Pyramidal cells of rodent presubiculum express a tetrodotoxin-insensitive Na+ current

Journal of Physiology

Volumn 587, Issue 17, 2009, Pages 4249-4264

  Fricker, Desdemona ^a   Dinocourt, Céline ^a   Eugène, Emmanuel ^a   Wood, John ^b   Miles, Richard ^a  

^a INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NAV1.8 SODIUM CHANNEL; NAV1.9 SODIUM CHANNEL; SODIUM CHANNEL; SODIUM ION; TETRODOTOXIN; UNCLASSIFIED DRUG; SODIUM CHANNEL NAV1.8; SODIUM CHANNEL NAV1.9;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL ACTIVITY; CONTROLLED STUDY; ELECTRIC POTENTIAL; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NONHUMAN; PRESUBICULUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE; PYRAMIDAL NERVE CELL; RAT; RODENT; SODIUM CONDUCTANCE; SODIUM CURRENT; SUBICULUM; TRANSPORT KINETICS; DEPOLARIZATION; FIRING RATE; FREQUENCY MODULATION; HIPPOCAMPUS; KINETICS; NERVE POTENTIAL; NERVOUS SYSTEM CONDUCTANCE; NERVOUS SYSTEM POTENTIAL; NEUROANATOMY; PRESUBICULUM NEURON; REPETITIVE FIRING; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ION CHANNEL GATING; PARAHIPPOCAMPAL GYRUS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; TETRODOTOXIN;

EID: 69949091312     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.175349     Document Type: Article

References (76)

1. Akopian AN, Okuse K, Souslova V, England S, Ogata N & Wood JN (1999a). Trans-splicing of a voltage-gated sodium channel is regulated by nerve growth factor. FEBS Lett 445, 177-182.
2. Akopian AN, Sivilotti L & Wood JN (1996). A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379, 257-262.
3. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH & Wood JN (1999b). The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2, 541-548.
4. Araya R, Nikolenko V, Eisenthal KB & Yuste R (2007). Sodium channels amplify spine potentials. Proc Natl Acad Sci U S A 104, 12347-12352.
5. Bar-Yehuda D & Korngreen A (2008). Space-clamp problems when voltage clamping neurons expressing voltage-gated conductances. J Neurophysiol 99, 1127-1136.
6. Bean BP (2007). The action potential in mammalian central neurons. Nat Rev Neurosci 8, 451-465.
7. Bennett V & Healy J (2008). Being there: Cellular targeting of voltage-gated sodium channels in the heart. J Cell Biol 180, 13-15.
8. 2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22, 10277-10290.
9. Bourinet E, Soong TW, Sutton K, Slaymaker S, Mathews E, Monteil A, Zamponi GW, Nargeot J & Snutch TP (1999). Splicing of α1A subunit gene generates phenotypic variants of P- and Q-type calcium channels. Nat Neurosci 2, 407-415.
10. Brown AM, Lee KS & Powell T (1981). Sodium current in single rat heart muscle cells. J Physiol 318, 479-500.
11. Cacucci F, Lever C, Wills TJ, Burgess N & O'Keefe J (2004). Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J Neurosci 24, 8265-8277.
12. Cai X, Wei DS, Gallagher SE, Bagal A, Mei YA, Kao JP, Thompson SM & Tang CM (2007). Hyperexcitability of distal dendrites in hippocampal pyramidal cells after chronic partial deafferentation. J Neurosci 27, 59-68.
13. + channel in chick dorsal root ganglion neurons. J Gen Physiol 104, 747-771.
14. Camacho JA, Hensellek S, Rougier JS, Blechschmidt S, Abriel H, Benndorf K & Zimmer T (2006). Modulation of Nav1.5 channel function by an alternatively spliced sequence in the DII/DIII linker region. J Biol Chem 281, 9498-9506.
15. + current in pyramidal neurones of rat perirhinal cortex: axonal location of channels and contribution to depolarizing drive during repetitive firing. J Physiol 582, 1179-1193.
16. 2+ channels. J Neurosci 24, 6334-6342.
17. V1.9 channels in enteric and spinal sensory neurons. Mol Cell Neurosci 26, 123-134.
18. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN & Waxman SG (1999). A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 19, RC43.
19. Dib-Hajj S, Black JA, Cummins TR & Waxman SG (2002). NaN/Nav1.9: A sodium channel with unique properties. Trends Neurosci 25, 253-259.
20. V1.8 (SNS/PN3): Expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol 550, 739-752.
21. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: Standards and advice. J Physiol 587, 713-719.
22. + conductance in neurons of the gastric mill rhythm generator of spiny lobsters. J Exp Biol 200, 1795-1807.
23. Fricker D & Miles R (2000). EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559-569.
24. Fricker D, Verheugen JA & Miles R (1999). Cell-attached measurements of the firing threshold of rat hippocampal neurones. J Physiol 517, 791-804.
25. Funahashi M, Harris E & Stewart M (1999). Re-entrant activity in a presubiculum-subiculum circuit generates epileptiform activity in vitro. Brain Res 849, 139-146.
26. Funahashi M & Stewart M (1997). Presubicular and parasubicular cortical neurons of the rat: Functional separation of deep and superficial neurons in vitro. J Physiol 501, 387-403.
27. + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58, 387-400.
28. Goldin AL (2001). Resurgence of sodium channel research. Annu Rev Physiol 63, 871-894.
29. Harris E & Stewart M (2001). Propagation of synchronous epileptiform events from subiculum backward into area CA1 of rat brain slices. Brain Res 895, 41-49.
30. Harvey PJ, Li Y, Li X & Bennett DJ (2006). Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats. J Neurophysiol 96, 1141-1157.
31. Heckman CJ, Johnson M, Mottram C & Schuster J (2008). Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist 14, 264-275.
32. Hille B (1992). Ionic Channels of Excitable Membranes. Sinauer Associates Inc., Sunderland, Massachusetts.
33. Hivert B, Luvisetto S, Navangione A, Tottene A & Pietrobon D (1999). Anomalous L-type calcium channels of rat spinal motoneurons. J Gen Physiol 113, 679-694.
34. Holthoff K, Kovalchuk Y & Konnerth A (2006). Dendritic spikes and activity-dependent synaptic plasticity. Cell Tissue Res 326, 369-377.
35. Hounsgaard J, Hultborn H, Jespersen B & Kiehn O (1988). Bistability of a-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405, 345-367.
36. Kerr NC, Gao Z, Holmes FE, Hobson SA, Hancox JC, Wynick D & James AF (2007). The sodium channel Nav1.5a is the predominant isoform expressed in adult mouse dorsal root ganglia and exhibits distinct inactivation properties from the full-length Nav1.5 channel. Mol Cell Neurosci 35, 283-291.
37. Kerr NC, Holmes FE & Wynick D (2004). Novel isoforms of the sodium channels Nav1.8 and Nav1.5 are produced by a conserved mechanism in mouse and rat. J Biol Chem 279, 24826-24833.
38. Korn SJ & Ikeda SR (1995). Permeation selectivity by competition in a delayed rectifier potassium channel. Science 269, 410-412.
39. Lee RH & Heckman CJ (1998). Bistability in spinal motoneurons in vivo: Systematic variations in persistent inward currents. J Neurophysiol 80, 583-593.
40. + channels amplify EPSPs in hippocampal CA1 pyramidal cells. J Neurophysiol 76, 2181-2191.
41. Madeja M, Wolf C & Speckmann EJ (2001). Reduction of voltage-operated sodium currents by the anticonvulsant drug sulthiame. Brain Res 900, 88-94.
42. Magistretti J, Mantegazza M, de Curtis M & Wanke E (1998). Modalities of distortion of physiological voltage signals by patch-clamp amplifiers: A modeling study. Biophys J 74, 831-842.
43. Menendez de la Prida L, Suarez F & Pozo MA (2003). Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro. Hippocampus 13, 728-744.
44. Moritz AT, Newkirk G, Powers RK & Binder MD (2007). Facilitation of somatic calcium channels can evoke prolonged tail currents in rat hypoglossal motoneurons. J Neurophysiol 98, 1042-1047.
45. Moser EI, Kropff E & Moser MB (2008). Place cells, grid cells, and the brain's spatial representation system. Annu Rev Neurosci 31, 69-89.
46. Muller W & Lux HD (1993). Analysis of voltage-dependent membrane currents in spatially extended neurons from point-clamp data. J Neurophysiol 69, 241-247.
47. Nishikawa S, Goto S, Hamasaki T, Yamada K & Ushio Y (2002). Involvement of reelin and Cajal-Retzius cells in the developmental formation of vertical columnar structures in the cerebral cortex: evidence from the study of mouse presubicular cortex. Cereb Cortex 12, 1024-1030.
48. O'Mara SM, Commins S, Anderson M & Gigg J (2001). The subiculum: A review of form, physiology and function. Prog Neurobiol 64, 129-155.
49. V1.9. J Physiol 586, 1077-1087.
50. h-channel gene PIIH: Modification of channel properties by alternative splicing and role in rhythmic activity. J Neurophysiol 97, 3880-3892.
51. Partridge LD & Valenzuela CF (2000). Block of hippocampal CAN channels by flufenamate. Brain Res 867, 143-148.
52. Powers RK & Binder MD (2003). Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89, 615-624.
53. Raingo J, Castiglioni AJ & Lipscombe D (2007). Alternative splicing controls G protein-dependent inhibition of N-type calcium channels in nociceptors. Nat Neurosci 10, 285-292.
54. + channel in mammalian cardiac cells. Two kinds of tetrodotoxin receptors in rat heart membranes. J Biol Chem 258, 8799-8805.
55. v1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86, 629-640.
56. v1.5 underlies the 'third TTX-R sodium current' in rat small DRG neurons. Brain Res Mol Brain Res 106, 70-82.
57. Rolls ET (2006). Neurophysiological and computational analyses of the primate presubiculum, subiculum and related areas. Behav Brain Res 174, 289-303.
58. Roy ML & Narahashi T (1992). Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J Neurosci 12, 2104-2111.
59. Rush AM, Cummins TR & Waxman SG (2007). Multiple sodium channels and their roles in electrogenesis within dorsal root ganglion neurons. J Physiol 579, 1-14.
60. + currents by lidocaine and bupivacaine reduce firing frequency in DRG neurons. J Neurophysiol 79, 1746-1754.
61. Schwindt PC & Crill WE (1995). Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J Neurophysiol 74, 2220-2224.
62. Sivilotti L, Okuse K, Akopian AN, Moss S & Wood JN (1997). A single serine residue confers tetrodotoxin insensitivity on the rat sensory-neuron-specific sodium channel SNS. FEBS Lett 409, 49-52.
63. Song W, Liu Z, Tan J, Nomura Y & Dong K (2004). RNA editing generates tissue-specific sodium channels with distinct gating properties. J Biol Chem 279, 32554-32561.
64. Souslova VA, Fox M, Wood JN & Akopian AN (1997). Cloning and characterization of a mouse sensory neuron tetrodotoxin-resistant voltage-gated sodium channel gene, Scn10a. Genomics 41, 201-209.
65. Stuart GJ & Sakmann B (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72.
66. Svirskis G, Gutman A & Hounsgaard J (2001). Electrotonic structure of motoneurons in the spinal cord of the turtle: Inferences for the mechanisms of bistability. J Neurophysiol 85, 391-398.
67. Taube JS, Muller RU & Ranck JB Jr (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10, 420-435.
68. Theiss RD, Kuo JJ & Heckman CJ (2007). Persistent inward currents in rat ventral horn neurones. J Physiol 580, 507-522.
69. + channel isoforms from human brain. Neuron 13, 1315-1330.
70. Tsien RW, Lipscombe D, Madison DV, Bley KR & Fox AP (1988). Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11, 431-438.
71. + current in the medial entorhinal cortex. Neuron 11, 1037-1047.
72. Williams SR & Mitchell SJ (2008). Direct measurement of somatic voltage clamp errors in central neurons. Nat Neurosci 11, 790-798.
73. Yoshida M & Hasselmo ME (2009). Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29, 4945-4952.
74. Zhong G, Masino MA & Harris-Warrick RM (2007). Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27, 4507-4518.
75. + channels: Primary structure and function of two isoforms and alternatively spliced variants. Am J Physiol Heart Circ Physiol 282, H1007-H1017.
76. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J, Nau C, Wood JN & Reeh PW (2007). Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447, 855-858.