Presynaptic action potential waveform determines cortical synaptic latency

Journal of Physiology

Volumn 589, Issue 5, 2011, Pages 1117-1131

  Boudkkazi, Sami ^a,b   Fronzaroli Molinieres, Laure ^a,b   Debanne, Dominique ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOPYRIDINE; CALCIUM ION; DENDROTOXIN; TETRODOTOXIN; TETRYLAMMONIUM; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CALCIUM CURRENT; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; HIPPOCAMPAL CA3 REGION; NEOCORTEX; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE FIBER; NEUROMODULATION; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SPIKE WAVE; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; WAVEFORM;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; HIPPOCAMPUS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, WISTAR; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SYNAPSES; SYNAPTIC TRANSMISSION; TETRAETHYLAMMONIUM;

EID: 79951992643     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.199653     Document Type: Article

References (51)

1. Angulo MC, Staiger JF, Rossier J & Audinat E (1999). Developmental synaptic changes increase the range of integrative capabilities of an identified excitatory neocortical connection. J Neurosci 19, 1566-1576.
2. Augustine GJ, Charlton MP & Smith SJ (1985). Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J Physiol 369, 163-181.
3. 2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22, 10593-10602.
4. Boudkkazi S, Carlier E, Ankri N, Caillard O, Giraud P, Fronzaroli-Molinieres L & Debanne D (2007). Release-dependent variations in synaptic latency: a putative code for short- and long-term synaptic dynamics. Neuron 56, 1048-1060.
5. + channels: an unexpected form of cellular plasticity. Nat Rev Neurosci 2, 397-407.
6. Carlier E, Sourdet V, Boudkkazi S, Déglise P, Ankri N, Fronzaroli-Molinieres L & Debanne D (2006). Metabotropic glutamate receptor subtype 1 regulates sodium currents in rat neocortical pyramidal neurons. J Physiol 577, 141-154.
7. Cudmore RH, Fronzaroli-Molinieres L, Giraud P & Debanne D (2010). Spike-time precision and network synchrony are controlled by the homeostatic regulation of the D-type potassium current. J Neurosci 30, 12885-12895.
8. Debanne D, Boudkkazi S, Campanac E, Cudmore R, Giraud P, Fronzaroli-Molinieres L, Carlier E & Caillard O (2008). Paired-recordings from synaptically-coupled cortical and hippocampal neurons in acute and cultured brain slices. Nat Protoc 3, 1559-1568.
9. Debanne D, Guérineau NC, Gähwiler BH & Thompson SM (1996). Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 491, 163-176.
10. + conductance in hippocampus. Nature 389, 286-289.
11. + channel. J Neurosci 24, 1236-1244.
12. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
13. + channel subunit Kv2.1. J Physiol 522, 19-31.
14. + channels in hippocampal mossy fiber boutons. Neuron 28, 927-939.
15. + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58, 387-400.
16. Grosse G, Draguhn A, Höhne L, Tapp R, Veh RW & Ahnert-Hilger G (2000). Expression of Kv1 potassium channels in mouse hippocampal primary cultures: development and activity-dependent regulation. J Neurosci 20, 1869-1882.
17. Inda MC, DeFelipe J & Muñoz A (2006). Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci U S A 103, 2920-2925.
18. Katz B & Miledi R (1967). A study of synaptic transmission in the absence of nerve impulses. J Physiol 192, 407-436.
19. Kole MHP, Letzkus JJ & Stuart GJ (2007). Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55, 633-647.
20. Lancaster B & Nicoll RA (1987). Properties of two calcium-activated hyperpolarizations in rat hippocampal neurons. J Physiol 389, 187-203.
21. Lin JW & Faber DS (2002). Modulation of synaptic delay during synaptic plasticity. Trends Neurosci 25, 449-455.
22. Llinas R, Steinberg IZ & Walton K (1981). Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys J 33, 323-352.
23. Lorincz A & Nusser Z (2008). Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28, 14329-14340.
24. Manor Y, Koch C & Segev I (1991). Effect of geometrical irregularities on propagation delay in axonal trees. Biophys J 60, 1424-1437.
25. 2+ channels in hippocampal neurons. Nature 395, 900-905.
26. Meeks JP, Jiang X & Mennerick S (2005). Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus. J Physiol 566, 425-441.
27. Mitterdorfer J & Bean BP (2002). Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 22, 10106-10115.
28. + current in rat hippocampal neurons. J Neurosci 19, 1728-1735.
29. Nicoll RA & Schmitz D (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6, 863-876.
30. Palmer LM & Stuart GJ (2006). Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26, 1854-1863.
31. Raab-Graham KF, Haddick PCG, Jan YN & Jan LY (2006). Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation to dendrites. Science 314, 144-148.
32. Reyes A & Sakmann B (1999). Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 19, 3827-3835.
33. Rieke F, Warland D, de Ruyter van Steveninck R & Bialek W (1997). Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA, USA.
34. Sabatini BL & Regehr WG (1996). Timing of neurotransmission at fast synapses in the mammalian brain. Nature 384, 170-172.
35. Sabatini BL & Regehr WG (1997). Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J Neurosci 17, 3425-3435.
36. Sabatini BL & Regehr WG (1999). Timing of synaptic transmission. Annu Rev Physiol 61, 521-542.
37. Saez I & Friedlander MJ (2009). Synaptic output of individual layer 4 neurons in guinea pig visual cortex. J Neurosci 29, 4930-4944.
38. 2+ modulates coding at CA3-CA3 synapses in the rat hippocampus. J Physiol 552, 513-524.
39. Scott LL, Hage TA & Golding NL (2007). Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive. J Physiol 583, 647-661.
40. Segev I (1990). Computer study of presynaptic inhibition controlling the spread of action potentials into axonal terminals. J Neurophysiol 63, 987-998.
41. Shah MM, Migliore M, Valencia I, Cooper EC & Brown DA (2008). Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 105, 7869-7874.
42. + channels detected in vivo. Nature 365, 72-75.
43. Shu Y, Hasenstaub A, Duque A, Yu Y & McCormick DA (2006). Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441, 761-765.
44. + current. Proc Natl Acad Sci U S A 104, 11453-11458.
45. Stoppini L, Buchs PA & Müller D (1991). A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37, 173-182.
46. Storm JF (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385, 733-759.
47. Storm JF (1990). Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83, 161-187.
48. Stühmer W, Ruppersberg JP, Schröter KH, Sakmann B, Stocker M, Giese KP, Perschke A, Baumann A & Pongs O (1989). Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J 8, 3235-3244.
49. Taschenberger H & von Gersdorff H (2000). Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20, 9162-9173.
50. Veh RW, Lichtinghagen R, Sewing S, Wunder F, Grumbach IM & Pongs O (1995). Immunohistochemical localization of five members of the Kv1 channel subunits: contrasting subcellular locations and neuron-specific co-localizations in rat brain. Eur J Neurosci 7, 2189-2205.
51. Vervaeke K, Gu N, Agdestein C, Hu H & Storm JF (2006). Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release. J Physiol 576, 235-256.