The DOI matches its Crossref record; 46 of the 46 references it cites were found in a registry or an index.
Parvalbumin Is a Mobile Presynaptic Ca2+Buffer in the Calyx of Held that Accelerates the Decay of Ca2+and Short-Term Facilitation
Open accessAbstract
Presynaptic Ca 2+signaling plays a crucial role in short-term plasticity of synaptic transmission. Here, we studied the role of mobile endogenous presynaptic Ca 2+buffer(s) in modulating paired-pulse facilitation at a large excitatory nerve terminal in the auditory brainstem, the calyx of Held. To do so, we assessed the effect of presynaptic whole-cell recording, which should lead to the diffusional loss of endogenous mobile Ca 2+buffers, on paired-pulse facilitation and on intracellular Ca 2+concentration ([Ca 2+]i) transients evoked by action potentials. In unperturbed calyces briefly preloaded with the Ca 2+indicator fura-6F, the [Ca 2+]i transient decayed surprisingly fast (τ fast, ∼30 ms). Presynaptic whole-cell recordings made without additional Ca 2+buffers slowed the decay kinetics of [Ca 2+]i and paired-pulse facilitation (twofold to threefold), but the amplitude of the [Ca 2+]i transient was changed only marginally. The fast [Ca 2+]i decay was restored by adding the slow Ca 2+buffer EGTA (50–100 μ m) or parvalbumin (100 μ m), a Ca 2+-binding protein with slow Ca 2+-binding kinetics, to the presynaptic pipette solution. In contrast, the fast Ca 2+buffer fura-2 strongly reduced the amplitude of the [Ca 2+]i transient and slowed its decay, suggesting that the mobile endogenous buffer in calyces of Held has slow, rather than fast, binding kinetics. In parvalbumin knock-out mice, the decay of [Ca 2+]i and facilitation was slowed approximately twofold compared with wild-type mice, similar to what is observed during whole-cell recordings in rat calyces of Held. Thus, in young calyces of Held, a mobile Ca 2+buffer with slow binding kinetics, primarily represented by parvalbumin, accelerates the decay of spatially averaged [Ca 2+]i and paired-pulse facilitation.
Overview
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
Figures
![Figure1 Rapid decay of AP-induced [Ca 2 + ] i transients in unperturbed calyces of Held. A , Fluorescence image showing a calyx of Held that was preloaded with 80 -100 𝛍 M fura-6F during a brief ( ∼ 30 s) whole-cell recording (left image taken at 1 × 1 pixel binning; right image taken at 8 × 15 binning). Scale bar, 10 𝛍 m. B , Fluorescence signals (top gray traces) of the six superpixels marked in A (black dots in right image) and the resulting average fluorescence signal (superimposed black trace) during a single 100 Hz train of 10 stimuli. The bottom black trace represents the background-corrected average fluorescence signal. The F 355 values (gray circles) measured before and after the stimulation were linearly interpolated (black dotted line) and used to calculate the fluorescence ratio (see Materials and Methods). C , Average [Ca 2 + ] i transients elicited by single APs (average of n = 32traces; C1 ) or by 10 APs at 100 Hz (average of n = 4; C2 ) in a calyx preloaded with fura-6F. The decays of both [Ca 2 + ] i transients were fitted with double exponentials (red traces). D , Average [Ca 2 + ] i transients evoked by single APs ( D1 ) and by 10 APs at 100 Hz ( D2 ), as assessed during a continuous whole-cell recording with 100 𝛍 Mfura-6F of the same terminal as shown in A-C . For comparison, the corresponding [Ca 2 + ] i transients obtained after preloading ( C ) are shown as dotted traces. The insets depict presynaptic APs measured in response to single stimuli and 100 Hz trains. Data in A-D are from the same cell. E , Fast decay time constants ( 𝛕 fast ; left) and mean amplitudes (right) of single AP-evoked [Ca 2 + ] i transients recorded in n = 5rat calyces after preloading (open bar) andafterrepatching(graybar).Notethesignificant slowing after repatching ( p = 0.009). F , Fast decay time constants ( 𝛕 fast ; left) and amplitudes ([Ca 2 + ] i ; right) of [Ca 2 + ] i transients in response to the 100 Hz trains.](/paper-figures/4cba6041d53f4e3c97ca1bf60ac4e289/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-1.png)
![Figure 2 TheslowCa 2 + buffers EGTA and parvalbumin restore the fast decay of AP-evoked [Ca 2 + ] i transients. A , AP-evoked [Ca 2 + ] i transient (average of n = 21sweeps)during presynaptic whole-cell recording of a calyx of Held with 100 𝛍 M fura-6F in the pipette solution. B , A [Ca 2 + ] i transient (average of n = 32) from another calyx, recorded with 100 𝛍 M fura-6F and 100 𝛍 M EGTA in the pipette solution. C , Example of a [Ca 2 + ] i transient (average of n = 18) measuredinaratcalyxwith100 𝛍 Mfura-6F and 100 𝛍 Mparvalbuminaddedtothepresynaptic pipette solution. Note that the [Ca 2 + ] i transients decay more rapidly in the presence of EGTA ( B ) and parvalbumin ( C ) compared with the no-added buffer condition ( A ). D , Example of a [Ca 2 + ] i transient (average of n = 10 sweeps) recorded with 50 𝛍 M fura-2. Note the small amplitude and the slow decay of [Ca 2 + ] i . In A-D , red lines are double-exponential ( A-C ) or single-exponential ( D ) fits of the [Ca 2 + ] i decay. E , Average fast decay time constants ( 𝛕 fast ) of AP-evoked [Ca 2 + ] i transients of calyces of Held recorded with 100 𝛍 Mfura-6F (open bars; n = 4 cells), 100 𝛍 M fura-6F and 100 𝛍 M EGTA (gray bars; n = 4 cells), 100 𝛍 M fura-6F and 50 𝛍 M parvalbumin (open red bar; n = 3 cells), 100 𝛍 M fura-6F and 100 𝛍 M parvalbumin (filled red bar; n = 4), or 50 𝛍 M fura-2 (blue bar; n = 5). The fura-2 data, which have an order of magnitude slower [Ca 2 + ] i decay, are plotted on the right y -axis. Note that 100 𝛍 M parvalbumin restored the rapid [Ca 2 + ] i decay observed in unperturbed calyces of Held (Fig. 1 E ) ( p = 0.4). F , Mean [Ca 2 + ] i amplitudes measured under the various Ca 2 + buffer conditions. The black and gray dotted lines in E and F represent the average ± SD of the corresponding values obtained in measurements of unperturbed calyces of Held (Fig. 1 E ).](/paper-figures/2676f2ad56904cf48f0069bf501b739b/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-2.png)

![Figure 4 Theinfluence of presynaptically added Ca 2 + buffers on paired-pulse facilitation and presynaptic [Ca 2 + ] i transients. A1 , Examples of presynaptic whole-cell calcium currents ( I Ca ) and EPSCs in response to paired voltage-clamp pulses of three different interstimulus intervals ( 𝚫 t ). A2 , Paired-pulse facilitation (mean ± SEM) of the recording shown in A1 . The data were fitted with an exponential function, with time constant 𝛕 = 93 ms. B , Paired-pulse facilitation in another cell pair, in which 100 𝛍 M EGTA was added to the presynaptic intracellular solution. Note the accelerated decay of facilitation. C , Mean facilitation (top) and presynaptic [Ca 2 + ] i (bottom) measured with 100 𝛍 M fura-6F added to the presynaptic pipette solution. D , Facilitation and presynaptic [Ca 2 + ] i transient in a cell pair recorded with 100 𝛍 M fura-6F and 75 𝛍 M EGTA in the presynaptic pipette solution. E , Facilitation and presynaptic [Ca 2 + ] i of a cell pair recorded with 50 𝛍 Mfura-2inthepresynapticpipettesolution. In A2-E , red lines are single- or double-exponential fits, with the time constants ( 𝛕 ) or fast time constants in the case of double-exponential fits ( 𝛕 fast ) as indicated. F , Average decay time constants of facilitation recorded under the various conditions of presynaptically added Ca 2 + buffer. Note the significant speeding of the decay of facilitation to ∼ 30 ms induced by 100 𝛍 M EGTA ( p = 0.029) or by 75 𝛍 M EGTA and 100 𝛍 M fura-6F ( p = 0.005). G , Average fast decay time constants of [Ca 2 + ] i transients recorded with 100 𝛍 M fura-6F without addedbuffer(redopenbar; n = 4cells) and with 75 𝛍 MEGTA( n = 9; red bar). The blue bar (right ordinate) shows the average decay time constant of [Ca 2 + ] i (monoexponential fit) measured with 50 𝛍 M fura-2 ( n = 3). EGTA (75 𝛍 M) significantly ( p = 0.0005) accelerated the decay of [Ca 2 + ] i compared with the no-added buffer condition (arrowhead). H , Amplitude of facilitation under the different conditions of presynaptically added Ca 2 + buffers. Note the significant decrease in facilitation in the presynaptic presence of 50 𝛍 M fura-2 (blue bar).](/paper-figures/5abfbb251d7b4f1da9a77008fb9d8e5b/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-4.png)
![Figure 5 AP-induced presynaptic [Ca 2 + ] i transients decay slowly in parvalbumin knockout mice. A , B , Example of [Ca 2 + ] i transients in a calyx of Held from a PV -/ -mouse ( A ) and from a wild-type (wt) mouse ( B ). The decay of the [Ca 2 + ] i transients were fitted with doubleexponential functions (gray traces). C , D , Average fast decay time constants ( 𝛕 fast ; C ) and average amplitudes ([Ca 2 + ] i ; D ) of [Ca 2 + ] i transients elicited by single APs in PV -/ -(gray bars; n = 11cells) and in wild-type (white bars; n = 7cells) cells. Note the significant slowing ( p = 0.0005) of the [Ca 2 + ] i transients in PV -/ -mice, whereas the [Ca 2 + ] i amplitudes were not significantly different ( p = 0.42).](/paper-figures/358f1484c8c544fea1f41a83a795a2c2/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-5.png)
![Figure 6 Paired-pulse facilitation decays slowly at the calyx of Held of parvalbumin knock-out mice. A1 , Representative EPSCs in response to pulse pairs at three different interstimulus intervals ( 𝚫 t ) in a PV -/ -cell, recorded at 0.6 mM extracellular [Ca 2 + ]. A2 , Mean facilitation as a function of the interstimulus interval of the PV -/ -cell shown in A1 ( n = 15 repetitions). The data were fitted by an exponential function, with a time constant of 77 ms. B , Paired-pulse facilitation in a cell from a wild-type (wt) mouse ( n = 17 repetitions). Note the fast decay of paired-pulse facilitation, with a time constant of 17 ms in this cell. C , Average decay time constants of paired-pulse facilitation obtained in n = 8 cells from PV -/ -mice (gray bar), and in n = 7 cells from wild-type mice (white bar). Note the significantly ( p = 0.039) slower decay of paired-pulse facilitation in PV -/ -mice. D , The amplitude of paired-pulse facilitation was unchanged between wild-type mice (open bar; n = 7 cells) and PV -/ -mice (gray bar; n = 8 cells; p = 0.96).](/paper-figures/75c258deacd745998cb1c09c00c30a46/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-6.png)
![Figure 7 Amodified single-compartment model of Ca 2 + signaling at the calyx of Held. An AP-evoked, spatially averaged [Ca 2 + ] i transient was simulated either in the absence of a slow Ca 2 + buffer (gray trace) or in the presence of 50 𝛍 M parvalbumin (PV). See Materials and Methods for the parameters used in the simulation. The inset shows the simulated [Ca 2 + ] i traces at increased time resolution. The simulated [Ca 2 + ] i transient in the absence of parvalbumin(graytraces)waswellfittedbyasingle-exponentialfunction,withtimeconstant 𝛕 = 78 ms.Inthepresenceof50 𝛍 Mparvalbumin, the initial decay of [Ca 2 + ] i wasaccelerated, and the decay of [Ca 2 + ] i was now best fit by a double-exponential function, with fast and slow time constants of 31 and 1310 ms, respectively. Note that the combination of a low endogenous Ca 2 + buffer capacity ( 𝛋 s = 40), a fast Ca 2 + extrusion rate ( 𝛄 = 500 s -1 ), and the presence of a Ca 2 + buffer with slow binding kinetics result in an extremely fast initial decay of spatially averaged [Ca 2 + ] i .](/paper-figures/9b99d76424884970b42fe343851cb84e/parvalbumin-is-a-mobile-presynaptic-ca-sup-2-sup-buffer-in-the-calyx-of-held-figure-7.png)
Verification
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?
In the citing paper
“The absence of PV in PV-/- Pvalb neurons does not affect basal synaptic transmission, but enhances facilitation [49, 50] and shortens delayed transmitter release [51].”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz, G., Poenie, M., & Tsien, R. Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83641-4 · Cited by 21,562
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023
Short-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
Calbindin D-28k and parvalbumin in the rat nervous system
Celio, M. R. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90091-h · Cited by 2,076
Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing
Rudy, B., & McBain, C. J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01892-0 · Cited by 781
Calcium gradients and buffers in bovine chromaffin cells.
Neher, E., & Augustine, G. J. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019127 · Cited by 753
Calcium influx and transmitter release in a fast CNS synapse
Borst, J. G. G., & Sakmann, B. J. (1996) · Nature · doi:10.1038/383431a0 · Cited by 632
Schneggenburger, R., Meyer, A. C., & Neher, E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80789-8 · Cited by 625
Self-citationDeterminants of the Time Course of Facilitation at the Granule Cell to Purkinje Cell Synapse
Atluri, P. P., & Regehr, W. G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-18-05661.1996 · Cited by 513
Pre‐ and postsynaptic whole‐cell recordings in the medial nucleus of the trapezoid body of the rat.
Borst, J. G. G., Helmchen, F., & Sakmann, B. J. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp021095 · Cited by 427
Cited by
Sorted by citations
Multiple Roles of Calcium Ions in the Regulation of Neurotransmitter Release
Neher, E., & Sakaba, T. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.019 · Cited by 966
Calcium Channel Regulation and Presynaptic Plasticity
Catterall, W. A., & Few, A. P. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.005 · Cited by 647
González‐Burgos, G., & Lewis, D. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn070 · Cited by 592
Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses
Eggermann, E., Bucurenciu, I., Goswami, S. P., & Jonas, P. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3125 · Cited by 500
Short-Term Presynaptic Plasticity
Regehr, W. G. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005702 · Cited by 482
Calcium Channels, Synaptic Plasticity, and Neuropsychiatric Disease
Nanou, E., & Catterall, W. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.017 · Cited by 492
GABAergic Interneurons Shape the Functional Maturation of the Cortex
Le Magueresse, C., & Monyer, H. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.011 · Cited by 425
Cytosolic Ca2+ BuffersPreprint
Schwaller, B. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004051 · Cited by 387
Self-citationNeuroplasticity of Neocortical Circuits in Schizophrenia
Lewis, D. A., & González‐Burgos, G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301563 · Cited by 372
Bucurenciu, I., Kulik, A., Schwaller, B., Frotscher, M., & Jonas, P. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.026 · Cited by 274
Self-citationThe continuing disappearance of “pure” Ca2+ buffers
Schwaller, B. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8564-6 · Cited by 257
Self-citationGABA Neuron Alterations, Cortical Circuit Dysfunction and Cognitive Deficits in Schizophrenia
González‐Burgos, G., Fish, K. N., & Lewis, D. A. (2011) · Neural Plasticity · doi:10.1155/2011/723184 · Cited by 250
Filice, F., Vörckel, K. J., Sungur, A. Ö., Wöhr, M., & Schwaller, B. (2016) · Molecular Brain · doi:10.1186/s13041-016-0192-8 · Cited by 240
Self-citationOxidative Stress‐Related Mechanisms in Schizophrenia Pathogenesis and New Treatment Perspectives
Ermakov, E. A., Dmitrieva, E. M., Parshukova, D. A., Kazantseva, D. V., Vasilieva, A. R., & Smirnova, L. P. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8881770 · Cited by 256
The Calyx of Held Synapse: From Model Synapse to Auditory Relay
Borst, J. G. G., & van Hoeve, J. S. S. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153236 · Cited by 225
A General Model of Synaptic Transmission and Short-Term Plasticity
Pan, B., & Zucker, R. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.025 · Cited by 195
Calcium Signaling in Dendritic SpinesPreprint
Higley, M. J., & Sabatini, B. L. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005686 · Cited by 187
Calcium Channels and Short-term Synaptic Plasticity
Catterall, W. A., Leal, K., & Nanou, E. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.r112.411645 · Cited by 153
Physiology of intracellular calcium buffering
Eisner, D. A., Neher, E., Taschenberger, H., & Smith, G. L. (2023) · Physiological Reviews · doi:10.1152/physrev.00042.2022 · Cited by 162
Hoftman, G. D., & Lewis, D. A. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr029 · Cited by 128
The Parvalbumin Hypothesis of Autism Spectrum Disorder
Filice, F., Janickova, L., Henzi, T., Bilella, A., & Schwaller, B. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.577525 · Cited by 118
Self-citationBrenowitz, S. D., & Regehr, W. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1064-07.2007 · Cited by 114
Calcium-Binding Proteins as Determinants of Central Nervous System Neuronal Vulnerability to Disease
Fairless, R., Williams, S. K., & Diem, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092146 · Cited by 110
Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool
Lee, J. S., Ho, W., & Lee, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114072109 · Cited by 102
Relative Roles of Different Mechanisms of Depression at the Mouse Endbulb of Held
Yang, H., & Xu‐Friedman, M. A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01293.2007 · Cited by 101
Sommeijer, J.-P., & Levelt, C. N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035323 · Cited by 100
Regulation of transmitter release by Ca2+ and synaptotagmin: insights from a large CNS synapse
Kochubey, O., Lou, X., & Schneggenburger, R. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.02.006 · Cited by 92
Self-citationCytosolic Ca 2+ Buffers Are Inherently Ca 2+ Signal ModulatorsPreprint
Schwaller, B. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a035543 · Cited by 94
Self-citationJiang, M., Zhu, J., Liu, Y., Yang, M., Tian, C., Jiang, S., Wang, Y., Guo, H., Wang, K., & Shu, Y. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001324 · Cited by 89
Orduz, D., Bischop, D. P., Schwaller, B., Schiffmann, S. N., & Gall, D. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.250795 · Cited by 88
Self-citationLin, K., Taschenberger, H., & Neher, E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2207987119 · Cited by 84
Efficient Ca2+ buffering in fast‐spiking basket cells of rat hippocampus
Aponte, Y., Bischofberger, J., & Jónás, P. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.147298 · Cited by 81
Bornschein, G., Arendt, O., Hallermann, S., Brachtendorf, S., Eilers, J., & Schmidt, H. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.254128 · Cited by 84
Lazarus, M. S., & Huang, Z. J. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00729.2010 · Cited by 77
Schwaller, B. (2012) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.11.008 · Cited by 75
Self-citationThe chandelier neuron in schizophrenia
Lewis, D. A. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20825 · Cited by 76
Müller, M., Felmy, F., & Schneggenburger, R. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.155838 · Cited by 71
Self-citationChang, 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
Müller, M., Goutman, J., Kochubey, O., & Schneggenburger, R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4378-09.2010 · Cited by 67
Self-citationAltered Cortical GABA Neurotransmission in Schizophrenia: Insights into Novel Therapeutic Strategies
Stan, A. D., & Lewis, D. A. (2012) · Current Pharmaceutical Biotechnology · doi:10.2174/138920112800784925 · Cited by 64
Developmental Changes in Short-Term Plasticity at the Rat Calyx of Held Synapse
Crins, T., Rusu, S., Rodríguez-Contreras, A., & Borst, J. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1995-11.2011 · Cited by 59
Wang, L., Fedchyshyn, M. J., & Yang, Y. (2009) · Molecular Brain · doi:10.1186/1756-6606-2-36 · Cited by 60
Reduced endogenous Ca 2+ buffering speeds active zone Ca 2+ signaling
Delvendahl, I., Jablonski, L., Baade, C., Matveev, V., Neher, E., & Hallermann, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1508419112 · Cited by 63
Mechanisms of short‐term plasticity at neuromuscular active zones of Drosophila
Hallermann, S., Heckmann, M., & Kittel, R. J. (2010) · HFSP journal · doi:10.2976/1.3338710 · Cited by 58
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 61
Self-citationFast resupply of synaptic vesicles requires synaptotagmin-3
Weingarten, D. J., Shrestha, A., Juda-Nelson, K., Kissiwaa, S. A., Spruston, E., & Jackman, S. L. (2022) · Nature · doi:10.1038/s41586-022-05337-1 · Cited by 55
Guilmi, M. N. D., Wang, T., Inchauspe, C. G., Forsythe, I. D., Ferrari, M. D., van den Maagdenberg, A. M. J. M., Borst, J. G. G., & Uchitel, O. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2526-13.2014 · Cited by 53
Cortical Interneuron Subtypes Vary in Their Axonal Action Potential Properties
Casale, A. E., Foust, A. J., Bal, T., & McCormick, D. A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1467-13.2015 · Cited by 53
Lipstein, 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 53
Neuroplasticity of excitatory and inhibitory cortical circuits in schizophrenia
Lewis, D. A. (2009) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2009.11.3/dalewis · Cited by 56
Curley, A. A., Eggan, S. M., Lazarus, M. S., Huang, Z. J., Volk, D. W., & Lewis, D. A. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.018 · Cited by 51
Mechanisms underlying short‐term modulation of transmitter release by presynaptic depolarization
Hori, T., & Takahashi, T. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.168765 · Cited by 51
Synaptic plasticity in the auditory system: a review
Friauf, E., Fischer, A. U., & Fuhr, M. F. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2176-x · Cited by 49
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 52
Kosaka, T., & Kosaka, K. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.09.008 · Cited by 48
Mochida, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092217 · Cited by 49
Kumar, P., Goettemoeller, A. M., Espinosa‐García, C., Tobin, B. R., Tfaily, A., Nelson, R. S., Natu, A., Dammer, E. B., Santiago, J. V., Malepati, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47028-7 · Cited by 53
A Single-Compartment Model of Calcium Dynamics in Nerve Terminals and DendritesPreprint
Helmchen, F., & Tank, D. W. (2015) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top085910 · Cited by 47
Acute Complexin Knockout Abates Spontaneous and Evoked Transmitter Release
López-Murcia, F. J., Reim, K., Jahn, O., Taschenberger, H., & Brose, N. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.030 · Cited by 45
The Calyx of Held in the auditory system: structure, function, and development
Baydyuk, M., Xu, J.-H., & Wu, L. (2016) · Hearing Research · doi:10.1016/j.heares.2016.03.009 · Cited by 33
Turovsky, E. A., Turovskaya, M. V., Kononov, A. V., & Зинченко, В. П. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.09.006 · Cited by 35
A theory of synaptic transmission
Wang, B., & Dudko, O. K. (2021) · eLife · doi:10.7554/elife.73585 · Cited by 38
Decreased parvalbumin mRNA expression in dorsolateral prefrontal cortex in Parkinson′s disease
Lanoue, A. C., Blatt, G. J., & Soghomonian, J. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.025 · Cited by 36
Woehler, A., Lin, K., & Neher, E. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.281097 · Cited by 31
Leão, R. M., & von Gersdorff, H. (2009) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2009000100014 · Cited by 32
Zhang, X., Xu, L., Zhu, X., Tang, Z.-H., Dong, Y.-B., Yu, Z., Shang, Q. S., Wang, Z., & Shen, H. (2023) · Nature Communications · doi:10.1038/s41467-023-43930-8 · Cited by 29
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 28
Nakamura, Y., Reva, M., & DiGregorio, D. A. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2061-17.2018 · Cited by 30
Hennig, M. H., Postlethwaite, M., Forsythe, I. D., & Graham, B. P. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.152124 · Cited by 29
Shepard, R. M., Heslin, K. A., & Coutellier, L. D. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.12.012 · Cited by 27
Short-term synaptic plasticity and intensity coding
MacLeod, K. M. (2011) · Hearing Research · doi:10.1016/j.heares.2011.03.001 · Cited by 29
Yao, L., & Sakaba, T. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00685.2010 · Cited by 26
Makowiecki, K., Garrett, A. R., Harvey, A. R., & Rodger, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-23979-y · Cited by 26
Neurotransmitter Release Site Replenishment and Presynaptic Plasticity
Mochida, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010327 · Cited by 26
Neher, E., & Taschenberger, H. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.10.012 · Cited by 15
Ca 2+ regulation of glutamate release from inner hair cells of hearing mice
Tobón, L. M. J., & Moser, T. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2311539120 · Cited by 25
Gilmanov, I. R., Samigullin, D. V., Vyskočil, F., Nikolsky, E. E., & Bukharaeva, E. A. (2008) · Journal of Computational Neuroscience · doi:10.1007/s10827-008-0079-5 · Cited by 24
Wichmann, C. (2015) · Hearing Research · doi:10.1016/j.heares.2015.07.008 · Cited by 21
Burgess, J. R., & Raven, E. L. (2009) · Advances in inorganic chemistry · doi:10.1016/s0898-8838(09)00205-0 · Cited by 21
Sehring, I. M., Klotz, C., Beisson, J., & Plattner, H. (2008) · Cell Calcium · doi:10.1016/j.ceca.2008.06.004 · Cited by 21
New insights into short-term synaptic facilitation at the frog neuromuscular junction
Ma, J., Kelly, L. S., Ingram, J., Price, T. J., Meriney, S. D., & Dittrich, M. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00198.2014 · Cited by 20
Iremonger, K. J., Benediktsson, A. M., & Bains, J. S. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.03.002 · Cited by 20
Babai, N. Z., Kochubey, O., Keller, D. X., & Schneggenburger, R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1990-14.2014 · Cited by 20
Self-citationLin, K., Erazo-Fischer, E., & Taschenberger, H. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3838-11.2012 · Cited by 19
Janickova, L., & Schwaller, B. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.571216 · Cited by 19
Self-citationLiao, C., & Lien, C. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.052 · Cited by 19
Lin, K., Taschenberger, H., & Neher, E. (2016) · The Journal of Physiology · doi:10.1113/jp272773 · Cited by 18
Presynaptic 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 17
Komaki, A., Shahidi, ., Sarihi, A., Hasanein, P., Lashgari, R., Haghparast, A., Salehi, I., & Kourosh‐Arami, M. (2013) · Europe PMC (PubMed Central) · Cited by 18
Szabolcsi, V., & Celio, M. R. (2014) · Glia · doi:10.1002/glia.22768 · Cited by 18
Schwaller, B. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374145-5.00120-0 · Cited by 17
Self-citationЗинченко, В. П., Turovskaya, M. V., Teplov, I. Y., Berezhnov, A. V., & Turovsky, E. A. (2016) · BIOPHYSICS · doi:10.1134/s0006350916010280 · Cited by 17
Details of Ca2+ dynamics matter
Neher, E. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.153080 · Cited by 16
Samigullin, D. V., Fatikhov, N. F., Khaziev, E. F., Skorinkin, A. I., Nikolsky, E. E., & Bukharaeva, E. A. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00029 · Cited by 15
Transients in global Ca 2+ concentration induced by electrical activity in a giant nerve terminal
Neher, E., & Taschenberger, H. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.248617 · Cited by 15
Zachařová, G., & Paleček, J. (2009) · Physiological Research · doi:10.33549/physiolres.931738 · Cited by 14
Diffusion of Ca2+ from Small Boutons en Passant into the Axon Shapes AP-Evoked Ca2+ Transients
Tran, V., & Stricker, C. (2018) · Biophysical Journal · doi:10.1016/j.bpj.2018.07.018 · Cited by 13
Loss of KCC2 in GABAergic Neurons Causes Seizures and an Imbalance of Cortical Interneurons
Zavalin, K. A., Hassan, A., Fu, C., Delpire, E. J., & Lagrange, A. H. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.826427 · Cited by 14
Gandhi, T., Liu, C., Adeyelu, T. T., Canepa, C. R., & Lee, C. C. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1114789 · Cited by 13
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
Metadata
- Authors
- Müller, M., Felmy, F., Schwaller, B., & Schneggenburger, R.
- Affiliations
- École Polytechnique Fédérale de Lausanne (CH)
- Ludwig-Maximilians-Universität München (DE)
- University of Fribourg (CH)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-02-28
- Volume
- 27
- Issue
- 9
- Pages
- 2261-2271
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673482
- OpenAlex
- W1975952480
- Cited by
- 155
- References
- 46
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 3 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 4 · 2019: 5 · 2018: 7 · 2017: 1 · 2016: 8 · 2015: 9 · 2014: 11 · 2013: 10 · 2012: 8
- FWCI
- 5.97
- 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)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- Deutsche Forschungsgemeinschaft (TP B1)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (100400, 3100A0)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Keywords
- parvalbumin, calyx of Held, paired-pulse facilitation, short-term plasticity, calcium transients, fura-2, EGTA, auditory brainstem, excitatory synapses
- MeSH terms
- Animals, Brain Stem, Calcium, Calcium-Binding Proteins, Mice, Inbred C57BL, Synaptic Transmission, Neuronal Plasticity, Parvalbumins, Rats, Wistar, Receptors, Presynaptic, Mice, Knockout, Patch-Clamp Techniques, Mice, Rats, In Vitro Techniques
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