Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells

Journal of Neurophysiology

Volumn 95, Issue 6, 2006, Pages 3480-3495

  Yue, Cuiyong ^a   Yaari, Yoel ^a,b  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOPYRIDINE; LINOPIRDINE; NEUROTRANSMITTER; PHENYTOIN; PHORBOL DIBUTYRATE; POTASSIUM CHANNEL BLOCKING AGENT; RETIGABINE; RILUZOLE; SODIUM CHANNEL; TETRODOTOXIN; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DEPOLARIZATION; DRUG EFFECT; MICROELECTRODE; NERVE CELL; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SODIUM CURRENT; SOMATIC CELL; SPIKE;

ACTION POTENTIALS; ANIMALS; AXONS; CELLS, CULTURED; DENDRITES; HIPPOCAMPUS; ION CHANNEL GATING; POTASSIUM CHANNELS; PYRAMIDAL CELLS; RATS; SYNAPTIC TRANSMISSION;

EID: 33744904168     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01333.2005     Document Type: Article

References (59)

1. Aiken SP, Lampe BJ, Murphy PA, and Brown BS. Reduction of spike frequency adaptation and blockade of M-current in rat CA1 pyramidal neurones by linopirdine (DuP 996), a neurotransmitter release enhancer. Br J Pharmacol 11: 1163-1168, 1995.
2. Azouz R, Jensen MS, and Yaari Y. Ionic basis of spike afterdepolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492: 211-223, 1996.
3. Benardo LS, Masukawa LM, and Prince DA. Electrophysiology of isolated hippocampal pyramidal dendrites. J Neurosci 2: 1614-1622, 1982.
4. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, and Matthews G. Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23: 2306-2313, 2003.
5. Brown BS and Yu SP. Modulation and genetic identification of the M channel. Prog Biophys Mol Biol 73: 135-166, 2000.
6. Brown DA. M currents. In: Ion Channels, edited by Narahashi T. New York: Plenum Press, 1988, vol. 1, p. 55-99.
7. Burbidge SA, Dalem TJ, Powellm AJ, Whitaker WR, Xie XM, Romanos MA, and Clare JJ. Molecular cloning, distribution and functional analysis of the NaV1.6 voltage-gated sodium channel from human brain. Brain Res Mol Brain Res 103: 80-90, 2002.
8. Cao YJ, Dreixler JC, Couey JJ, and Houamed KM. Modulation of recombinant and native neuronal SK channels by the neuroprotective drug riluzole. Eur J Pharmacol 449: 47-54, 2002.
9. 2+-dependent spike afterdepolarization and bursting in developing rat CA1 neurons. J Physiol 567: 79-93, 2005.
10. + channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J Physiol 559: 187-203,2004.
11. Costa PF, Ribeiro MA, and Santos AI. Afterpotential characteristics and firing patterns in maturing rat hippocampal CA1 neurones in in vitro slices. Brain Res Dev Brain Res 62: 263-272, 1991.
12. + channel. J Neurosci 24: 1236-1244, 2004.
13. Doerner D, Pitler TA, and Alger BE. Protein kinase C activators block specific calcium and potassium current components in isolated hippocampal neurons. J Neurosci 8: 4069-4078, 1988.
14. Fontana DJ, Inouye GT, and Johnson RM. Linopirdine (DuP 996) improves performance in several tests of learning and memory by modulation of cholinergic neurotransmission. Pharmacol Biochem Behav 49: 1075-1082, 1994.
15. French CR, Sah P, Buckett KJ, and Gage PW. A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95: 1139-1157, 1990.
16. Gasparini S and DiFrancesco D. Action of the hyperpolarization-activated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pfluegers Arch 435: 99-106, 1997.
17. Goldin AL. Diversity of mammalian voltage-gated sodium channels. Ann NY Acad Sci 868: 38-50, 1999.
18. Golding NL, Jung HY, Mickus T, and Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J Neurosci 19: 8789-8798, 1999.
19. Gu N, Vervaeke K, Hu H, and Storm JF. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization (mAHP) and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715, 2005.
20. Halliwell JV and Adams PR. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250: 71-92, 1982.
21. Harris KD, Hirase H, Leinekugel X, Henze DA, and Buzsáki G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32: 141-149, 2001.
22. Hodgkin AL and Katz B. The effect of sodium ions on the electrical activity of the giant axon of the squid. J Physiol 108: 37-77, 1949.
23. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997.
24. + current in rat hippocampal pyramidal cells. J Physiol 545: 783-805, 2002.
25. Jensen MS, Azouz R, and Yaari Y. Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium. J Neurophysiol 71: 831-839, 1994.
26. Jensen MS, Azouz R, and Yaari Y. Spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492: 199-210, 1996.
27. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, and Migliore M. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol 525: 75-81, 2000.
28. Madison DV and Nicoll RA. Control of repetitive discharge of rat CA1 pyramidal neurones in vitro. J Physiol 354: 319-331, 1984.
29. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998.
30. Magee JC and Carruth M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82: 1895-1901, 1999.
31. Main MJ, Cryan JE, Dupere JR, Cox B, Clare JJ, and Burbidge SA. Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol Pharmacol 58: 253-262, 2000.
32. Malenka RC, Madison DV, Andrade R, and Nicoll RA. Phorbol esters mimic some cholinergic actions in hippocampal pyramidal neurons. J Neurosci 6: 475-480, 1986.
33. Marrion NV. Control of M-current. Annu Rev Physiol 59: 483-504, 1997.
34. Otto T, Eichenbaum H, Wiener SI, and Wible CG. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1: 181-192, 1991.
35. Peters HC, Hu H, Pongs O, Storm JF, and Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 8: 51-60, 2005.
36. Pike FG, Meredith RM, Olding AW, and Paulsen O. Rapid report: postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J Physiol 518: 571-576, 1999.
37. Ranck JB Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41: 461-531, 1973.
38. + channels. Br J Pharmacol 137: 1173-1186, 2002.
39. Rundfeldt C and Netzer R. The novel anticonvulsant retigabine activates M-currents in Chinese hamster ovary-cells transfected with human KCNQ2/3 subunits. Neurosci Lett 282: 73-76, 2000.
40. 2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J Physiol 532: 205-216, 2001.
41. Schnee ME and Brown BS. Selectivity of linopirdine (DuP 996), a neuro-transmitter release enhancer in blocking voltage-dependent and calcium-activated potassium currents in hippocampal neurons. J Pharmacol Exp Ther 286: 709-717, 1998.
42. Schroeder BC, Hechenberger M, Weinreich F, Kubisch C, and Jentsch TJ. KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J Biol Chem 275: 24089-24095, 2000.
43. Shah M, Mistry M, Marsh SJ, Brown DA, and Delmas P. Molecular correlates of the M-current in cultured rat hippocampal neurons. J Physiol 544: 29-37, 2002.
44. Smith MR, Smith RD, Plummer NW, Meisler MH, and Goldin AL. Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18: 6093-6102, 1998.
45. Spruston N, Schiller Y, Stuart G, and Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268: 297-300, 1995.
46. Stefani A, Spadoni F, and Bernardi G. Differential inhibition by riluzole, lamotrigine, and phenytoin of sodium and calcium currents in cortical neurons: implications for neuroprotective strategies. Exp Neurol 147: 115-122, 1997.
47. Su H, Alroy G, Kirson ED, and Yaari Y. Extracellular calcium modulates persistent sodium current-dependent intrinsic bursting in rat hippocampal neurons. J Neurosci 27: 4173-4182, 2001.
48. 2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J Neurosci 22: 3645-3655, 2002.
49. Surges R, Freiman TM, and Feuerstein TJ. Input resistance is voltage dependent due to activation of Ih channels in rat CA1 pyramidal cells. J Neurosci Res 76: 475-480, 2004.
50. Tatulian L, Delmas P, Abogadie FC, and Brown DA. Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anticonvulsant drug retigabine. J Neurosci 21: 5535-5545, 2001.
51. Thomas MJ, Watabe AM, Moody TD, Makhinson M, and O'Dell TJ. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J Neurosci 18: 7118-7126, 1998.
52. Turner RW, Meyers DE, Richardson TL, and Barker JL. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. J Neurosci 11: 2270-2280, 1991.
53. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, and McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282: 1890-1893, 1998.
54. Wickenden AD, Yu W, Zou A, Jegla T, and Wagoner PK. Retigabine, a novel anti-convulsant, enhances activation of KCNQ2/Q3 potassium channels. Mol Pharmacol 58: 591-600, 2000.
55. Wong RK, Prince DA, and Basbaum AI. Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci USA 76: 986-990, 1979.
56. Wu SN and Li HF. Characterization of riluzole-induced stimulation of large-conductance calcium-activated potassium channels in rat pituitary GH3 cells. J Investig Med 47: 484-495, 1999.
57. Yaari Y, Hamon B, and Lux HD. Development of two types of calcium channels in cultured mammalian hippocampal neurons. Science 235: 680-682, 1987.
58. + channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J Neurosci 25: 9704-9720, 2005.
59. Yue C and Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24: 4614-4624, 2004.