Kinetic properties and functional dynamics of sodium channels during repetitive spiking in a slow pacemaker neuron

Journal of Neuroscience

Volumn 30, Issue 36, 2010, Pages 12113-12127

  Milescu, Lorin S ^a,b   Yamanishi, Tadashi ^b   Ptak, Krzysztof ^b   Smith, Jeffrey C ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CADMIUM CHLORIDE; TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL; AMINO ACID RECEPTOR BLOCKING AGENT; SODIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHANNEL GATING; CONTROLLED STUDY; FEMALE; KINETICS; MALE; NEWBORN; NONHUMAN; PACEMAKER NERVE CELL; PATCH CLAMP; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; RAPHE NUCLEUS; RAT; SODIUM CURRENT; SPIKE WAVE; SUBTHRESHOLD SODIUM CURRENT; SUPRATHRESHOLD SODIUM CURRENT; VALIDATION PROCESS; VOLTAGE CLAMP; WHOLE CELL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; BIOPHYSICS; CYTOLOGY; DRUG EFFECTS; IN VITRO STUDY; NERVE CELL; NONLINEAR SYSTEM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROBABILITY; PROCEDURES; SPRAGUE DAWLEY RAT; TIME;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; BIOPHYSICAL PROCESSES; CADMIUM CHLORIDE; EXCITATORY AMINO ACID ANTAGONISTS; MODELS, NEUROLOGICAL; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; PROBABILITY; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; TETRODOTOXIN; TIME FACTORS; IN VITRO TECHNIQUES;

EID: 77956594956     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0445-10.2010     Document Type: Article

References (49)

1. Alzheimer C, Schwindt PC, Crill WE (1993) Modal gating of Na+ channels as a mechanism of persistent Na+current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci 13:660-673. (Pubitemid 23045149)
2. Armstrong CM (2006) Na channel inactivation from open and closed states. Proc Natl Acad Sci U S A 103:17991-17996.
3. Bean BP (1981) Sodium channel inactivation in the crayfish giant axon: must channels open before inactivating? Biophys J 35:595-614.
4. Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451-465.
5. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-8503.
6. Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555-592. (Pubitemid 30164943)
7. Blair NT, Bean BP (2003) Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23:10338-10350.
8. Brown AM, Schwindt PC, Crill WE (1994) Different voltage dependence of transient and persistent Na+ currents is compatible with modal-gating hypothesis for sodium channels. J Neurophysiol 71:2562-2565.
9. Carter BC, Bean BP (2009) Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast-spiking neurons. Neuron 64:898-909.
10. Catterall WA, Dib-Hajj S, Meisler MH, Pietrobon D (2008) Inherited neuronal ion channelopathies: new windows on complex neurological diseases. J Neurosci 28:11768-11777.
11. + channel fast inactivation. Neuron 22:73-87.
12. Colquhoun D, Hawkes AG (1995) A Q-matrix cookbook: how to write only one program to calculate the single-channel and macroscopic predictions for any kinetic mechanism. In: Single channel recording, Ed 2 (Sakmann B, Neher E, eds), pp 589-636. New York: Plenum.
13. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC (2002) Persistent sodium current, membrane properties and bursting behavior of pre-Bötzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250.
14. Delcour AH, Lipscombe D, Tsien RW (1993) Multiple modes of N-type calcium channel activity distinguished by differences in gating kinetics. J Neurosci 13:181-194.
15. Fellin T, Luvisetto S, Spagnolo M, Pietrobon D (2004) Modal gating of human CaV2.1 (P/Q-type) calcium channels: II. The b mode and reversible uncoupling of inactivation. J Gen Physiol 124:136-174.
16. Fleidervish IA, Friedman A, Gutnick MJ (1996) Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol 493:83-97. (Pubitemid 26152612)
17. Fletcher R, Powell MJD (1963) A rapidly convergent descent method for minimization. Computing J 2:163-168.
18. Goldfarb M, Schoorlemmer J, Williams A, Diwakar S, Wang Q, Huang X, Giza J, Tchetchik D, Kelley K, Vega A, Matthews G, Rossi P, Ornitz DM, D'Angelo E (2007) Fibroblast growth factor homologous factors control neuronal excitability through modulation of voltage-gated sodium channels. Neuron 55:449-463.
19. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol Lond 117:500-544.
20. Horn R, Vandenberg CA (1984) Statistical properties of single sodium channels. J Gen Physiol 84:505-534. (Pubitemid 15203550)
21. Irvine LA, Jafri MS, Winslow RL (1999) Cardiac sodium channel Markov model with temperature dependence and recovery from inactivation. Biophys J 76:1868-1885.
22. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
23. Khaliq ZM, Bean BP (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltage-dependent sodium conductances. J Neurosci 30:7401-7413.
24. Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-4912.
25. + channels during depolarization in guinea-pig cardiac cells. Pflugers Arch 416:493-500.
26. Koshiya N, Smith JC (1999) Neuronal pacemaker for breathing visualized in vitro. Nature 400:360-363. (Pubitemid 29344200)
27. Kuo CC, Bean BP (1994) Na+ channels must deactivate to recover from inactivation. Neuron 12:819-829.
28. Legendre P, Westbrook GL (1991) Ifenprodil blocks N-methyl-D-aspartate receptors by a two-component mechanism. Mol Pharmacol 40:289-298.
29. Luvisetto S, Fellin T, Spagnolo M, Hivert B, Brust PF, Harpold MM, Stauderman KA, Williams ME, Pietrobon D (2004) Modal gating of human CaV2.1 (P/Q-type) calcium channels: I. The slow and the fast gating modes and their modulation by beta subunits. J Gen Physiol 124: 445-461.
30. Menon V, Spruston N, Kath WL (2009) A state-mutating genetic algorithm to design ion-channel models. Proc Natl Acad Sci U S A 106:16829-16834.
31. Michaelevski I, Chikvashvili D, Tsuk S, Singer-Lahat D, Kang Y, Linial M, Gaisano HY, Fili O, Lotan I (2003) Direct interaction of target SNAREs with the Kv2.1 channel. Modal regulation of channel activation and inactivation gating. J Biol Chem 278:34320-34330.
32. Mickus T, Jung H, Spruston N (1999) Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys J 76:846-860.
33. Milescu LS, Akk G, Sachs F (2005) Maximum likelihood estimation of ion channel kinetics from macroscopic currents. Biophys J 88:2494-2515. (Pubitemid 40976119)
34. Milescu LS, Yamanishi T, Ptak K, Mogri MZ, Smith JC (2008) Real-time kinetic modeling of voltage-gated ion channels using dynamic clamp. Biophys J 95:66-87.
35. Milescu LS, Bean BP, Smith JC (2010) Isolation of somatic Na+currents by selective inactivation of axonal channels with a voltage prepulse. J Neurosci 30:7740-7748.
36. Nilius B, Benndorf K, Markwardt F, Franke T (1987) Modulation of single cardiac sodium channels by DPI 201-106. Gen Physiol Biophys 6:409-424.
37. Patlak J (1991) Molecular kinetics of voltage-dependent Na+ channels. Physiol Rev 71:1047-1080.
38. Popescu G, Auerbach A (2003) Modal gating of NMDA receptors and the shape of their synaptic response. Nat Neurosci 6:476-483.
39. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical recipes in C: the art of scientific computing, Ed 2. New York: Cambridge UP.
40. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB, Smith JC (2009) Raphé neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29:3720-3737.
41. Rall W, Segev I (1985) Space-clamp problems when voltage clamping branched neurons with intracellular microelectrodes. In: Voltage and patch-clamping with microelectrodes (Smith TG Jr, Lecar H, Redman SJ, eds), pp 191-215. Bethesda, MD: American Physiological Society.
42. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80:729-737.
43. Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) Dynamic clampcomputer- generated conductances in real neurons. J Neurophysiol 69: 992-995. (Pubitemid 23102967)
44. Swensen AM, Bean BP (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23:9650-9663.
45. Taddese A, Bean BP (2002) Subthreshold sodium current from rapidly in-activating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33:587-600.
46. Vervaeke K, Hu H, Graham LJ, Storm JF (2006) Contrasting effects of the persistent Na+ current on neuronal excitability and spike timing. Neuron 49:257-270.
47. Williams SR, Stuart GJ (1999) Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521:467-482. (Pubitemid 30003926)
48. Yu Y, Shu Y, McCormick DA (2008) Cortical action potential backpropagation explains spike threshold variability and rapid-onset kinetics. J Neurosci 28:7260-7272.
49. Zhou JY, Potts JF, Trimmer JS, Agnew WS, Sigworth FJ (1991) Multiple gating modes and the effect of modulating factors on the microI sodium channel. Neuron 7:775-785.