Background sodium current stabilizes bursting in respiratory pacemaker neurons

Journal of Neurobiology

Volumn 60, Issue 4, 2004, Pages 481-489

  Tryba, Andrew K ^a   Ramirez, Jan Marino ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Background current; Breathing; Endogenous bursting; Rhythm generation

Indexed keywords

SODIUM; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; BREATHING; CONTROLLED STUDY; DEPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NERVE CELL; NONHUMAN; PACEMAKER; PATCH CLAMP; PRIORITY JOURNAL; RHYTHM; SODIUM CURRENT;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; CELL MEMBRANE; MEDULLA OBLONGATA; MICE; NERVE NET; NEURONS; POTASSIUM; RESPIRATORY CENTER; RESPIRATORY PHYSIOLOGY; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 4243075317     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.20050     Document Type: Article

References (54)

1. Angstadt JD, Calabrese RL. 1989. A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J Neurosci 9:2846-2857.
2. Arbas ES, Calabrese RL. 1987. Slow oscillations of membrane potential in interneurons that control heartbeat in the medicinal leech. J Neurosci 12:3953-3960.
3. Boeckxstaens GE. 2002. Understanding and controlling the enteric nervous system Best Practice and Research. Clin Gastroenterol 16:1013-1023.
4. Cohen HC, Rosen KM, Pick A. 1975. Disorders of impulse conduction and impulse formation caused by hyperkalemia in man. Am Heart J 89:501-509.
5. Coulombe A, Lefevre IA, Baro I, Coraboeuf E. 1989. Barium- and calcium-permeable channels open at negative membrane potentials in rat ventricular myocytes. J Membr Biol 111:57-67.
6. Debarbieux F, Brunton J, Charpak S. 1998. Effect of bicuculline on thalamic activity: a direct blockade of IAHP in reticularis neurons. J Neurophysiol 79:2911-2918.
7. Del Negro CA, Johnson SM, Buter RJ, Smith JC. 2001. Models of respiratory rhythm generation in the pre-Bötzinger complex. III. Experimental tests of model predictions. J Neurophysiol 86:59-74.
8. Del Negro CA, Koshiya N, Butera RA 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.
9. DiFrancesco, D. 1993. Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55:455-472.
10. Do MTH, Bean BP. 2003. Subthreshold sodium currents and pacemaking in subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120.
11. Durroux T, Gallo-Payet N, Bilodeau L, Payet MD. 1992. Background calcium permeable channels in glomerulosa cells from adrenal gland. J Membr Biol 129:145-153.
12. Funk G, Smith JC, Feldman JL. 1994. Development of thyrotropin-releasing hormone and noreprinephrine potentiation of inspiratory-related hypoglossal motorneuron discharge in neonatal and juvenile mice in vitro. J Neurophysiol 72:2538-2541.
13. Goodman CS, Spitzer NC. 1981. The mature electrical properties of identified neurons: differentiation from neuroblast to neurone. Nature 280:208-214.
14. Grolleau F, Lapied B. 2000. Dorsal unpaired median neurons in the insect central nervous system: towards a better understanding of the ionic mechanisms underlying spontaneous electrical activity. J Exp Biol 203:1633-1648.
15. Haller M, Mironov SL, Karschin A, Richter DW. 2001. Dynamic activation of Katp channels in rhythmically active neurons. J Physiol 537:69-81.
16. Hansen AJ. 1985. Effects of anoxia on ion distribution in the brain. Physiol Rev 65:101-148.
17. Herlenius E, Lagercrantz H. 1999. Adenosinergic modulation of respiratory neurones in the neonatal rat brainstem in vitro. J Physiol 518:159-172.
18. Jinno S, Ishizuka S, Kosaka. 2003. Ionic currents underlying rhythmic bursting of ventral mossy cells in the developing mouse dentate gyrus. Eur J Neurosci 17:1338-1354.
19. Jensen MS, Azouz Y, Yaari Y. 1994. Variant firing patterns in rate hypocampal pyramidal cells modulated by extracellular potassium. J Neurophysiol 71:831-839.
20. Johnson SM, Koshiya N, Smith JC. 2001. Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Bötzinger complex "island." J Neurophysiol 85:1772-1776.
21. Johnson SW, Seutin V. 1997. Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents. Neurosci Lett 231:13-16.
22. Kiehn O, Kjaerulff O, Tresch MC, Harris-Warrick RM. 2000. Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53:649-659.
23. Koyano K, Tanaka K, Kuba K. 1992. A patch-clamp study of the muscarinic-sensitive potassium channel in bullfrog sympathetic ganglion cells. J Physiol (Lond) 454:231-246.
24. Lapied B, Stankiewicz M, Grolleau F, Rochat H, Zlotkin E, Pelhate M. 1999. Biophysical properties of scorpion α-toxin-sensitive background sodium channel contributing to the pacemaker activity in insect neurosecretory cells (DUM neurons). Eur J Neurosci 11:1449-1460.
25. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, et al. 2003. Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22:216-224.
26. McCormick DA, Pape H-C. 1990. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic neurons. J Physiol 431:291-318.
27. Miles GB, Parkis MA, Lipski J, Funk GD. 2002. Modulation of phrenic motoneuron excitability by ATP: consequences for respiratory-related output in vitro. J Appl Physiol 92:1899-1910.
28. + concentrations, extra- and intracellular voltages and the effect of TTX in hypoxic rat hippocampal slices. J Neurophysiol 83:735-745.
29. Nam SC, Hockberger PE. 1997. Analysis of spontaneous electrical activity in cerebellar Purkinje cells acutely isolated from postnatal rats. J Neurobiol 33:18-32.
30. Neher E. 1992. Correction for liquid junction potentials in patch clamp experiments. Methods Enzmol 207:123-131.
31. Newstead CG, Donaldson GC, Sneyd JR. 1990. Potassium as a respiratory signal in humans. J Appl Physiol 69:1799-1803.
32. Orkand RK. 1980. Extracellular potassium accumulation in the nervous system. FASEB J 39:1515-1518.
33. Paterson DJ, Dorrington KL, Bergel DH, Kerr G, Miall RC, Stein JF, Nye PC. 1992. Effect of potassium on ventilation in the rhesus monkey. Exp Physiol 77:217-220.
34. Pape H-C. 1996. Queer current and pacemaker: the hyperpolarization- activated cation current in neurons. Annul Rev Physiol 58:299-327.
35. Peña F, Ramirez JM. 2003. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064.
36. Poolos NP, Mauk MD, Kocsis JD. 1987. Activity-evoked increases in extracellular potassium modulate presynaptic excitability in the CA1 region of the hippocampus. J Neurophysiol 58:404-416.
37. Raman IM, Gustafson AE, Padgett D. 2000. Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004-9016.
38. Raman IM, Sprunger LK, Meisler MH, BP Bean. 1997. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19:881-891.
39. Ramirez JM, Telgkamp P, Elsen FP, Quellmalz UJA, Richter DW. 1997. Respiratory rhythm generation in mammals: synaptic and membrane properties. Respir Physiol 110:71-85.
40. Rybak IA, St. John WM, Paton FR. 2001. Models of neuronal bursting behavior: implications for in vivo versus in vitro respiratory rhythmogenesis. In: Poon and Kazemi, editors. Frontiers in modeling and control of breathing. New York: Kluwer Academic-Plenum Publishers.
41. 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.
42. Schaap J, Pennartz CM, Meijer JH. 2003. Electrophysiology of the circadian pacemaker in mammals. Chronobiol Int 20:171-188.
43. Singer W, Lux HD. 1975. Extracellular potassium gradients and visual receptive fields in the cat striate cortex. Brain Res 96:378-383.
44. Somjen GG. 2002. Ion regulation in the brain: implications for pathophysiology. Neuroscientist 8:254-267.
45. Stankiewicz M, Grolleau F, Rochat H, Zlotkin E, Pelhate M, Lapied B. 1999. Insect background sodium channel as a new target for scorpion alpha toxin. Pestic Sci 55:1021-1026.
46. Telgkamp P, Cao YQ, Basbaum Al, Ramirez JM. 2002. Long-term deprivation of substance P in PPT-A mutant mice alters the anoxic response of the isolated respiratory network. J Neurophysiol 88:206-213.
47. Telgkamp P, Ramirez JM. 1999. Differential response of respiratory nuclei to anoxia in rhythmic brainstem slices of mice. J Neurophysiol 82:2163-2170.
48. 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.
49. Thoby-Brisson M, Telgkamp P, Ramirez JM. 2000. The role of the hyperpolarization-activated current in modulating rhythmic activity in the isolated respiratory network of mice. J Neurosci 20:2994-3005.
50. Tryba AK, Peña F, JM Ramirez. 2003. Stabilization of bursting in respiratory pacemaker neurons J Neurosci 23:3538-3546.
51. Tryba AK, Ramirez JM. 2003. Response of the respiratory network of mice to hyperthermia J Neurophysiol 89:2975-2983.
52. Ward SM, Sanders KM. 2001. Physiology and pathophysiology of the interstitial cell of Cajal: from bench to bedside. I. Functional development and plasticity of interstitial cells of Cajal networks. Am J Physiol 281:G602-G611.
53. Xiong Z-Q, JL Stringer. 2000. Sodium pump activity, not glial spatial buffering, clears potassium after epileptiform activity induced in the dentate gyrus. J Neurophysiol 83:1443-1451.
54. Zilberter YI, Starmer CF, Starobin J, Grant AO. 1994. Late Na channels in cardiac cells: the physiological role of background Na channels. Biophys J 67:153-160.