INaP underlies intrinsic spiking and rhythm generation in networks of cultured rat spinal neurons

European Journal of Neuroscience

Volumn 20, Issue 4, 2004, Pages 976-988

  Darbon, Pascal ^a   Yvon, Cédric ^a   Legrand, Jean Christophe ^a   Streit, Jürg ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Hyperpolarization activated cationic current; Population burst; Rhythmic activity; Sodium persistent current; Spinal network

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); RILUZOLE; MONOVALENT CATION; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; EMBRYO; HYPERPOLARIZATION; MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; RHYTHM; SPINAL CORD NERVE CELL; TECHNIQUE; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; DRUG EFFECT; NERVE CELL; NERVE CELL NETWORK; PERIODICITY; PHYSIOLOGY; SPINAL CORD;

ACTION POTENTIALS; ANIMALS; CATIONS, MONOVALENT; CELLS, CULTURED; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; RATS; RILUZOLE; SODIUM CHANNELS; SPINAL CORD;

EID: 4344608331     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03565.x     Document Type: Article

References (44)

1. Angstadt, J.D. (1999) Persistent inward currents in cultured Retzius cells of the medicinal leech. J. Comp. Physiol. [A], 184, 49-61.
2. Ballerini, L. & Galante, M. (1998) Network bursting by organotypic spinal slice cultures in the presence of bicuculline and/or strychnine is developmentally regulated. Eur. J. Neurosci., 10, 2871-2879.
3. Beurrier, C., Bioulac, B. & Hammond, C. (2000) Slowly inactivating sodium current [I (NaP)] underlies single-spike activity in rat subthalamic neurons. J. Neurophysiol., 83, 1951-1957.
4. Bevan, M.D. & Wilson, C.J. (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J. Neurosci., 19, 7617-7628.
5. Bracci, E., Ballerini, L. & Nistri, A. (1996) Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord. J. Neurophysiol., 75, 640-647.
6. Butera, R.J. Jr, Rinzel, J. & Smith, J.C. (1999) Models of respiratory rhythm generation in the pre-Botzinger complex. I. Bursting pacemaker neurons. J. Neurophysiol., 82, 382-397.
7. Butt, S.J., Harris-Warrick, R.M. & Kiehn, O. (2002) Firing properties of identified interneuron populations in the mammalian hindlimb central pattern generator. J. Neurosci., 22, 9961-9971.
8. Cazalets, J.R., Borde, M. & Clarac, F. (1996) The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat. J. Neurosci, 16, 298-306.
9. Cowley, K.C. & Schmidt, B.J. (1995) Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J. Neurophysiol., 74, 1109-1117.
10. Darbon, P., Pignier, C., Niggli, E. & Streit, J. (2002a) Involvement of calcium in rhythmic activity induced by disinhibition in cultured spinal cord networks. J. Neurophysiol., 88, 1461-1468.
11. Darbon, P., Scicluna, L., Tscherter, A. & Streit, J. (2002b) Mechanisms controlling bursting activity induced by disinhibition in spinal cord networks. Eur. J. Neurosci., 15, 671-683.
12. Darbon, P., Tscherter, A., Yvon, C. & Streit, J. (2003) Role of the electrogenic Na/K pump in disinhibition-induced bursting in cultured spinal networks. J. Neurophysiol., 90, 3119-3129.
13. Del Negro, C.A., Koshiya, N., Butera, R.J. Jr & Smith, J.C. (2002a) Persistent sodium current, membrane properties and bursting behavior of pre-botzinger complex inspiratory neurons in vitro. J. Neurophysiol., 88, 2242-2250.
14. Del Negro, C.A., Morgado-Valle, C. & Feldman, J.L. (2002b) Respiratory rhythm: an emergent network property? Neuron, 34, 821-830.
15. Duprat, F., Lesage, F., Patel, A.J., Fink, M., Romey, G. & Lazdunski, M. (2000) The neuroprotective agent riluzole activates the two P domain K (+) channels TREK-1 and TRAAK. Mol. Pharmacol., 57, 906-912.
16. Ellerkmann, R.K., Riazanski, V., Elger, C.E., Urban, B.W. & Beck, H. (2001) Slow recovery from inactivation regulates the availability of voltage-dependent Na (+) channels in hippocampal granule cells, hilar neurons and basket cells. J. Physiol (Lond.), 532, 385-397.
17. Fleidervish, I.A., Friedman, A. & Gutnick, M.J. (1996) Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J. Physiol (Lond.), 493, 83-97.
18. Ghamari-Langroudi, M. & Bourque, C.W. (2001) Ionic basis of the caesium-induced depolarisation in rat supraoptic nucleus neurones. J. Physiol (Lond.), 536, 797-808.
19. Grillner, S., Ekeberg, El Manira, A., Lansner, A., Parker, D., Tegner, J. & Wallen, P. (1998) Intrinsic function of a neuronal network - a vertebrate central pattern generator. Brain Res. Brain Res. Rev., 26, 184-197.
20. Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch., 391, 85-100.
21. Hanson, M.G. & Landmesser, L.T. (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic mouse spinal cord. J. Neurosci., 23, 587-600.
22. He, Y., Benz, A., Fu, T., Wang, M., Covey, D.F., Zorumski, C.F. & Mennerick, S. (2002) Neuroprotective agent riluzole potentiates postsynaptic GABA (A) receptor function. Neuropharmacology, 42, 199-209.
23. Huang, C.S., Song, J.H., Nagata, K., Yeh, J.Z. & Narahashi, T. (1997) Effects of the neuroprotective agent riluzole on the high voltage-activated calcium channels of rat dorsal root ganglion neurons. J. Pharmacol. Exp. Ther., 282, 1280-1290.
24. Jinno, S., Ishizuka, S. & Kosaka, T. (2003) Ionic currents underlying rhythmic bursting of ventral mossy cells in the developing mouse dentate gyrus. Eur. J. Neurosci., 17, 1338-1354.
25. Kiehn, O. & Kjaerulff, O. (1998) Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann. NY Acad. Sci., 860, 110-129.
26. Luthi, A. & McCormick, D.A. (1998) H-current: properties of a neuronal and network pacemaker. Neuron, 21, 9-12.
27. Martin, D., Thompson, M.A. & Nadler, J.V. (1993) The neuroprotective agent riluzole inhibits release of glutamate and aspartate from slices of hippocampal area CA1. Eur. J. Pharmacol., 250, 473-476.
28. 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.
29. Mohammadi, B., Krampfl, K., Moschref, H., Dengler, R. & Bufler, J. (2001) Interaction of the neuroprotective drug riluzole with GABA (A) and glycine receptor channels. Eur. J. Pharmacol., 415, 135-140.
30. Müller, W. & Swandulla, D. (1995) Synaptic feedback excitation has hypothalamic neural networks generate quasirhythmic burst activity. J. Neurophysiol., 73, 855-861.
31. Pape, H.C. (1996) Queer current and pacemaker: the hyperpolarization- activated cation current in neurons. Annu. Rev. Physiol., 58, 299-327.
32. Rekling, J.C. & Feldman, J.L. (1998) PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol., 60, 385-405.
33. Rybak, I.A., Shevtsova, N.A., St-John, W.M., Paton, J.F. & Pierrefiche, O. (2003) Endogenous rhythm generation in the pre-Botzinger complex and ionic currents: modelling and in vitro studies. Eur. J. Neurosci., 18, 239-357.
34. Sanchez-Vives, M.V. & McCormick, D.A. (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci., 3, 1027-1034.
35. Santoro, B., Chen, S., Luthi, A., Pavlidís, P., Shumyatsky, G.P., Tibbs, G.R. & Siegelbaum, S.A. (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci., 20, 5264-5275.
36. Streit, J. (1993) Regular oscillations of synaptic activity in spinal networks in vitro. J. Neurophysiol., 70, 871-878.
37. Streit, J., Tscherter, A.O., H.M. & Philipp, R. (2001) The generation of rhythmic activity in dissociated cultures of rat spinal cord. Eur. J. Neurosci., 14, 191-202.
38. Taddese, A. & Bean, B.P. (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron, 33, 587-600.
39. Tscherter, A., Heuschkel, M.O., Renaud, P. & Streit, J. (2001) Spatiotemporal characterization of rhythmic activity in spinal cord slice cultures. Eur. J. Neurosci., 14, 179-190.
40. Urbani, A. & Belluzzi, O. (2000) Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur. J. Neurosci., 12, 3567-3174.
41. Washbum, D.L., Anderson, J.W. & Ferguson, A.V. (2000) A subthreshold persistent sodium current mediates bursting in rat subfomical organ neurones. J. Physiol. (Lond.), 529, 359-371.
42. Wenner, P. & O'Donovan, M.J. (2001) Mechanisms that initiate spontaneous network activity in the developing chick spinal cord. J. Neurophysiol., 86, 1481-1198.
43. Williams, S.R., Christensen, S.R., Stuart, G.J. & Hausser, M. (2002) Membrane potential bistability is controlled by the hyperpolarization-activated current I (H) in rat cerebellar Purkinje neurons in vitro. J. Physiol (Lond.), 539, 469-483.
44. Zona, C., Siniscalchi, A., Mercuri, N.B. & Bernardi, G. (1998) Riluzole interacts with voltage-activated sodium and potassium currents in cultured rat cortical neurons. Neuroscience, 85, 931-938.