Persistent sodium current in layer 5 neocortical neurons is primarily generated in the proximal axon

Journal of Neuroscience

Volumn 26, Issue 13, 2006, Pages 3465-3473

  Astman, Nadav ^a   Gutnick, Michael J ^a   Fleidervish, Ilya A ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Axon; Excitability; Layer 5 pyramidal neuron; Neocortex; Persistent sodium current; Sodium channel

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; DENDRITE; FEMALE; MALE; MEMBRANE CURRENT; MOLECULAR DYNAMICS; NEOCORTEX; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SODIUM CURRENT; SOMATIC CELL;

ACTION POTENTIALS; ANIMALS; AXONS; CELLS, CULTURED; LONG-TERM POTENTIATION; MEMBRANE POTENTIALS; MICE; NEOCORTEX; NERVE NET; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 33645456325     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4907-05.2006     Document Type: Article

References (59)

1. Alzheimer C (1994) A novel voltage-dependent cation current in rat neocortical neurones. J Physiol (Lond) 479:199-205.
2. + current in pyramidal neurons from rat sensorimotor cortex. J Neurophysiol 69:290-292.
3. + current in pyramidal neurons from rat and cat sensorimotor cortex. J Neurosci 13:660-673.
4. Andreasen M, Lambert JD (1999) Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones. J Physiol (Lond) 519:85-100.
5. Angelides KJ, Elmer LW, Loftus D, Elson E (1988) Distribution and lateral mobility of voltage-dependent sodium channels in neurons. J Cell Biol 106:1911-1925.
6. Blanton MG, Lo Turco JJ, Kriegstein AR (1989) Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 30:203-210.
7. + currents is compatible with modal-gating hypothesis for sodium channels. J Neurophysiol 71:2562-2565.
8. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR (2000) Sodium channel Na(v)1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 97:5616-5620.
9. + channels: an unexpected form of cellular plasticity. Nat Rev Neurosci 2:397-407.
10. Carr DB, Day M, Cantrell AR, Held J, Scheuer T, Catterall WA, Surmeier DJ (2003) Transmitter modulation of slow, activity-dependent alterations in sodium channel availability endows neurons with a novel form of cellular plasticity. Neuron 39:793-806.
11. Catterall WA (1981) Localization of sodium channels in cultured neural cells. J Neurosci 1:777-783.
12. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
13. Chandler WK, Meves H (1966) Incomplete sodium inactivation in internally perfused giant axons from Loligo forbesi. J Physiol (Lond) 186:121P-122P.
14. + channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16:6676-6686.
15. Colbert CM, Pan E (2002) Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5:533-538.
16. Crill WE (1996) Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58:349-362.
17. Cummins TR, Aglieco F, Renganathan M, Herzog RI, Dib-Hajj SD, Waxman SG (2001) Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci 21:5952-5961.
18. + channels in hippocampal mossy fiber boutons. Neuron 45:405-417.
19. 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.
20. + current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J Physiol (Lond) 493:83-97.
21. Fleidervish IA, Binshtok AM, Gutnick MJ (1998) Functionally distinct NMDA receptors mediate horizontal connectivity within layer 4 of mouse barrel cortex. Neuron 21:1055-1065.
22. Goldin AL (2001) Resurgence of sodium channel research. Annu Rev Physiol 63:871-894.
23. Gong B, Rhodes KJ, Bekele-Arcuri Z, Trimmer JS (1999) Type I and type II Na(+) channel alpha-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J Comp Neurol 412:342-352.
24. Gutnick MJ, Crill W (1995) The cortical neuron as an electrophysiological unit. In: The cortical neuron (Gutnick MJ, Mody I, eds), pp 33-51. New York: Oxford UP.
25. Haas HL, Schaerer B, Vosmansky M (1979) A simple perfusion chamber for the study of nervous tissue slices in vitro. J Neurosci Methods 1:323-325.
26. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
27. Hammarstrom AK, Gage PW (1998) Inhibition of oxidative metabolism increases persistent sodium current in rat CA1 hippocampal neurons. J Physiol (Lond) 510:735-741.
28. Hammarstrom AK, Gage PW (1999) Nitric oxide increases persistent sodium current in rat hippocampal neurons. J Physiol (Lond) 520:451-461.
29. 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.
30. Huguenard JR, Hamill OP, Prince DA (1989) Sodium channels in dendrites of rat cortical pyramidal neurons. Proc Natl Acad Sci USA 86:2473-2477.
31. Jones EG, Powell TP (1969) Synapses on the axon hillocks and initial segments of pyramidal cell axons in the cerebral cortex. J Cell Sci 5:495-507.
32. + channels during depolarization in guinea-pig cardiac cells. Pflügers Arch 416:493-500.
33. + channels amplify EPSPs in hippocampal CA1 pyramidal cells. J Neurophysiol 76:2181-2191.
34. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George Jr AL (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884.
35. + current in entorhinal cortex neurons. J Neurosci 19:7334-7341.
36. + channel activity in dendritic processes of mammalian cortical neurones. J Physiol (Lond) 521:629-636.
37. Mainen ZF, Joerges J, Huguenard JR, Sejnowski TJ (1995) A model of spike initiation in neocortical pyramidal neurons. Neuron 15:1427-1439.
38. Mantegazza M, Yu FH, Powell AJ, Clare JJ, Catterall WA, Scheuer T (2005) Molecular determinants for modulation of persistent sodium current by G-protein βγ subunits. J Neurosci 25:3341-3349.
39. Migliore M, Shepherd GM (2002) Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3:362-370.
40. +-sensitive dye. J Neurophysiol 78:1188-1192.
41. Neher E, Stevens CF (1977) Conductance fluctuations and ionic pores in membranes. Annu Rev Biophys Bioeng 6:345-381.
42. Patlak JB, Ortiz M (1985) Slow currents through single sodium channels of the adult rat heart. J Gen Physiol 86:89-104.
43. Patlak JB, Ortiz M, Horn R (1986) Opentime heterogeneity during bursting of sodium channels in frog skeletal muscle. Biophys J 49:773-777.
44. Qu Y, Rogers JC, Chen SF, McCormick KA, Scheuer T, Catterall WA (1999) Functional roles of the extracellular segments of the sodium channel alpha subunit in voltage-dependent gating and modulation by beta1 subunits. J Biol Chem 274:32647-32654.
45. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
46. Rush AM, Dib-Hajj SD, Waxman SG (2005) Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J Physiol (Lond) 564:803-815.
47. Smith MR, Smith RD, Plummer NW, Meisler MH, Goldin AL (1998) Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18:6093-6102.
48. Spruston N, Jaffe DB, Johnston D (1994) Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties. Trends Neurosci 17:161-166.
49. Srinivasan J, Schachner M, Catterall WA (1998) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci USA 95:15753-15757.
50. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29:645-655.
51. Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15:1065-1076.
52. Stuart G, Schiller J, Sakmann B (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol (Lond) 505:617-632.
53. Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69-72.
54. Stuart GJ, Dodt HU, Sakmann B (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch 423:511-518.
55. Taddese A, Bean BP (2002) Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron 33:587-600.
56. Waters J, Schaefer A, Sakmann B (2005) Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog Biophys Mol Biol 87:145-170.
57. + channel subtypes in central neurons. Neuron 3:695-704.
58. Yu FH, Catterall WA (2003) Overview of the voltage-gated sodium channel family. Genome Biol 4:207.
59. + channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J Neurosci 25:9704-9720.