Sodium currents in medullary neurons isolated from the pre-Bötzinger complex region

Journal of Neuroscience

Volumn 25, Issue 21, 2005, Pages 5159-5170

  Ptak, Krzysztof ^a,b   Zummo, Greer G ^a   Alheid, George F ^a   Tkatch, Tatiana ^a   Surmeier, D James ^a   McCrimmon, Donald R ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

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

Author keywords

Central pattern generator; Pacemaker; Persistent current; Pre B tzinger; Respiration; Riluzole; Sodium channels

Indexed keywords

RILUZOLE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; HODGKIN HUXLEY EQUATION; INTERNEURON; MEDULLA OBLONGATA; MEMBRANE DEPOLARIZATION; NERVE CELL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM CURRENT; STEADY STATE; VOLTAGE CLAMP;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, NORTHERN; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; MEMBRANE POTENTIALS; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RILUZOLE; RNA, MESSENGER; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; STILBAMIDINES; TETRODOTOXIN;

EID: 19444384305     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4238-04.2005     Document Type: Article

References (70)

1. Afshari FS, Ptak K, Khaliq ZM, Grieco TM, Slater NT, McCrimmon DR, Raman IM (2004) Resurgent Na currents in four classes of neurons of the cerebellum. J Neurophysiol 92:2831-2843.
2. Alheid GF, Gray PA, Jiang M, Feldman JL, McCrimmon DR (2002) Parvalbumin in respiratory neurons of the ventrolateral medulla of the adult rat. J Neurocytol 31:693-717.
3. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342:175-177.
4. + current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci 13:660-673.
5. Ambalavanar R, Morris R (1989) Fluoro-gold injected either subcutaneously or intravascularly results in extensive retrograde labelling of CNS neurones having axons terminating outside the blood-brain barrier. Brain Res 505:171-175.
6. Bean BP, Cohen CJ, Tsien RW (1983) Lidocaine block of cardiac sodium channels. J Gen Physiol 81:613-642.
7. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-8503.
8. Benoit E, Escande D (1991) Riluzole specifically blocks inactivated Na channels in myelinated nerve fibre. Pflügers Arch 419:603-609.
9. Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829-4843.
10. Butera Jr RJ, Rinzel J, Smith JC (1999a) Models of respiratory rhythm generation in the preBötzinger complex. I. Bursting pacemaker neurons. J Neurophysiol 82:382-397.
11. Butera Jr RJ, Rinzel J, Smith JC (1999b) Models of respiratory rhythm generation in the preBötzinger complex. II. Populations of coupled pacemaker neurons. J Neurophysiol 82:398-415.
12. Carr DB, Cooper DC, Ulrich SL, Spruston N, Surmeier DJ (2002) Serotonin receptor activation inhibits sodium current and dendritic excitability in prefrontal cortex via a protein kinase C-dependent mechanism. J Neurosci 22:6846-6855.
13. Carr DB, Day M, Cantrell AR, Held J, Scheuer T, Catterall WA, Surmeier DJ (2003) Transmitter modulation of slow, activity-dependent alternations in sodium channel availability endows neurons with a novel form of cellular plasticity. Neuron 39:793-806.
14. Dargent B, Paillart C, Carlier E, Alcaraz G, Martin-Eauclaire MF, Couraud F (1994) Sodium channel internalization in developing neurons. Neuron 13:683-690.
15. Del Negro CA, Koshiya N, Butera Jr RJ, Smith JC (2002a) Persistent sodium current, membrane properties and bursting behavior of preBötzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250.
16. Del Negro CA, Morgado-Valle C, Feldman JL (2002b) Respiratory rhythm: an emergent network property? Neuron 34:821-830.
17. Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL (2005) Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25:446-453.
18. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120.
19. Donahue LM, Coates W, Lee VH, Ippensen DC, Arze SE, Poduslo SE (2000) The cardiac sodium channel mRNA is expressed in the developing and adult rat and human brain. Brain Res 887:335-343.
20. Feldman JL, McCrimmon DR (2003) Neural control of breathing. In: Fundamental neuroscience, Chap 37, Ed 2 (Squire LR, Bloom FE, Roberts JL, Zigmond MJ, McConnell SK, Spitzer NC, eds), pp 967-990. New York: Academic.
21. Feldman JL, Mitchell GS, Nattie EE (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26:239-266.
22. Fleidervish IA, Gutnick MJ (1996) Kinetics of slow inactivation of persistent sodium current in layer V neurons of mouse neocortical slices. J Neurophysiol 76:2125-2130.
23. French CR, Sah P, Buckett KJ, Gage PW (1990) A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95:1139-1157.
24. Goldin AL (2001) Resurgence of sodium channel research. Annu Rev Physiol 63:871-894.
25. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL (1999) Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286:1566-1568.
26. Gray PA, Janczewski WA, Mellen N, McCrimmon DR, Feldman JL (2001) Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 4:927-930.
27. Hartmann HA, Colom LV, Sutherland ML, Noebels JL (1999) Selective localization of cardiac SCN5A sodium channels in limbic regions of rat brain. Nat Neurosci 2:593-595.
28. Hebert T, Drapeau P, Pradier L, Dunn RJ (1994) Block of the rat brain IIA sodium channel α-subunit by the neuroprotective drug riluzole. Mol Pharmacol 45:1055-1060.
29. Henze DA, Buzsáki G (2001) Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity. Neuroscience 105:121-130.
30. Hille B (1977) Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor interaction. J Gen Physiol 69:497-515.
31. 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.
32. + conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol 59:778-795.
33. Johnson SM, Smith JC, Funk GD, Feldman JL (1994) Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat. J Neurophysiol 72:2598-2608.
34. Kay AR, Sugimori M, Llinàs R (1998) Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J Neurophysiol 80:1167-1179.
35. Koshiya N, Smith JC (1999) Neuronal pacemaker for breathing visualized in vitro. Nature 400:360-363.
36. Kuo CC, Bean BP (1994) Slow binding of phenytoin to inactivated sodium channels in rat hippocampal neurons. Mol Pharmacol 46:716-725.
37. Lee RH, Heckman CJ (2000) Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20:6734-6740.
38. Magistretti J, Alonso A (1999) Biophysical properties and slow voltage-dependent inactivation of a sustained sodium current in entorhinal cortex layer-II principal neurons: a whole-cell and single-channel study. J Gen Physiol 114:491-509.
39. 5 dopamine receptor activation differentially modulates rapidly inactivating and persistent sodium currents in prefrontal cortex pyramidal neurons. J Neurosci 21:2268-2277.
40. McCrimmon DR, Monnier A, Ptak K, Zummo G, Zhang Z, Alheid GF (2001) Respiratory rhythm generation: preBötzinger neuron discharge patterns and persistent sodium current. Adv Exp Med Biol 499:147-152.
41. Monnier A, Alheid GF, McCrimmon DR (2003) Defining ventral medullary respiratory compartments with a glutamate receptor agonist in the rat. J Physiol (Lond) 548:859-874.
42. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
43. Pape HC, Driesang RB (1998) Ionic mechanisms of intrinsic oscillations in neurons of the basolateral amygdaloid complex. J Neurophysiol 79:217-226.
44. Parri HR, Crunelli V (1998) Sodium current in rat and cat thalamocortical neurons: role of a non-inactivating component in tonic and burst firing. J Neurosci 18:854-867.
45. Ptak K, Alheid GF, Jiang M, Surmeier DJ, McCrimmon DR (2001a) Characterization of persistent sodium current in a subset of pre-Bötzinger complex neurons. Soc Neurosci Abstr 27:633.9.
46. Ptak K, Zummo G, Alheid GF, McCrimmon DR (2001b) Presence of persistent sodium currents in the pre-Bötzinger neurons. FASEB J 15:A425.
47. Ptak K, Zummo G, Alheid GF, Surmeier DJ, McCrimmon DR (2002) Biophysical and molecular proprieties of persistent sodium current in pre-Bötzinger complex respiratory neurons. Soc Neurosci Abstr 28:221.8.
48. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
49. Raman IM, Sprunger LK, Meisler MH, Bean BP (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19:881-891.
50. Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004-9016.
51. Ramirez JM, Schwarzacher SW, Pierrefiche O, Olivera BM, Richter DW (1998) Selective lesioning of the cat pre-Bötzinger complex in vivo eliminates breathing but not gasping. J Physiol (Lond) 507:895-907.
52. Relding JC, Feldman JL (1998) PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60:385-405.
53. Rybak IA, Ptak K, Shevtsova NA, McCrimmon DR (2003) Sodium currents in neurons from the rostroventrolateral medulla of the rat. J Neurophysiol 90:1635-1642.
54. Sah P, Gibb AJ, Gage PW (1988) The sodium current underlying action potentials in guinea pig hippocampal CA1 neurons. J Gen Physiol 91:373-398.
55. Schwindt PC, Crill WE (1995) Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74:2220-2224.
56. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL (1991) PreBötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726-729.
57. Smith JC, Butera RJ, Koshiya N, Del Negro C, Wilson CG, Johnson SM (2000) Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model. Respir Physiol 122:131-147.
58. Smith MR, Smith RD, Plummer NW, Meisler MH, Goldin AL (1998) Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18:6093-6102.
59. Solomon IC, Edelman NH, Neubauer JA (1999) Patterns of phrenic motor output evoked by chemical stimulation of neurons located in the pre-Bötzinger complex in vivo. J Neurophysiol 81:1150-1161.
60. Song JH, Huang CS, Nagata K, Yeh JZ, Narahashi T (1997) Differential action of riluzole on tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels J Pharmacol Exp Ther 282:707-714.
61. St. John WM, Paton JF (2000) Characterizations of eupnea, apneusis and gasping in a perfused rat preparation. Respir Physiol 123:201-213.
62. A or glycine receptors. Respir Physiol Neurobiol 132:265-277.
63. Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15:1065-1076.
64. Taddese A, Bean BP (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33:587-600.
65. Thoby-Brisson M, Ramirez JM (2001) Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice. J Neurophysiol 86:104-112.
66. Tukey JW (1977) Exploratory data analysis. Menlo Park, CA: Addison-Wesley.
67. Urbani A, Belluzzi O (2000) Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 12:3567-3574.
68. Vega-Saenz de Miera EC, Rudy B, Sugimori M, Llinàs R (1997) Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc Natl Acad Sci USA 94:7059-7064.
69. Wang H, Germanson TP, Guyenet PG (2002) Depressor and tachypneic responses to chemical stimulation of the ventral respiratory group are reduced by ablation of neurokinin-1 receptor-expressing neurons. J Neurosci 22:3755-3764.
70. Wessendorf MW (1991) Fluoro-gold: composition, and mechanism of uptake. Brain Res 553:135-148.