Control and plasticity of the presynaptic action potential waveform at small CNS nerve terminals

Neuron

Volumn 84, Issue 4, 2014, Pages 778-789

  Hoppa, Michael B ^a   Gouzer, Geraldine ^a   Armbruster, Moritz ^a   Ryan, Timothy A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; POTASSIUM CHANNEL KV3.1; SHAKER POTASSIUM CHANNEL; SHAW POTASSIUM CHANNEL; UNCLASSIFIED DRUG; CALCIUM; POTASSIUM CHANNEL;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DENTATE GYRUS; EXOCYTOSIS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; NERVE CELL PLASTICITY; NERVE ENDING; NEUROMODULATION; NONHUMAN; PRESYNAPTIC POTENTIAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL NOISE RATIO; SPIKE WAVE; WAVEFORM; ACTION POTENTIAL; ANIMAL; HIPPOCAMPUS; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTOSOME;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS; HIPPOCAMPUS; NEURONAL PLASTICITY; NEURONS; POTASSIUM CHANNELS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84918826604     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.09.038     Document Type: Article

References (56)

1. Abdul-Ghani M.A., Valiante T.A., Pennefather P.S. Sr2+ and quantal events at excitatory synapses between mouse hippocampal neurons in culture. J.Physiol. 1996, 495:113-125.
2. Alle H., Roth A., Geiger J.R. Energy-efficient action potentials in hippocampal mossy fibers. Science 2009, 325:1405-1408.
3. Alle H., Kubota H., Geiger J.R. Sparse but highly efficient Kv3 outpace BKCa channels in action potential repolarization at hippocampal mossy fiber boutons. J.Neurosci. 2011, 31:8001-8012.
4. Ariel P., Ryan T.A. Optical mapping of release properties in synapses. Front Neural Circuits 2010, 4.
5. Ariel P., Hoppa M.B., Ryan T.A. Intrinsic variability in Pv, RRP size, Ca(2+) channel repertoire, and presynaptic potentiation in individual synaptic boutons. Front Synaptic Neurosci 2012, 4:9.
6. Augustine G.J., Charlton M.P., Smith S.J. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J.Physiol. 1985, 367:163-181.
7. Balaji J., Ryan T.A. Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc. Natl. Acad. Sci. USA 2007, 104:20576-20581.
8. Bean B.P. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 2007, 8:451-465.
9. Bischofberger J., Geiger J.R., Jonas P. Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J.Neurosci. 2002, 22:10593-10602.
10. Borst J.G., Sakmann B. Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J.Physiol. 1998, 506:143-157.
11. Borst J.G., Sakmann B. Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:347-355.
12. Boudkkazi S., Fronzaroli-Molinieres L., Debanne D. Presynaptic action potential waveform determines cortical synaptic latency. J.Physiol. 2011, 589:1117-1131.
13. Bradley J., Luo R., Otis T.S., DiGregorio D.A. Submillisecond optical reporting of membrane potential insitu using a neuronal tracer dye. J.Neurosci. 2009, 29:9197-9209.
14. Debanne D., Campanac E., Bialowas A., Carlier E., Alcaraz G. Axon physiology. Physiol. Rev. 2011, 91:555-602.
15. Deng P.Y., Rotman Z., Blundon J.A., Cho Y., Cui J., Cavalli V., Zakharenko S.S., Klyachko V.A. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 2013, 77:696-711.
16. Dodge F.A., Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J.Physiol. 1967, 193:419-432.
17. Engel D., Jonas P. Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron 2005, 45:405-417.
18. Forsythe I.D., Barnes-Davies M. The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc. Biol. Sci. 1993, 251:143-150.
19. Foust A.J., Yu Y., Popovic M., Zecevic D., McCormick D.A. Somatic membrane potential and Kv1 channels control spike repolarization in cortical axon collaterals and presynaptic boutons. J.Neurosci. 2011, 31:15490-15498.
20. Gong B., Liu M., Qi Z. Membrane potential dependent duration of action potentials in cultured rat hippocampal neurons. Cell. Mol. Neurobiol. 2008, 28:49-56.
21. Gong Y., Li J.Z., Schnitzer M.J. Enhanced Archaerhodopsin Fluorescent Protein Voltage Indicators. PLoS ONE 2013, 8:e66959.
22. Gutman G.A., Chandy K.G., Grissmer S., Lazdunski M., McKinnon D., Pardo L.A., Robertson G.A., Rudy B., Sanguinetti M.C., Stühmer W., Wang X. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol. Rev. 2005, 57:473-508.
23. Hille B. Ion channels of excitable membranes 2001, Sinauer, Sunderland, Mass., U.S.A. Third Edition.
24. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J.Physiol. 1952, 117:500-544.
25. Hoppa M.B., Lana B., Margas W., Dolphin A.C., Ryan T.A. α2δ expression sets presynaptic calcium channel abundance and release probability. Nature 2012, 486:122-125.
26. Hu H., Jonas P. A supercritical density of Na(+) channels ensures fast signaling in GABAergic interneuron axons. Nat. Neurosci. 2014, 17:686-693.
27. Johnston J., Forsythe I.D., Kopp-Scheinpflug C. Going native:voltage-gated potassium channels controlling neuronal excitability. J.Physiol. 2010, 588:3187-3200.
28. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J.Physiol. 1967, 192:407-436.
29. Kole M.H., Letzkus J.J., Stuart G.J. Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 2007, 55:633-647.
30. Kralj J.M., Douglass A.D., Hochbaum D.R., Maclaurin D., Cohen A.E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 2012, 9:90-95.
31. Leão R.M., Kushmerick C., Pinaud R., Renden R., Li G.L., Taschenberger H., Spirou G., Levinson S.R., von Gersdorff H. Presynaptic Na+ channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J.Neurosci. 2005, 25:3724-3738.
32. Li L., Bischofberger J., Jonas P. Differential gating and recruitment of P/Q-, N-, and R-type Ca2+ channels in hippocampal mossy fiber boutons. J.Neurosci. 2007, 27:13420-13429.
33. Llinás R., Steinberg I.Z., Walton K. Presynaptic calcium currents in squid giant synapse. Biophys. J. 1981, 33:289-321.
34. Maclaurin D., Venkatachalam V., Lee H., Cohen A.E. Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc. Natl. Acad. Sci. USA 2013, 110:5939-5944.
35. Maric D., Maric I., Smith S.V., Serafini R., Hu Q., Barker J.L. Potentiometric study of resting potential, contributing K+ channels and the onset of Na+ channel excitability in embryonic rat cortical cells. Eur. J. Neurosci. 1998, 10:2532-2546.
36. Meeks J.P., Jiang X., Mennerick S. Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus. J.Physiol. 2005, 566:425-441.
37. Meunier F.M. Relationship between presynaptic membrane potential and acetylcholine release in synaptosomes from Torpedo electric organ. J.Physiol. 1984, 354:121-137.
38. Mintz I.M., Sabatini B.L., Regehr W.G. Calcium control of transmitter release at a cerebellar synapse. Neuron 1995, 15:675-688.
39. Mitterdorfer J., Bean B.P. Potassium currents during the action potential of hippocampal CA3 neurons. J.Neurosci. 2002, 22:10106-10115.
40. + influx achieves homeostatic potentiation of neurotransmitter release. Curr. Biol. 2012, 22:1102-1108.
41. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
42. Podleski T., Changeux J.P. Effects associated with permeability changes caused by gramicidin A in electroplax membrane. Nature 1969, 221:541-545.
43. Popovic M.A., Foust A.J., McCormick D.A., Zecevic D. The spatio-temporal characteristics of action potential initiation in layer 5 pyramidal neurons: a voltage imaging study. J.Physiol. 2011, 589:4167-4187.
44. Pumplin D.W., Reese T.S., Llinás R. Are the presynaptic membrane particles the calcium channels?. Proc. Natl. Acad. Sci. USA 1981, 78:7210-7213.
45. Rowan M.J., Tranquil E., Christie J.M. Distinct Kv channel subtypes contribute to differences in spike signaling properties in the axon initial segment and presynaptic boutons of cerebellar interneurons. J.Neurosci. 2014, 34:6611-6623.
46. Sabatini B.L., Regehr W.G. Timing of neurotransmission at fast synapses in the mammalian brain. Nature 1996, 384:170-172.
47. Sabatini B.L., Regehr W.G. Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J.Neurosci. 1997, 17:3425-3435.
48. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 1992, 359:832-835.
49. Schneggenburger R., Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 2000, 406:889-893.
50. Scimemi A., Diamond J.S. The number and organization of Ca2+ channels in the active zone shapes neurotransmitter release from Schaffer collateral synapses. J.Neurosci. 2012, 32:18157-18176.
51. Smart S.L., Lopantsev V., Zhang C.L., Robbins C.A., Wang H., Chiu S.Y., Schwartzkroin P.A., Messing A., Tempel B.L. Deletion of the K(V)1.1 potassium channel causes epilepsy in mice. Neuron 1998, 20:809-819.
52. Storm J.F. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J.Physiol. 1987, 385:733-759.
53. Takahashi T., Momiyama A. Different types of calcium channels mediate central synaptic transmission. Nature 1993, 366:156-158.
54. Taschenberger H., von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J.Neurosci. 2000, 20:9162-9173.
55. Wheeler D.B., Randall A., Tsien R.W. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 1994, 264:107-111.
56. Xu M., Cao R., Xiao R., Zhu M.X., Gu C. The axon-dendrite targeting of Kv3 (Shaw) channels is determined by a targeting motif that associates with the T1 domain and ankyrin G. J.Neurosci. 2007, 27:14158-14170.