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Abstract:

The two fundamental forms of short-term plasticity, short-term depression and facilitation, coexist at most synapses, but little is known about their interaction. Here, we studied the interplay between short-term depression and facilitation at calyx of Held synapses. Stimulation at a "low" frequency of 10 or 20 Hz, which is in the range of the spontaneous activity of these auditory neurons in vivo, induced synaptic depression. Surprisingly, an instantaneous increase of the stimulation frequency to 100 or 200 Hz following the low-frequency train uncovered a robust facilitation of EPSCs relative to the predepressed amplitude level. This facilitation decayed rapidly (∼30 ms) and depended on presynaptic residual Ca2+, but it was not caused by Ca2+ current facilitation. To probe the release probability of the remaining readily releasable vesicles following the low-frequency train we made presynaptic Ca2+ uncaging experiments in the predepressed state of the synapse. We found that low-frequency stimulation depletes the fast-releasable vesicle pool (FRP) down to ∼40% of control and that the remaining FRP vesicles are released with ∼2-fold slower release kinetics, indicating a hitherto unknown intrinsic heterogeneity among FRP vesicles. Thus, vesicles with an intrinsically lower release probability predominate after low frequency stimulation and undergo facilitation during the onset of subsequent high-frequency trains. Facilitation in the predepressed state of the synapse might help to stabilize the amount of transmitter release at the onset of high-frequency firing at these auditory synapses. Copyright © 2010 the authors.

Registro:

Documento: Artículo
Título:Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity
Autor:Müller, M.; Goutman, J.D.; Kochubey, O.; Schneggenburger, R.
Filiación:Laboratory of Synaptic Mechanisms, Brain-Mind Institute, École Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland
Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, United States
Instituto de Investigaciones en Ingeniería Genética Y Biología Molecular, Universidad Buenos Aires-Consejo Nacional de Investigaciones Científicas Y Técnicas, 1428 Buenos Aires, Argentina
Palabras clave:acoustic nerve fiber; animal experiment; animal tissue; article; brain slice; brain stem; central nervous system; facilitation; in vivo study; kinetics; nerve cell plasticity; nerve cell stimulation; neurotransmitter release; nonhuman; priority journal; probability; rat; synapse vesicle; synaptic inhibition; synaptic transmission; Wistar rat; Acoustic Stimulation; Action Potentials; Animals; Auditory Pathways; Brain Stem; Calcium; Excitatory Postsynaptic Potentials; Neuronal Plasticity; Neurotransmitter Agents; Patch-Clamp Techniques; Rats; Rats, Wistar; Synapses; Synaptic Vesicles
Año:2010
Volumen:30
Número:6
Página de inicio:2007
Página de fin:2016
DOI: http://dx.doi.org/10.1523/JNEUROSCI.4378-09.2010
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.
ISSN:02706474
CODEN:JNRSD
CAS:Calcium, 7440-70-2; Neurotransmitter Agents
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02706474_v30_n6_p2007_Muller

Referencias:

  • Atluri, P.P., Regehr, W.G., Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse (1996) J Neurosci, 16, pp. 5661-5671
  • Betz, W.J., Depression of transmitter release at the neuromuscular junction of the frog (1970) J Physiol, 206, pp. 629-644
  • Blatow, M., Caputi, A., Burnashev, N., Monyer, H., Rozov, A., Ca2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k- containing terminals (2003) Neuron, 38, pp. 79-88
  • Borst, J.G., Helmchen, F., Sakmann, B., Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat (1995) J Physiol, 489, pp. 825-840
  • Boudkkazi, S., Carlier, E., Ankri, N., Caillard, O., Giraud, P., Fronzaroli-Molinieres, L., Debanne, D., Release-dependent variations in synaptic latency: A putative code for short- and long-term synaptic dynamics (2007) Neuron, 56, pp. 1048-1060
  • Fedchyshyn, M.J., Wang, L.Y., Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse (2007) J Physiol, 581, pp. 581-602
  • Felmy, F., Schneggenburger, R., Developmental expression of the Ca 2+-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice (2004) Eur J Neurosci, 20, pp. 1473-1482
  • Felmy, F., Neher, E., Schneggenburger, R., Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation (2003) Neuron, 37, pp. 801-811
  • Forsythe, I.D., Tsujimoto, T., Barnes-Davies, M., Cuttle, M.F., Takahashi, T., Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse (1998) Neuron, 20, pp. 797-807
  • Foster, K.A., Regehr, W.G., Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse (2004) Neuron, 43, pp. 119-131
  • Grynkiewicz, G., Poenie, M., Tsien, R.Y., A new generation of Ca 2+ indicators with greatly improved fluorescence properties (1985) J Biol Chem, 260, pp. 3440-3450
  • Heinemann, C., Chow, R.H., Neher, E., Zucker, R.S., Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca 2+ (1994) Biophys J, 67, pp. 2546-2557
  • Helmchen, F., Borst, J.G., Sakmann, B., Calcium dynamics associated with a single action potential in a CNS presynaptic terminal (1997) Biophys J, 72, pp. 1458-1471
  • Hermann, J., Pecka, M., von Gersdorff, H., Grothe, B., Klug, A., Synaptic transmission at the calyx of Held under in vivo like activity levels (2007) J Neurophysiol, 98, pp. 807-820
  • Hori, T., Takahashi, T., Mechanisms underlying short-term modulation of transmitter release by presynaptic depolarization (2009) J Physiol, 587, pp. 2987-3000
  • Hsu, S.F., Augustine, G.J., Jackson, M.B., Adaptation of Ca 2+-triggered exocytosis in presynaptic terminals (1996) Neuron, 17, pp. 501-512
  • Inchauspe, C.G., Forsythe, I.D., Uchitel, O.D., Changes in synaptic transmission properties due to the expression of N-type calcium channels at the calyx of Held synapse of mice lacking P/Q-type calcium channels (2007) J Physiol, 584, pp. 835-851
  • Iwasaki, S., Takahashi, T., Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem (2001) J Physiol, 534, pp. 861-871
  • Katz, B., Miledi, R., The role of calcium in neuromuscular facilitation (1968) J Physiol, 195, pp. 481-492
  • Kochubey, O., Schneggenburger, R., Optical imaging in neuroscience: A laboratory manual, , 2010 Ca2+ uncaging in nerve terminals, eds, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, in press
  • Kochubey, O., Han, Y., Schneggenburger, R., Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca 2+ - secretion coupling at the rat calyx of Held (2009) J Physiol, 587, pp. 3009-3023
  • Kopp-Scheinpflug, C., Fuchs, K., Lippe, W.R., Tempel, B.L., Rübsamen, R., Decreased temporal precision of auditory signaling in Kcna1-null mice: An electrophysiological study in vivo (2003) J Neurosci, 23, pp. 9199-9207
  • Korogod, N., Lou, X., Schneggenburger, R., Presynaptic Ca2+ - requirements and developmental regulation of posttetanic potentiation at the calyx of Held (2005) J Neurosci, 25, pp. 5127-5137
  • Liley, A.W., North, K.A., An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction (1953) J Neurophysiol, 16, pp. 509-527
  • Lorteije, J.A., Rusu, S.I., Kushmerick, C., Borst, J.G., Reliability and precision of the mouse calyx of Held synapse (2009) J Neurosci, 29, pp. 13770-13784
  • Lou, X., Scheuss, V., Schneggenburger, R., Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion (2005) Nature, 435, pp. 497-501
  • Meyer, A.C., Neher, E., Schneggenburger, R., Estimation of quantal size and number of functional active zones at the calyx of Held synapse by nonstationary EPSC variance analysis (2001) J Neurosci, 21, pp. 7889-7900
  • Mochida, S., Few, A.P., Scheuer, T., Catterall, W.A., Regulation of presynaptic CaV2.1 channels by Ca2+ sensor proteins mediates short-term synaptic plasticity (2008) Neuron, 57, pp. 210-216
  • Müller, M., Felmy, F., Schwaller, B., Schneggenburger, R., Parvalbumin is a mobile presynaptic Ca2+ buffer in the calyx of Held that accelerates the decay of Ca2+ and short-term facilitation (2007) J Neurosci, 27, pp. 2261-2271
  • Müller, M., Felmy, F., Schneggenburger, R., A limited contribution of Ca2+ current facilitation to paired-pulse facilitation of transmitter release at the rat calyx of Held (2008) J Physiol, 586, pp. 5503-5520
  • Nakamura, T., Yamashita, T., Saitoh, N., Takahashi, T., Developmental changes in calcium/calmodulin-dependent inactivation of calcium currents at the rat calyx of Held (2008) J Physiol, 586, pp. 2253-2261
  • Naraghi, M., Müller, T.H., Neher, E., Two-dimensional determination of the cellular Ca2+ binding in bovine chromaffin cells (1998) Biophys J, 75, pp. 1635-1647
  • Neher, E., Sakaba, T., Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of Held (2001) J Neurosci, 21, pp. 444-461
  • Sakaba, T., Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of Held (2006) J Neurosci, 26, pp. 5863-5871
  • Sakaba, T., Neher, E., Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse (2001) Neuron, 32, pp. 1119-1131
  • Scheuss, V., Schneggenburger, R., Neher, E., Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of held synapse (2002) J Neurosci, 22, pp. 728-739
  • Schlüter, O.M., Basu, J., Südhof, T.C., Rosenmund, C., Rab3 superprimes synaptic vesicles for release: Implications for short-term synaptic plasticity (2006) J Neurosci, 26, pp. 1239-1246
  • Schneggenburger, R., Neher, E., Intracellular calcium dependence of transmitter release rates at a fast central synapse (2000) Nature, 406, pp. 889-893
  • Sommer, I., Lingenhohl, K., Friauf, E., Principal cells of the rat medial nucleus of the trapezoid body: An intracellular in vivo study of their physiology and morphology (1993) Exp Brain Res, 95, pp. 223-239
  • Sonntag, M., Englitz, B., Kopp-Scheinpflug, C., Rubsamen, R., Early postnatal development of spontaneous and acoustically evoked discharge activity of principal cells of the medial nucleus of the trapezoid body: An in vivo study in mice (2009) J Neurosci, 29, pp. 9510-9520
  • Tang, Y., Schlumpberger, T., Kim, T., Lueker, M., Zucker, R.S., Effects of mobile buffers on facilitation: Experimental and computational studies (2000) Biophys J, 78, pp. 2735-2751
  • Taschenberger, H., Scheuss, V., Neher, E., Release kinetics, quantal parameters and their modulation during short-term depression at a developing CNS synapse in the rat (2005) J Physiol, 568, pp. 513-537
  • Tolnai, S., Englitz, B., Scholbach, J., Jost, J., Rubsamen, R., Spike transmission delay at the calyx of Held in vivo: Rate dependence, phenomenological modeling, and relevance for sound localization (2009) J Neurophysiol, 102, pp. 1206-1217
  • Trommershäuser, J., Schneggenburger, R., Zippelius, A., Neher, E., Heterogeneous presynaptic release-probabilities: Functional relevance for short-term plasticity (2003) Biophys J, 84, pp. 1563-1579
  • von Gersdorff, H., Schneggenburger, R., Weis, S., Neher, E., Presynaptic depression at a calyx synapse: The small contribution of metabotropic glutamate receptors (1997) J Neurosci, 17, pp. 8137-8146
  • Wadel, K., Neher, E., Sakaba, T., The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release (2007) Neuron, 53, pp. 563-575
  • Waldeck, R.F., Pereda, A., Faber, D.S., Properties and plasticity of paired-pulse depression at a central synapse (2000) J Neurosci, 20, pp. 5312-5320
  • Wang, L.Y., Kaczmarek, L.K., High-frequency firing helps replenish the readily releasable pool of synaptic vesicles (1998) Nature, 394, pp. 384-388
  • Weis, S., Schneggenburger, R., Neher, E., Properties of a model of Ca2+-dependent vesicle pool dynamics and short term synaptic depression (1999) Biophys J, 77, pp. 2418-2429
  • Wölfel, M., Lou, X., Schneggenburger, R., A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse (2007) J Neurosci, 27, pp. 3198-3210
  • Wu, L.G., Borst, J.G., The reduced release probability of releasable vesicles during recovery from short-term synaptic depression (1999) Neuron, 23, pp. 821-832
  • Xu, J., Wu, L.G., The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse (2005) Neuron, 46, pp. 633-645
  • Zucker, R.S., Regehr, W.G., Short-term synaptic plasticity (2002) Annu Rev Physiol, 64, pp. 355-405

Citas:

---------- APA ----------
Müller, M., Goutman, J.D., Kochubey, O. & Schneggenburger, R. (2010) . Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity. Journal of Neuroscience, 30(6), 2007-2016.
http://dx.doi.org/10.1523/JNEUROSCI.4378-09.2010
---------- CHICAGO ----------
Müller, M., Goutman, J.D., Kochubey, O., Schneggenburger, R. "Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity" . Journal of Neuroscience 30, no. 6 (2010) : 2007-2016.
http://dx.doi.org/10.1523/JNEUROSCI.4378-09.2010
---------- MLA ----------
Müller, M., Goutman, J.D., Kochubey, O., Schneggenburger, R. "Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity" . Journal of Neuroscience, vol. 30, no. 6, 2010, pp. 2007-2016.
http://dx.doi.org/10.1523/JNEUROSCI.4378-09.2010
---------- VANCOUVER ----------
Müller, M., Goutman, J.D., Kochubey, O., Schneggenburger, R. Interaction between facilitation and depression at a large CNS synapse reveals mechanisms of short-term plasticity. J. Neurosci. 2010;30(6):2007-2016.
http://dx.doi.org/10.1523/JNEUROSCI.4378-09.2010