesicular docking in the rat dentate gyrus
Marrone, D. F., LeBoutillier, J. C., & Petit, T. L. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2004.12.019 · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Astrocyte morphology: Diversity, plasticity, and role in neurological diseases
Zhou, B., Zuo, Y., & Jiang, R. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13123 · Cited by 417 · see citing works
Functional Proteomics Identify Cornichon Proteins as Auxiliary Subunits of AMPA Receptors
Schwenk, J., Harmel, N., Zolles, G., Bildl, W., Kulik, Á., Heimrich, B., Chisaka, O., Jónás, P., Schulte, U., Fakler, B., et al. (2009) · Science · doi:10.1126/science.1167852 · Cited by 388 · see citing works
What is the mammalian dentate gyrus good for?
Treves, A., Tashiro, A., Witter, M. P., & Moser, E. I. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.073 · Cited by 282 · see citing works
Conditions and Constraints for Astrocyte Calcium Signaling in the Hippocampal Mossy Fiber Pathway
Haustein, M. D., Kracun, S., Lu, X., Shih, T., Jackson‐Weaver, O., Tong, X., Xu, J. P., Yang, X. W., O’Dell, T. J., Marvin, J. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.041 · Cited by 249 · see citing works
Astrocyte-Synapse Structural Plasticity
Bernardinelli, Y., Müller, D., & Nikonenko, I. (2014) · Neural Plasticity · doi:10.1155/2014/232105 · Cited by 243 · see citing works
Kandalepas, P. C., Sadleir, K. R., Eimer, W. A., Zhao, J., Nicholson, D. A., & Vassar, R. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1152-3 · Cited by 240 · see citing works
Astrocytic control of synaptic function
Papouin, T., Dunphy, J. M., Tolman, M., Foley, J., & Haydon, P. G. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0154 · Cited by 229 · see citing works
Zinc Dynamics and Action at Excitatory Synapses
Vergnano, A. M., Rebola, N., Savtchenko, L. P., Pinheiro, P. S., Casado, M., Kieffer, B. L., Rusakov, D. A., Mulle, C., & Paoletti, P. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.034 · Cited by 213 · see citing works
Operation and plasticity of hippocampal CA3 circuits: implications for memory encoding
Rebola, N., Carta, M., & Mulle, C. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.10 · Cited by 211 · see citing works
Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain
Faulkner, R. L., Jang, M., Liu, X.-B., Duan, X., Sailor, K. A., Kim, J. Y., Ge, S., Jones, E. G., Ming, G., Song, H., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806658105 · Cited by 208 · see citing works
Li, L., Bischofberger, J., & Jonas, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1709-07.2007 · Cited by 206 · see citing works
Cadherin-9 Regulates Synapse-Specific Differentiation in the Developing Hippocampus
Williams, M. E., Wilke, S. A., Daggett, A., Davis, E. K., Otto, S. J., Ravi, D., Ripley, B. A., Bushong, E. A., Ellisman, M. H., Klein, G., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.019 · Cited by 202 · see citing works
Wnt Signaling in the Vertebrate Central Nervous System: From Axon Guidance to Synaptic FunctionPreprint
Salinas, P. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008003 · Cited by 189 · see citing works
Versatile control of synaptic circuits by astrocytes: where, when and how?
Dallérac, G. M., Zapata, J., & Rouach, N. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0080-6 · Cited by 187 · see citing works
Vyleta, N. P., & Jonas, P. (2014) · Science · doi:10.1126/science.1244811 · Cited by 189 · see citing works
Gogolla, N., Galimberti, I., Deguchi, Y., & Caroni, P. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.022 · Cited by 181 · see citing works
Wilke, S. A., Antonios, J. K., Bushong, E. A., Badkoobehi, A., Malek, E., Hwang, M., Terada, M., Ellisman, M. H., & Ghosh, A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1600-12.2013 · Cited by 179 · see citing works
Horstmann, H., Körber, C., Sätzler, K., Aydin, D., & Kuner, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035172 · Cited by 157 · see citing works
Self-citationMorphological plasticity of astroglia: Understanding synaptic microenvironment
Heller, J. P., & Rusakov, D. A. (2015) · Glia · doi:10.1002/glia.22821 · Cited by 150 · see citing works
Assessments of dentate gyrus function: discoveries and debates
Borzello, M., Ramirez, S., Treves, A., Lee, I., Scharfman, H. E., Stark, C. E. L., Knierim, J. J., & Rangel, L. M. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00710-z · Cited by 138 · see citing works
Wiera, G., & Mozrzymas, J. W. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00427 · Cited by 117 · see citing works
Brain metabolic sensing and metabolic signaling at the level of an astrocyte
Marina, N., Turovsky, E. A., Christie, I. N., Hosford, P. S., Hadjihambi, A., KORSAK, A. S., Ang, R., Mastitskaya, S., SheikhBahaei, S., Theparambil, S. M., et al. (2017) · Glia · doi:10.1002/glia.23283 · Cited by 118 · 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
Restivo, L., Niibori, Y., Mercaldo, V., Josselyn, S. A., & Frankland, P. W. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3238-14.2015 · Cited by 112 · see citing works
Super-resolving Microscopy in Neuroscience
Werner, C. D., Sauer, M., & Geis, C. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c01174 · Cited by 111 · see citing works
Hippocampal development – Old and new findings
Khalaf‐Nazzal, R., & Francis, F. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.061 · Cited by 103 · see citing works
Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus
Szabadics, J., & Soltész, I. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5390-08.2009 · Cited by 96 · see citing works
Diversity of astroglial functions alludes to subcellular specialisation
Rusakov, D. A., Bard, L., Stewart, M. G., & Henneberger, C. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.02.008 · Cited by 89 · see citing works
Martins, N. R. B., Angelica, A., Chakravarthy, K., Svidinenko, Y., Boehm, F. J., Opris, I., Lebedev, M. A., Swan, M., Garan, S. A., Rosenfeld, J. V., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00112 · Cited by 91 · see citing works
Plasticity-dependent, full detonation at hippocampal mossy fiber-CA3 pyramidal neuron synapses
Vyleta, N. P., Borges-Merjane, C., & Jonas, P. (2016) · eLife · doi:10.7554/elife.17977 · Cited by 91 · see citing works
Andres‐Alonso, M., Ammar, M. R., Butnaru, I., Gomes, G. M., Sanhueza, G. A., Raman, R., Yuanxiang, P., Borgmeyer, M., Lopez‐Rojas, J., Raza, S. A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13224-z · Cited by 82 · see citing works
Exercise Reverses Behavioral and Synaptic Abnormalities after Maternal Inflammation
Andoh, M., Shibata, K., Okamoto, K., Onodera, J., Morishita, K., Miura, Y., Ikegaya, Y., & Koyama, R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.015 · Cited by 85 · see citing works
Cole, J. D., Espinueva, D. F., Seib, D. R., Ash, A. M., Cooke, M. B., Cahill, S. P., O’Leary, T. P., Kwan, S. S., & Snyder, J. S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1665-19.2020 · Cited by 83 · see citing works
Zheng, K., Jensen, T. P., Savtchenko, L. P., Levitt, J. A., Suhling, K., & Rusakov, D. A. (2017) · Scientific Reports · doi:10.1038/srep42022 · 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
Scott, R. S., Lalic, T., Kullmann, D. M., Capogna, M., & Rusakov, D. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2932-08.2008 · Cited by 74 · see citing works
Sharma, G., Grybko, M. J., & Vijayaraghavan, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5407-07.2008 · Cited by 75 · see citing works
Midorikawa, M., & Sakaba, T. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.016 · Cited by 71 · see citing works
Condomitti, G., Wierda, K. D. B., Schroeder, A., Rubio, S. E., Vennekens, K. M., Orlandi, C., Martemyanov, K. A., Gounko, N. V., Savas, J. N., & de Wit, J. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.038 · Cited by 72 · see citing works
Information processing and synaptic plasticity at hippocampal mossy fiber terminals
Evstratova, A., & Tóth, K. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00028 · Cited by 67 · 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
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
Self-citationGating and permeation of kainate receptors: differences unveiled
Perrais, D., Veran, J., & Mulle, C. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.08.004 · Cited by 67 · 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
The mossy fiber bouton: the "common" or the "unique" synapse?
Rollenhagen, A. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00002 · Cited by 66 · see citing works
Self-citationControl of Long-Term Plasticity by Glutamate Transporters
Valtcheva, S., & Venance, L. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00010 · Cited by 62 · 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
Lanore, F., Labrousse, V. F., Szabó, Z. M., Normand, E., Blanchet, C., & Mulle, C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2049-12.2012 · Cited by 65 · see citing works
Structural plasticity of dentate granule cell mossy fibers during the development of limbic epilepsy
Danzer, S. C., He, X., Loepke, A. W., & McNamara, J. O. (2009) · Hippocampus · doi:10.1002/hipo.20589 · Cited by 61 · see citing works
Apóstolo, N., Smukowski, S. N., Vanderlinden, J., Condomitti, G., Rybakin, V., ten Bos, J., Trobiani, L., Portegies, S., Vennekens, K. M., Gounko, N. V., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18956-x · Cited by 61 · see citing works
Galimberti, I., Bednarek, E., Donato, F., & Caroni, P. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.016 · Cited by 60 · see citing works
Borges-Merjane, C., Kim, O., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.022 · Cited by 60 · see citing works
Krzisch, M., Temprana, S. G., Mongiat, L. A., Armida, J., Schmutz, V., Virtanen, M. A., Kocher-Braissant, J., Kraftsik, R., Vutskits, L., Conzelmann, K.-K., et al. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0768-y · Cited by 57 · 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
RIM-BP2 primes synaptic vesicles via recruitment of Munc13-1 at hippocampal mossy fiber synapses
Brockmann, M. M., Maglione, M., Willmes, C., Stumpf, A., Bouazza, B. A., Velasquez, L. M., Grauel, M., Beed, P., Lehmann, M., Gimber, N., et al. (2018) · bioRxiv · doi:10.7554/elife.43243 · Cited by 53 · see citing works
Structural plasticity of hippocampal mossy fiber synapses as revealed by high‐pressure freezing
Zhao, S., Studer, D., Chai, X., Graber, W. A., Brose, N., Nestel, S., Young, C. C., Rodriguez, E., Saetzler, K., & Frotscher, M. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23040 · Cited by 56 · see citing works
Self-citationSpermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses
Maglione, M., Kochlamazashvili, G., Eisenberg, T., Rácz, B., Michael, E., Toppe, D., Stumpf, A., Wirth, A., Zeug, A., Müller, F. E., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-56133-3 · Cited by 55 · see citing works
Understanding the molecular diversity of synapses
van Oostrum, M., & Schuman, E. M. (2025) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00888-w · Cited by 49 · see citing works
Are unreliable release mechanisms conserved from NMJ to CNS?
Tarr, T. B., Dittrich, M., & Meriney, S. D. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.09.009 · Cited by 52 · see citing works
Yakoubi, R., Rollenhagen, A., von Lehe, M., Shao, Y., Sätzler, K., & Lübke, J. H. R. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy146 · Cited by 55 · see citing works
Self-citationLin, K., Oleskevich, S., & Taschenberger, H. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.209189 · Cited by 51 · see citing works
Yakoubi, R., Rollenhagen, A., von Lehe, M., Miller, D., Walkenfort, B., Hasenberg, M., Sätzler, K., & Lübke, J. H. R. (2019) · eLife · doi:10.7554/elife.48373 · Cited by 53 · see citing works
Self-citationNeuroD2 regulates the development of hippocampal mossy fiber synapses
Wilke, S. A., Hall, B. J., Antonios, J. K., DeNardo, L. A., Otto, S. J., Yuan, B., Chen, F., Robbins, E. M., Tiglio, K., Williams, M. E., et al. (2012) · Neural Development · doi:10.1186/1749-8104-7-9 · Cited by 51 · 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
Ablating astrocyte insulin receptors leads to delayed puberty and hypogonadism in mice
Manaserh, I. H., Chikkamenahalli, L. L., Ravi, S., Dube, P. R., Park, J. J., & Hill, J. W. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000189 · Cited by 49 · see citing works
Heterogeneity of glutamatergic synapses: cellular mechanisms and network consequences
Wichmann, C., & Kuner, T. (2021) · Physiological Reviews · doi:10.1152/physrev.00039.2020 · Cited by 59 · see citing works
Szabadics, J., Varga, C., Brunner, J., Chen, K., & Soltész, I. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5602-09.2010 · Cited by 49 · see citing works
Chamberland, S., Evstratova, A., & Tóth, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0847-14.2014 · Cited by 48 · see citing works
Dense 4D nanoscale reconstruction of living brain tissue
Velicky, P., Miguel, E., Michalska, J. M., Lyudchik, J., Wei, D., Lin, Z., Watson, J. F., Troidl, J., Beyer, J., Ben‐Simon, Y., et al. (2023) · Nature Methods · doi:10.1038/s41592-023-01936-6 · Cited by 43 · see citing works
Upreti, C., Otero, R., Partida, C., Skinner, F., Thakker, R. A., Otalora, L. F. P., Zhou, Z., Maglakelidze, G., Velı́šková, J., Velı́šek, L., et al. (2012) · Brain · doi:10.1093/brain/awr341 · Cited by 48 · see citing works
McAuliffe, J. J., Bronson, S. L., Hester, M. S., Murphy, B. L., Dahlquist‐Topalá, R., Richards, D. A., & Danzer, S. C. (2011) · Hippocampus · doi:10.1002/hipo.20726 · Cited by 47 · see citing works
Rollenhagen, A., Klook, K., Sätzler, K., Qi, G., Anstötz, M., Feldmeyer, D., & Lübke, J. H. R. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0850-5 · Cited by 53 · see citing works
Self-citationAtypical Functional Properties of GluK3-Containing Kainate Receptors
Perrais, D., Coussen, F., & Mulle, C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2724-09.2009 · Cited by 47 · see citing works
cAMP-Dependent Synaptic Plasticity at the Hippocampal Mossy Fiber Terminal
Shahoha, M., Cohen, R., Ben-Simon, Y., & Ashery, U. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.861215 · Cited by 46 · see citing works
Evstratova, A., Chamberland, S., Faúndez, V., & Tóth, K. (2014) · Nature Communications · doi:10.1038/ncomms6530 · Cited by 46 · see citing works
Differential expression of liprin‐α family proteins in the brain suggests functional diversification
Spangler, S. A., Jaarsma, D., de Graaff, E., Wulf, P. S., Akhmanova, A. S., & Hoogenraad, C. C. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22665 · Cited by 45 · see citing works
Structure, biophysics, and circuit function of a “giant” cortical presynaptic terminal
Vandael, D., & Jonas, P. (2024) · Science · doi:10.1126/science.adg6757 · Cited by 45 · see citing works
Kikuchi, T., González‐Soriano, J., Kastanauskaite, A., Benavides‐Piccione, R., Merchán-Pérez, Á., DeFelipe, J., & Blázquez‐Llorca, L. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz343 · Cited by 43 · see citing works
Lavoie, N., Jeyaraju, D. V., Peralta, M. R., Seress, L., Pellegrini, L., & Tóth, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4164-11.2011 · Cited by 42 · see citing works
Brandalise, F., & Gerber, U. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1317667111 · Cited by 43 · see citing works
Invaginating Structures in Mammalian Synapses
Petralia, R. S., Wang, Y., Mattson, M. P., & Yao, P. J. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00004 · Cited by 42 · see citing works
Fukaya, R., Maglione, M., Sigrist, S. J., & Sakaba, T. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016754118 · Cited by 42 · see citing works
Zucca, S., Griguoli, M., Malézieux, M., Grosjean, N., Carta, M., & Mulle, C. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2057-16.2016 · Cited by 39 · see citing works
Rollenhagen, A., Ohana, O., Sätzler, K., Hilgetag, C. C., Kuhl, D., & Lübke, J. H. R. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00024 · Cited by 45 · see citing works
Self-citationChamberland, 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
Transmitter release site organization can predict synaptic function at the neuromuscular junction
Laghaei, R., Ma, J., Tarr, T. B., Homan, A. E., Kelly, L. S., Tilvawala, M., Vuocolo, B. S., Rajasekaran, H. P., Meriney, S. D., & Dittrich, M. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00168.2017 · Cited by 33 · see citing works
An emerging view of presynaptic structure from electron microscopic studies
Siksou, L., Triller, A., & Marty, S. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.05888.x · Cited by 37 · see citing works
Martinello, K., Giacalone, E., Migliore, M., Brown, D. A., & Shah, M. M. (2019) · Communications Biology · doi:10.1038/s42003-019-0408-4 · Cited by 32 · see citing works
Fukaya, R., Hirai, H., Sakamoto, H., Hashimotodani, Y., Hirose, K., & Sakaba, T. (2023) · Science Advances · doi:10.1126/sciadv.add3616 · Cited by 34 · see citing works
Liu, J., Qi, J., Chen, X., Li, Z., Hong, B., Ma, H., Li, G., Shen, L., Liu, D., Kong, Y., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111151 · Cited by 33 · see citing works
Lee, S. H., Lutz, D., Mossalam, M., Bolshakov, V. Y., Frotscher, M., & Shen, J. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0189-5 · Cited by 33 · see citing works
Self-citationThe single place fields of CA3 cells: A two‐stage transformation from grid cells
de Almeida, L., Idiart, M., & Lisman, J. E. (2010) · Hippocampus · doi:10.1002/hipo.20882 · Cited by 32 · see citing works
Presynaptic active zone density during development and synaptic plasticity
Clarke, G. L. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00012 · Cited by 33 · see citing works
Ali, A. A. H., Schwarz‐Herzke, B., Rollenhagen, A., Anstötz, M., Holub, M., Lübke, J. H. R., Rose, C. R., Schnittler, H., & von Gall, C. (2019) · Glia · doi:10.1002/glia.23754 · Cited by 32 · see citing works
Self-citationStructural plasticity of spines at giant mossy fiber synapses
Zhao, S., Studer, D., Chai, X., Graber, W. A., Brose, N., Nestel, S., Young, C. C., Rodriguez, E., Saetzler, K., & Frotscher, M. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00103 · Cited by 37 · see citing works
Self-citationMaingret, V., Barthet, G., Deforges, S., Jiang, N., Mulle, C., & Amédée, T. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.10.012 · Cited by 30 · see citing works
Dufour, A., Rollenhagen, A., Sätzler, K., & Lübke, J. H. R. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv270 · Cited by 37 · see citing works
Self-citationOrlando, M., Dvorzhak, A., Bruentgens, F., Maglione, M., Rost, B. R., Sigrist, S. J., Breustedt, J., & Schmitz, D. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001149 · Cited by 30 · see citing works
Wilke, S. A., Raam, T., Antonios, J. K., Bushong, E. A., Koo, E. H., Ellisman, M. H., & Ghosh, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084349 · Cited by 30 · see citing works
Martin, E. A., Woodruff, D. M., Rawson, R. L., & Williams, M. E. (2017) · eNeuro · doi:10.1523/eneuro.0088-17.2017 · Cited by 29 · see citing works
- Authors
- Rollenhagen, A., Sätzler, K., Rodríguez, E. P., Jonas, P., Frotscher, M., & Lübke, J. H. R.
- Affiliations
- Forschungszentrum Jülich (DE)
- University of Ulster (GB)
- University of Freiburg (DE)
- Corresponding author
- Lübke, Joachim H. R.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-09-26
- Volume
- 27
- Issue
- 39
- Pages
- 10434-10444
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673150
- OpenAlex
- W1976225114
- Cited by
- 246
- References
- 52
- Citations by year
- 2026: 5 · 2025: 16 · 2024: 19 · 2023: 15 · 2022: 8 · 2021: 18 · 2020: 15 · 2019: 25 · 2018: 18 · 2017: 18 · 2016: 9 · 2015: 9 · 2014: 16 · 2013: 5 · 2012: 14
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- JuSER (Forschungszentrum Jülich) (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft
- 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
- active zone, synaptic vesicles, readily releasable pool, synaptic vesicle recycling, reserve pool, presynaptic plasticity, 3D reconstruction
- MeSH terms
- Animals, Microscopy, Electron, Synaptic Transmission, Neuronal Plasticity, Synapses, Synaptic Vesicles, Rats, Wistar, Neurotransmitter Agents, Mossy Fibers, Hippocampal, Imaging, Three-Dimensional, Models, Animal, Rats
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
