QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (173) Citing Articles via Google Scholar Google Scholar Articles by Regehr, W. G. Articles by Tank, D. W. Search for Related Content PubMed PubMed Citation Articles by Regehr, W. G. Articles by Tank, D. W.

 Previous Article  |  Next Article 

Journal of Neuroscience, Vol 14, 523-537, Copyright © 1994 by Society for Neuroscience

ARTICLE

The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse

WG Regehr, KR Delaney and DW Tank
AT&T Bell Laboratories, Murray Hill, New Jersey 07974.

The mossy fiber synapse between dentate granule cells and CA3 pyramidal cells in the guinea pig hippocampus shows a robust short-term synaptic enhancement. We have simultaneously measured presynaptic residual free calcium ([Ca2+]i) and postsynaptic field potentials at this synapse to examine the role of [Ca2+]i in this enhancement. Single action potentials produced an increase in [Ca2+]i of 10-50 nM that decayed to resting levels with a time constant of about 1 sec. Trains of action potentials produced larger [Ca2+]i increases that returned more slowly to resting levels. Following the onset of moderate frequency stimulus trains (0.1-5 Hz), synaptic transmission and [Ca2+]i both increased and eventually plateaued. During the steady-state phase a linear relationship between [Ca2+]i and synaptic enhancement was observed. During the initial buildup, however, [Ca2+]i rose more rapidly than synaptic enhancement. Similarly, during the decay phase immediately following termination of a stimulus train, [Ca2+]i returned to prestimulus levels faster than synaptic enhancement. High concentrations of the calcium buffer EGTA in the presynaptic terminal slowed the buildup and decay of both [Ca2+]i and synaptic enhancement produced by stimulus trains. Under these conditions, the time course of [Ca2+]i and synaptic enhancement were well matched. This suggests that, despite the differences in kinetic rates observed for normal buffering conditions, increases in [Ca2+]i play a causal role in short-term enhancement. An increase in [Ca2+]i of 10-30 nM produced a twofold enhancement. We propose a simple kinetic model to explain these results. The model assumes that synaptic enhancement is controlled by a Ca-dependent first-order reaction. According to this scheme, a change in [Ca2+]i alters neurotransmitter release, but the slow kinetics of the underlying reaction introduces a temporal filter, producing a delay in the change in synaptic enhancement.

This article has been cited by other articles:

				J. Breustedt, A. Gundlfinger, F. Varoqueaux, K. Reim, N. Brose, and D. Schmitz Munc13-2 Differentially Affects Hippocampal Synaptic Transmission and Plasticity Cereb Cortex, August 21, 2009; (2009) bhp170v1. [Abstract] [Full Text] [PDF]

				H. Vara, F. Onofri, F. Benfenati, M. Sassoe-Pognetto, and M. Giustetto ERK activation in axonal varicosities modulates presynaptic plasticity in the CA3 region of the hippocampus through synapsin I PNAS, June 16, 2009; 106(24): 9872 - 9877. [Abstract] [Full Text] [PDF]

				J. S. Lee, M.-H. Kim, W.-K. Ho, and S.-H. Lee Presynaptic Release Probability and Readily Releasable Pool Size Are Regulated by Two Independent Mechanisms during Posttetanic Potentiation at the Calyx of Held Synapse J. Neurosci., August 6, 2008; 28(32): 7945 - 7953. [Abstract] [Full Text] [PDF]

				R. Scott, A. Ruiz, C. Henneberger, D. M. Kullmann, and D. A. Rusakov Analog Modulation of Mossy Fiber Transmission Is Uncoupled from Changes in Presynaptic Ca2+ J. Neurosci., July 30, 2008; 28(31): 7765 - 7773. [Abstract] [Full Text] [PDF]

				D. Jeon, I. Song, W. Guido, K. Kim, E. Kim, U. Oh, and H.-S. Shin Ablation of Ca2+ Channel {beta}3 Subunit Leads to Enhanced N-Methyl-D-aspartate Receptor-dependent Long Term Potentiation and Improved Long Term Memory J. Biol. Chem., May 2, 2008; 283(18): 12093 - 12101. [Abstract] [Full Text] [PDF]

				D. Lee, K.-H. Lee, W.-K. Ho, and S.-H. Lee Target Cell-Specific Involvement of Presynaptic Mitochondria in Post-Tetanic Potentiation at Hippocampal Mossy Fiber Synapses J. Neurosci., December 12, 2007; 27(50): 13603 - 13613. [Abstract] [Full Text] [PDF]

				N. Korogod, X. Lou, and R. Schneggenburger Posttetanic potentiation critically depends on an enhanced Ca2+ sensitivity of vesicle fusion mediated by presynaptic PKC PNAS, October 2, 2007; 104(40): 15923 - 15928. [Abstract] [Full Text] [PDF]

				I. A. Khasabova, C. L. Stucky, C. Harding-Rose, L. Eikmeier, A. J. Beitz, L. G. Coicou, A. E. Hanson, D. A. Simone, and V. S. Seybold Chemical Interactions between Fibrosarcoma Cancer Cells and Sensory Neurons Contribute to Cancer Pain J. Neurosci., September 19, 2007; 27(38): 10289 - 10298. [Abstract] [Full Text] [PDF]

				J.-M. Liao, C.-H. Yang, C.-L. Cheng, S.-F. Pan, M.-J. Chen, P.-C. Huang, G.-D. Chen, K.-C. Tung, H.-Y. Peng, and T.-B. Lin Spinal glutamatergic NMDA-dependent cyclic pelvic nerve-to-external urethra sphincter reflex potentiation in anesthetized rats Am J Physiol Renal Physiol, September 1, 2007; 293(3): F790 - F800. [Abstract] [Full Text] [PDF]

				M. J. Fedchyshyn and L.-Y. Wang Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse J. Physiol., June 1, 2007; 581(2): 581 - 602. [Abstract] [Full Text] [PDF]

				R. L. P. Habets and J. G. G. Borst Dynamics of the readily releasable pool during post-tetanic potentiation in the rat calyx of Held synapse J. Physiol., June 1, 2007; 581(2): 467 - 478. [Abstract] [Full Text] [PDF]

				T. P. Jensen, A. G. Filoteo, T. Knopfel, and R. M. Empson Presynaptic plasma membrane Ca2+ ATPase isoform 2a regulates excitatory synaptic transmission in rat hippocampal CA3 J. Physiol., February 15, 2007; 579(1): 85 - 99. [Abstract] [Full Text] [PDF]

				H. F. Altimimi and P. P. M. Schnetkamp Na+-dependent Inactivation of the Retinal Cone/Brain Na+/Ca2+-K+ Exchanger NCKX2 J. Biol. Chem., February 9, 2007; 282(6): 3720 - 3729. [Abstract] [Full Text] [PDF]

				V. Matveev, R. Bertram, and A. Sherman Residual Bound Ca2+ Can Account for the Effects of Ca2+ Buffers on Synaptic Facilitation J Neurophysiol, December 1, 2006; 96(6): 3389 - 3397. [Abstract] [Full Text] [PDF]

				V. A. Klyachko and C. F. Stevens Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses. J. Neurosci., June 28, 2006; 26(26): 6945 - 6957. [Abstract] [Full Text] [PDF]

				R. Scott and D. A. Rusakov Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J. Neurosci., June 28, 2006; 26(26): 7071 - 7081. [Abstract] [Full Text] [PDF]

				M. Trevino and R. Gutierrez The GABAergic projection of the dentate gyrus to hippocampal area CA3 of the rat: pre- and postsynaptic actions after seizures J. Physiol., September 15, 2005; 567(3): 939 - 949. [Abstract] [Full Text] [PDF]

				M.-H. Kim, N. Korogod, R. Schneggenburger, W.-K. Ho, and S.-H. Lee Interplay between Na+/Ca2+ Exchangers and Mitochondria in Ca2+ Clearance at the Calyx of Held J. Neurosci., June 29, 2005; 25(26): 6057 - 6065. [Abstract] [Full Text] [PDF]

				S. Ge and J. A. Dani Nicotinic Acetylcholine Receptors at Glutamate Synapses Facilitate Long-Term Depression or Potentiation J. Neurosci., June 29, 2005; 25(26): 6084 - 6091. [Abstract] [Full Text] [PDF]

				N. Korogod, X. Lou, and R. Schneggenburger Presynaptic Ca2+ Requirements and Developmental Regulation of Posttetanic Potentiation at the Calyx of Held J. Neurosci., May 25, 2005; 25(21): 5127 - 5137. [Abstract] [Full Text] [PDF]

				M. Kukley, M. Schwan, B. B. Fredholm, and D. Dietrich The Role of Extracellular Adenosine in Regulating Mossy Fiber Synaptic Plasticity J. Neurosci., March 16, 2005; 25(11): 2832 - 2837. [Abstract] [Full Text] [PDF]

				J. M. Kalkstein and K. L. Magleby Augmentation Increases Vesicular Release Probability in the Presence of Masking Depression at the Frog Neuromuscular Junction J. Neurosci., December 15, 2004; 24(50): 11391 - 11403. [Abstract] [Full Text] [PDF]

				J. Breustedt and D. Schmitz Assessing the Role of GLUK5 and GLUK6 at Hippocampal Mossy Fiber Synapses J. Neurosci., November 10, 2004; 24(45): 10093 - 10098. [Abstract] [Full Text] [PDF]

				M. Kukley, P. Stausberg, G. Adelmann, I. P. Chessell, and D. Dietrich Ecto-Nucleotidases and Nucleoside Transporters Mediate Activation of Adenosine Receptors on Hippocampal Mossy Fibers by P2X7 Receptor Agonist 2'-3'-O-(4-Benzoylbenzoyl)-ATP J. Neurosci., August 11, 2004; 24(32): 7128 - 7139. [Abstract] [Full Text] [PDF]

				M. Beierlein, K. R. Gee, V. V. Martin, and W. G. Regehr Presynaptic Calcium Measurements at Physiological Temperatures Using a New Class of Dextran-Conjugated Indicators J Neurophysiol, July 1, 2004; 92(1): 591 - 599. [Abstract] [Full Text] [PDF]

				B. Granseth and S. Lindstrom Augmentation of corticogeniculate EPSCs in principal cells of the dorsal lateral geniculate nucleus of the rat investigated in vitro J. Physiol., April 1, 2004; 556(1): 147 - 157. [Abstract] [Full Text] [PDF]

				H. J. Abel, J.C.F. Lee, J. C. Callaway, and R. C. Foehring Relationships Between Intracellular Calcium and Afterhyperpolarizations in Neocortical Pyramidal Neurons J Neurophysiol, January 1, 2004; 91(1): 324 - 335. [Abstract] [Full Text]

				K. A. Moore, R. A. Nicoll, and D. Schmitz Adenosine gates synaptic plasticity at hippocampal mossy fiber synapses PNAS, November 25, 2003; 100(24): 14397 - 14402. [Abstract] [Full Text] [PDF]

				E S L. Faber and P. Sah Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala J. Physiol., October 15, 2003; 552(2): 483 - 497. [Abstract] [Full Text] [PDF]

				J. Breustedt, K. E. Vogt, R. J. Miller, R. A. Nicoll, and D. Schmitz {alpha}1E-Containing Ca2+ channels are involved in synaptic plasticity PNAS, October 14, 2003; 100(21): 12450 - 12455. [Abstract] [Full Text] [PDF]

				M. B. Jackson and S. J. Redman Calcium Dynamics, Buffering, and Buffer Saturation in the Boutons of Dentate Granule-Cell Axons in the Hilus J. Neurosci., March 1, 2003; 23(5): 1612 - 1621. [Abstract] [Full Text] [PDF]

				A. I. Ivanov and R. L. Calabrese Modulation of Spike-Mediated Synaptic Transmission by Presynaptic Background Ca2+ in Leech Heart Interneurons J. Neurosci., February 15, 2003; 23(4): 1206 - 1218. [Abstract] [Full Text] [PDF]

				H. Kamiya, S. Ozawa, and T. Manabe Kainate Receptor-Dependent Short-Term Plasticity of Presynaptic Ca2+ Influx at the Hippocampal Mossy Fiber Synapses J. Neurosci., November 1, 2002; 22(21): 9237 - 9243. [Abstract] [Full Text] [PDF]

				J. N. Armstrong, T. B. Brust, R. G. Lewis, and B. A. MacVicar Activation of Presynaptic P2X7-Like Receptors Depresses Mossy Fiber-CA3 Synaptic Transmission through p38 Mitogen-Activated Protein Kinase J. Neurosci., July 15, 2002; 22(14): 5938 - 5945. [Abstract] [Full Text] [PDF]

				D. A. Henze, D. B. T. McMahon, K. M. Harris, and G. Barrionuevo Giant Miniature EPSCs at the Hippocampal Mossy Fiber to CA3 Pyramidal Cell Synapse Are Monoquantal J Neurophysiol, January 1, 2002; 87(1): 15 - 29. [Abstract] [Full Text] [PDF]

				J. Pamidimukkala and M. Hay Frequency dependence of endocytosis in aortic baroreceptor neurons and role of group III mGluRs Am J Physiol Heart Circ Physiol, July 1, 2001; 281(1): H387 - H395. [Abstract] [Full Text] [PDF]

				J. H. Schaffhausen, T. M. Fischer, and T. J. Carew Contirbution of Postsynaptic Ca2+ to the Induction of Posttetanic Potentiation in the Neural Circuit for Siphon Withdrawal in Aplysia J. Neurosci., March 1, 2001; 21(5): 1739 - 1749. [Abstract] [Full Text] [PDF]

				K. E. Vogt and W. G. Regehr Cholinergic Modulation of Excitatory Synaptic Transmission in the CA3 Area of the Hippocampus J. Neurosci., January 1, 2001; 21(1): 75 - 83. [Abstract] [Full Text] [PDF]

				Y. Komatsu and Y. Yoshimura Activity-Dependent Maintenance of Long-Term Potentiation at Visual Cortical Inhibitory Synapses J. Neurosci., October 15, 2000; 20(20): 7539 - 7546. [Abstract] [Full Text] [PDF]

				V. Brezina, P. J. Church, and K. R. Weiss Temporal Pattern Dependence of Neuronal Peptide Transmitter Release: Models and Experiments J. Neurosci., September 15, 2000; 20(18): 6760 - 6772. [Abstract] [Full Text] [PDF]

				M. Muschol and B. M. Salzberg Dependence of Transient and Residual Calcium Dynamics on Action-Potential Patterning during Neuropeptide Secretion J. Neurosci., September 15, 2000; 20(18): 6773 - 6780. [Abstract] [Full Text] [PDF]

				A. Vyshedskiy, T. Allana, and J.-W. Lin Analysis of Presynaptic Ca2+ Influx and Transmitter Release Kinetics during Facilitation at the Inhibitor of the Crayfish Neuromuscular Junction J. Neurosci., September 1, 2000; 20(17): 6326 - 6332. [Abstract] [Full Text] [PDF]

				C. L. Cox, W. Denk, D. W. Tank, and K. Svoboda Action potentials reliably invade axonal arbors of rat neocortical neurons PNAS, August 6, 2000; (2000) 170278697. [Abstract] [Full Text]

				C. M. Hempel, K. H. Hartman, X.-J. Wang, G. G. Turrigiano, and S. B. Nelson Multiple Forms of Short-Term Plasticity at Excitatory Synapses in Rat Medial Prefrontal Cortex J Neurophysiol, May 1, 2000; 83(5): 3031 - 3041. [Abstract] [Full Text] [PDF]

				I. V. Goussakov, K. Fink, C. E. Elger, and H. Beck Metaplasticity of Mossy Fiber Synaptic Transmission Involves Altered Release Probability J. Neurosci., May 1, 2000; 20(9): 3434 - 3441. [Abstract] [Full Text] [PDF]

				K. Narita, T. Akita, J. Hachisuka, S.-M. Huang, K. Ochi, and K. Kuba Functional Coupling of Ca2+ Channels to Ryanodine Receptors at Presynaptic Terminals: Amplification of Exocytosis and Plasticity J. Gen. Physiol., April 1, 2000; 115(4): 519 - 532. [Abstract] [Full Text] [PDF]

				M. B. Lips and B. U. Keller Activity-Related Calcium Dynamics in Motoneurons of the Nucleus Hypoglossus From Mouse J Neurophysiol, December 1, 1999; 82(6): 2936 - 2946. [Abstract] [Full Text] [PDF]

				K. Jensen, M. S. Jensen, and J. D C Lambert Post-tetanic potentiation of GABAergic IPSCs in cultured rat hippocampal neurones J. Physiol., August 15, 1999; 519(1): 71 - 84. [Abstract] [Full Text] [PDF]

				O. M. Schluter, E. Schnell, M. Verhage, T. Tzonopoulos, R. A. Nicoll, R. Janz, R. C. Malenka, M. Geppert, and T. C. Sudhof Rabphilin Knock-Out Mice Reveal That Rabphilin Is Not Required for Rab3 Function in Regulating Neurotransmitter Release J. Neurosci., July 15, 1999; 19(14): 5834 - 5846. [Abstract] [Full Text] [PDF]

				X.-Y. Jiang and T. W. Abrams Use-Dependent Decline of Paired-Pulse Facilitation at Aplysia Sensory Neuron Synapses Suggests a Distinct Vesicle Pool or Release Mechanism J. Neurosci., December 15, 1998; 18(24): 10310 - 10319. [Abstract] [Full Text] [PDF]

				B. A. Armitage and S. A. Siegelbaum Presynaptic Induction and Expression of Homosynaptic Depression at Aplysia Sensorimotor Neuron Synapses J. Neurosci., November 1, 1998; 18(21): 8770 - 8779. [Abstract] [Full Text] [PDF]

				P. P. Atluri and W. G. Regehr Delayed Release of Neurotransmitter from Cerebellar Granule Cells J. Neurosci., October 15, 1998; 18(20): 8214 - 8227. [Abstract] [Full Text] [PDF]

				K. A. Radcliffe and J. A. Dani Nicotinic Stimulation Produces Multiple Forms of Increased Glutamatergic Synaptic Transmission J. Neurosci., September 15, 1998; 18(18): 7075 - 7083. [Abstract] [Full Text] [PDF]

				J. S. Dittman and W. G. Regehr Calcium Dependence and Recovery Kinetics of Presynaptic Depression at the Climbing Fiber to Purkinje Cell Synapse J. Neurosci., August 15, 1998; 18(16): 6147 - 6162. [Abstract] [Full Text] [PDF]

				D. Wang and L. Maler Differential roles of Ca2+/calmodulin-dependent kinases in posttetanic potentiation at input selective glutamatergic pathways PNAS, June 9, 1998; 95(12): 7133 - 7138. [Abstract] [Full Text] [PDF]

				E. C. Cooper, A. Milroy, Y. N. Jan, L. Y. Jan, and D. H. Lowenstein Presynaptic Localization of Kv1.4-Containing A-Type Potassium Channels Near Excitatory Synapses in the Hippocampus J. Neurosci., February 1, 1998; 18(3): 965 - 974. [Abstract] [Full Text] [PDF]

				J. A. Varela, K. Sen, J. Gibson, J. Fost, L. F. Abbott, and S. B. Nelson A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex J. Neurosci., October 15, 1997; 17(20): 7926 - 7940. [Abstract] [Full Text] [PDF]

				T. M. Fischer, R. S. Zucker, and T. J. Carew Activity-Dependent Potentiation of Synaptic Transmission From L30 Inhibitory Interneurons of Aplysia Depends on Residual Presynaptic Ca2+ But Not on Postsynaptic Ca2+ J Neurophysiol, October 1, 1997; 78(4): 2061 - 2071. [Abstract] [Full Text] [PDF]

				N. Lasser-Ross, W. N. Ross, and Y. Yarom Activity-Dependent [Ca2+]i Changes in Guinea Pig Vagal Motoneurons: Relationship to the Slow Afterhyperpolarization J Neurophysiol, August 1, 1997; 78(2): 825 - 834. [Abstract] [Full Text] [PDF]

				A. Vyshedskiy and J.-W. Lin Activation and Detection of Facilitation as Studied by Presynaptic Voltage Control at the Inhibitor of the Crayfish Opener Muscle J Neurophysiol, May 1, 1997; 77(5): 2300 - 2315. [Abstract] [Full Text] [PDF]

				P. A. Salin, M. Scanziani, R. C. Malenka, and R. A. Nicoll Distinct short-term plasticity at two excitatory synapses in the hippocampus PNAS, November 12, 1996; 93(23): 13304 - 13309. [Abstract] [Full Text] [PDF]

				P. P. Atluri and W. G. Regehr Determinants of the Time Course of Facilitation at the Granule Cell to Purkinje Cell Synapse J. Neurosci., September 15, 1996; 16(18): 5661 - 5671. [Abstract] [Full Text] [PDF]

				D. D. Cummings, K. S. Wilcox, and M. A. Dichter Calcium-Dependent Paired-Pulse Facilitation of Miniature EPSC Frequency Accompanies Depression of EPSCs at Hippocampal Synapses in Culture J. Neurosci., September 1, 1996; 16(17): 5312 - 5323. [Abstract] [Full Text] [PDF]

				N. N. Urban and G. Barrionuevo Induction of Hebbian and Non-Hebbian Mossy Fiber Long-Term Potentiation by Distinct Patterns of High-Frequency Stimulation J. Neurosci., July 1, 1996; 16(13): 4293 - 4299. [Abstract] [Full Text] [PDF]

				B G Frenguelli and R Malinow Fluctuations in intracellular calcium responses to action potentials in single en passage presynaptic boutons of layer V neurons in neocortical slices. Learn. Mem., January 1, 1996; 3(2-3): 150 - 159. [Abstract] [PDF]

				M. Weisskopf, P. Castillo, R. Zalutsky, and R. Nicoll Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP Science, September 23, 1994; 265(5180): 1878 - 1882. [Abstract] [PDF]

				D. Schmitz, J. Mellor, and R. A. Nicoll Presynaptic Kainate Receptor Mediation of Frequency Facilitation at Hippocampal Mossy Fiber Synapses Science, March 9, 2001; 291(5510): 1972 - 1976. [Abstract] [Full Text]

				C. L. Cox, W. Denk, D. W. Tank, and K. Svoboda From the Cover: Action potentials reliably invade axonal arbors of rat neocortical neurons PNAS, August 15, 2000; 97(17): 9724 - 9728. [Abstract] [Full Text] [PDF]

				J. A. D. Sanchez and M. D. Kirk Short-Term Synaptic Enhancement Modulates Ingestion Motor Programs of Aplysia J. Neurosci., July 15, 2000; 20(14): RC85 - RC85. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help