Developmental expression of Na+ currents in mouse Purkinje neurons

European Journal of Neuroscience

Volumn 24, Issue 9, 2006, Pages 2557-2566

  Fry, Mark ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Action potential; Neuronal development; Patch clamp; Persistent current; Resurgent current; Sodium current

Indexed keywords

SODIUM ION; VOLTAGE GATED SODIUM CHANNEL;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; FREQUENCY ANALYSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NEWBORN; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; POSTNATAL GROWTH; PRIORITY JOURNAL; PURKINJE CELL; SODIUM CURRENT; SYNAPTIC POTENTIAL; UPREGULATION;

ACTION POTENTIALS; ANIMALS; CEREBELLUM; MICE; MICE, TRANSGENIC; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; SODIUM; SODIUM CHANNELS;

EID: 33750927150     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05139.x     Document Type: Article

References (64)

1. Bader, C.R., Bertrand, D. & Kato, A.C. (1983) Membrane currents in a developing parasympathetic ganglion. Dev. Biol., 98, 515-519.
2. Black, J.A., Yokoyama, S., Higashida, H., Ransom, B.R. & Waxman, S.G. (1994) Sodium channel mRNAs I, II and III in the CNS: cell-specific expression. Brain Res. Mol. Brain Res., 22, 275-289.
3. Calvet, M.C. (1974) Patterns of spontaneous electrical activity in tissue cultures of mammalian cerebral cortex vs. cerebellum. Brain Res., 69, 281-295.
4. + channel expression and function in rat Purkinje neurons. J. Neurosci., 22, 4456-4467.
5. Costa, P.F. (1996) The kinetic parameters of sodium currents in maturing acutely isolated rat hippocampal CA1 neurones. Brain Res. Dev. Brain Res., 91, 29-40.
6. Crepel, F. (1971) Maturation of climbing fiber responses in the rat. Brain Res., 35, 272-276.
7. Crill, W.E. (1996) Persistent sodium current in mammalian central neurons. Annu. Rev. Physiol., 58, 349-362.
8. Do, M.T. & Bean, B.P. (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron, 39, 109-120.
9. Etzion, Y. & Grossman, Y. (2001) Highly 4-aminopyridine sensitive delayed rectifier current modulates the excitability of guinea pig cerebellar Purkinje cells. Exp. Brain Res., 139, 419-425.
10. Felts, P.A., Yokoyama, S., Dib-Hajj, S., Black, J.A. & Waxman, S.G. (1997) Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res. Mol. Brain Res., 45, 71-82.
11. Gao, B.X. & Ziskind-Conhaim, L. (1998) Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J. Neurophysiol., 80, 3047-3061.
12. Garcia, K.D., Sprunger, L.K., Meisler, M.H. & Beam, K.G. (1998) The sodium channel Scn8a is the major contributor to the postnatal developmental increase of sodium current density in spinal motoneurons. J. Neurosci., 18, 5234-5239.
13. Grieco, T.M., Afshari, F.S. & Raman, I.M. (2002) A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar purkinje neurons. J. Neurosci., 22, 3100-3107.
14. Grieco, T.M., Malhotra, J.D., Chen, C., Isom, L.L. & Raman, I.M. (2005) Open-channel block by the cytoplasmic tail of sodium channel beta4 as a mechanism for resurgent sodium current. Neuron, 45, 233-244.
15. Gruol, D.L. (1983) Cultured cerebellar neurons. endogenous and exogenous components of Purkinje cell activity and membrane response to putative transmitters. Brain Res., 263, 223-241.
16. Gruol, D.L., Deal, C.R. & Yool, A.J. (1992) Developmental changes in calcium conductances contribute to the physiological maturation of cerebellar Purkinje neurons in culture. J. Neurosci., 12, 2838-2848.
17. Gruol, D.L. & Franklin, C.L. (1987) Morphological and physiological differentiation of Purkinje neurons in cultures of rat cerebellum. J. Neurosci., 7, 1271-1293.
18. 2+ regulation of neuronal properties in early developing purkinje neurons. Cerebellum., 4, 128-139.
19. Hamon, B., Conde, F., Jaillard, D., Thomasset, M. & Crepel, F. (1991) In vitro development of rat cerebellar neurons of early embryonic origin. An anatomical and electrophysiological study. Eur. J. Neurosci., 3, 855-865.
20. Hockberger, P.E., Tseng, H.Y. & Connor, J.A. (1989) Development of rat cerebellar Purkinje cells: electrophysiological properties following acute isolation and in long-term culture. J. Neurosci., 9, 2258-2271.
21. Hodgkin, A. & Huxley, A. (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J. Physiol. (Lond.), 116, 449-472.
22. + conductances in rat neocortical neurons: appearance of a slowly inactivating component. J. Neurophysiol., 59, 778-795.
23. Jarvinen, M.K. (2003) The Impact of Sodium Channel Isoform Expression on Cerebellar Purkinje Cell Development. Thesis/Dissertation. Dartmouth Medical School, Hanover, NH, USA.
24. + channel isoform expression during developmental changes in electrical activity. A patch clamp and single cell RT-PCR analysis of Purkinje cells in cerebellar slices. Soc. Neurosci. Abstr., 46, 24.
25. Kapoor, R., Jaeger, C.B. & Llinas, R. (1988) Electrophysiology of the mammalian cerebellar cortex in organ culture. Neuroscience, 26, 493-507.
26. Kay, A.R., Sugimori, M. & Llinas, R. (1998) Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J. Neurophysiol., 80, 1167-1179.
27. Khaliq, Z.M., Gouwens, N.W. & Raman, I.M. (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J. Neurosci., 23, 4899-4912.
28. Khaliq, Z.M. & Raman, I.M. (2006) Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J. Neurosci., 26, 1935-1944.
29. Liljelund, P., Netzeband, J.G. & Gruol, D.L. (2000) L-Type calcium channels mediate calcium oscillations in early postnatal Purkinje neurons. J. Neurosci., 20, 7394-7403.
30. Llinas, R. & Sugimori, M. (1980a) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (Lond.), 305, 197-213.
31. Llinas, R. & Sugimori, M. (1980b) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.), 305, 171-195.
32. MacDermott, A.B. & Westbrook, G.L. (1986) Early development of voltage-dependent sodium currents in cultured mouse spinal cord neurons. Dev. Biol., 113, 317-326.
33. McCobb, D.P., Best, P.M. & Beam, K.G. (1990) The differentiation of excitability in embryonic chick limb motoneurons. J. Neurosci., 10, 2974-2984.
34. McCormick, D.A. & Prince, D.A. (1987) Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J. Physiol. (Lond.), 393, 743-762.
35. McKay, B.E. & Turner, R.W. (2005) Physiological and morphological development of the rat cerebellar Purkinje cell. J. Physiol. (Lond.), 567, 829-850.
36. Morgan, K., Stevens, E.B., Shah, B., Cox, P.J., Dixon, A.K., Lee, K., Pinnock, R.D., Hughes, J., Richardson, P.J., Mizuguchi, K. & Jackson, A.P. (2000) Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl Acad. Sci. USA, 97, 2308-2313.
37. + channel expression in rat cerebellum during postnatal development. J. Neurosci., 18, 16-25.
38. + channel activity contributes to the maturation of cellular firing patterns in developing cerebellar Purkinje neurons. Brain Res. Dev. Brain Res., 108, 193-203.
39. Nam, S.C. & Hockberger, P.E. (1997) Analysis of spontaneous electrical activity in cerebellar Purkinje cells acutely isolated from postnatal rats. J. Neurobiol., 33, 18-32.
40. Park, C.C. & Ahmed, Z. (1991) Characterization of sodium current in developing rat diencephalic neurons in serum-free culture. J. Neurophysiol., 65, 1011-1021.
41. Pineda, R.H., Heiser, R.A. & Ribera, A.B. (2005) Developmental, molecular, and genetic dissection of INa in vivo in embryonic zebrafish sensory neurons. J. Neurophysiol., 93, 3582-3593.
42. Raman, I.M. & Bean, B.P. (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci., 17, 4517-4526.
43. Raman, I.M. & Bean, B.P. (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci., 19, 1663-1674.
44. Raman, I.M., Sprunger, L.K., Meisler, M.H. & Bean, B.P. (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron, 19, 881-891.
45. Raman, I.M., Gustafson, A.E. & Padgett, D. (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J. Neurosci., 20, 9004-9016.
46. Rothe, T., Juttner, R., Bahring, R. & Grantyn, R. (1999) Ion conductances related to development of repetitive firing in mouse retinal ganglion neurons in situ. J. Neurobiol., 38, 191-206.
47. + channel beta 1 subunit mRNA expression in developing rat central nervous system. Brain Res. Mol. Brain Res., 34, 239-250.
48. Schaller, K.L. & Caldwell, J.H. (2000) Developmental and regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J. Comp. Neurol., 420, 84-97.
49. Schaller, K.L. & Caldwell, J.H. (2003) Expression and distribution of voltage-gated sodium channels in the cerebellum. Cerebellum., 2, 2-9.
50. Schaller, K.L., Krzemien, D.M., Yarowsky, P.J., Krueger, B.K. & Caldwell, J.H. (1995) A novel, abundant sodium channel expressed in neurons and glia. J. Neurosci., 15, 3231-3242.
51. Shah, B.S., Stevens, E.B., Pinnock, R.D., Dixon, A.K. & Lee, K. (2001) Developmental expression of the novel voltage-gated sodium channel auxiliary subunit beta3, in rat CNS. J. Physiol. (Lond.), 534, 763-776.
52. Sharma, S.K., Nayar, U., Maheshwari, M.C. & Singh, B. (1993) Purkinje cell evoked unit activity in developing normal and undernourished rats. J. Neurol. Sci., 116, 212-219.
53. Stuart, G. & Hausser, M. (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron, 13, 703-712.
54. Swensen, A.M. & Bean, B.P. (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J. Neurosci., 23, 9650-9663.
55. Swensen, A.M. & Bean, B.P. (2005) Robustness of burst firing in dissociated purkinje neurons with acute or long-term reductions in sodium conductance. J. Neurosci., 25, 3509-3520.
56. Taddese, A. & Bean, B.P. (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron, 33, 587-600.
57. Tomomura, M., Rice, D.S., Morgan, J.I. & Yuzaki, M. (2001) Purification of Purkinje cells by fluorescence-activated cell sorting from transgenic mice that express green fluorescent protein. Eur. J. Neurosci., 14, 57-63.
58. Vega-Saenz de Miera, E.C., Rudy, B., Sugimori, M. & Llinas, R. (1997) Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc. Natl Acad. Sci. USA, 94, 7059-7064.
59. 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.
60. Womack, M. & Khodakhah, K. (2002) Active contribution of dendrites to the tonic and trimodal patterns of activity in cerebellar Purkinje neurons. J. Neurosci., 22, 10603-10612.
61. Woodward, D.J., Hoffer, B.J. & Lapham, L.W. (1969) Postnatal development of electrical and enzyme histochemical activity in Purkinje cells. Exp. Neurol., 23, 120-139.
62. Woodward, D.J., Hoffer, B.J., Siggins, G.R. & Bloom, F.E. (1971) The ontogenetic development of synaptic junctions, synaptic activation and responsiveness to neurotransmitter substances in rat cerebellar purkinje cells. Brain Res., 34, 73-97.
63. +-selective channel activity during differentiation of the Purkinje neuron in culture. J. Neurosci., 8, 1971-1980.
64. Yu, F.H., Westenbroek, R.E., Silos-Santiago, I., McCormick, K.A., Lawson, D., Ge, P., Ferriera, H., Lilly, J., DiStefano, P.S., Catterall, W.A., Scheuer, T. & Curtis, R. (2003) Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2. J. Neurosci., 23, 7577-7585.