Null mutation of the α4 nicotinic receptor subunit increases the propensity of muscarinic-mediated neuronal bursting in mouse hippocampal slices

Neuropharmacology

Volumn 51, Issue 3, 2006, Pages 587-596

  Reid, Christopher A ^a   Coleman, Harold A ^a   Finkelstein, David I ^a   Horne, Malcolm K ^a   Drago, John ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Alpha 4; Burst firing; Carbachol; Epileptiform; Knockout; Nicotinic receptors

Indexed keywords

CARBACHOL; MUSCARINIC RECEPTOR; NICOTINIC ALPHA 4 RECEPTOR; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; AMINO ACID RECEPTOR STIMULATING AGENT; CHOLINERGIC RECEPTOR STIMULATING AGENT; MUSCARINE; MUSCARINIC AGENT; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; EPILEPTIC DISCHARGE; EPILEPTIC NERVE CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GENE MUTATION; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTRACELLULAR RECORDING; KNOCKOUT MOUSE; MALE; MICROELECTRODE; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEIZURE SUSCEPTIBILITY; SPECIES COMPARISON; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; DRUG INTERACTION; ELECTROSTIMULATION; GENETICS; IN VITRO STUDY; METHODOLOGY; MOUSE MUTANT; PATCH CLAMP; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CARBACHOL; CHOLINERGIC AGONISTS; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, KNOCKOUT; MUSCARINE; MUSCARINIC AGONISTS; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; PYRAMIDAL CELLS; RECEPTORS, NICOTINIC;

EID: 33747066384     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2006.05.001     Document Type: Article

References (43)

1. Albuquerque E.X., Alkondon M., Pereira E.F., Castro N.G., Schrattenholz A., Barbosa C.T., Bonfante-Cabarcas R., Aracava Y., Eisenberg H.M., and Maelicke A. Properties of neuronal nicotinic acetylcholine receptors: pharmacological characterization and modulation of synaptic function. J. Pharmacol. Exp. Ther. 280 (1997) 1117-1136
2. Alkondon M., and Albuquerque E.X. Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J. Pharmacol. Exp. Ther. 265 (1993) 1455-1473
3. Alkondon M., and Albuquerque E.X. Nicotinic acetylcholine receptor α7 and α4β2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J. Neurophysiol. 86 (2001) 3043-3055
4. A receptors in hippocampal neurons. Mol. Pharmacol. 59 (2001) 814-824
5. Barbarosie M., and Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J. Neurosci. 17 (1997) 9308-9314
6. Bertrand S., Weiland S., Berkovic S.F., Steinlein O.K., and Bertrand D. Properties of neuronal nicotinic acetylcholine receptor mutants from humans suffering from autosomal dominant nocturnal frontal lobe epilepsy. Br. J. Pharmacol. 125 (1998) 751-760
7. Bertrand D., Picard F., Le Hellard S., Weiland S., Favre I., Phillips H., Bertrand S., Berkovic S.F., Malafosse A., and Mulley J. How mutations in the nAChRs can cause ADNFLE epilepsy. Epilepsia 43 Suppl. 5 (2002) 112-122
8. Bianchi R., and Wong R.K.S. Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro. J. Neurophysiol. 72 (1994) 131-138
9. Caraiscos V.B., Elliott E.M., You-Ten K.E., Cheng V.Y., Belelli D., Newell J.G., Jackson M.F., Lambert J.J., Rosahl T.W., Wafford K.A., MacDonald J.F., and Orser B.A. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by α5 subunit-containing γ-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. USA 101 (2004) 3662-3667
10. Cobb S.R., Bulters D.O., Suchak S., Riedel G., Morris R.G., and Davies C.H. Activation of nicotinic acetylcholine receptors patterns network activity in the rodent hippocampus. J. Physiol. 518 (1999) 131-140
11. h is necessary for patterning of mGluR and mAChR induced network activity in the hippocampal CA3 region. Neuropharmacology 44 (2003) 293-303
12. Fabian-Fine R., Skehel P., Errington M.L., Davies H.A., Sher E., Stewart M.G., and Fine A. Ultrastructural distribution of the α7 nicotinic acetylcholine receptor subunit in rat hippocampus. J. Neurosci. 21 (2001) 7993-8003
13. Figl A., Viseshakul N., Shafaee N., Forsayeth J., and Cohen B.N. Two mutations linked to nocturnal frontal lobe epilepsy cause use-dependent potentiation of the nicotinic ACh response. J. Physiol. 513 (1998) 655-670
14. Fisahn A., Pike F.G., Buhl E.H., and Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394 (1998) 186-189
15. Fischer Y. The hippocampal intrinsic network oscillator. J. Physiol. 554 (2004) 156-174
16. * nicotinic receptors. J. Neurosci. 25 (2005) 11396-11411
17. A receptor in the pilocarpine model of temporal lobe epilepsy. Hippocampus 13 (2003) 633-645
18. Ji D., and Dani J.A. Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J. Neurophysiol. 83 (2000) 2682-2690
19. 2+ permeability, conductance, and gating of human α4β2 nicotinic acetylcholine receptors. J. Neurosci. 17 (1997) 9035-9047
20. Kuzmiski J.B., and MacVicar B.A. Cyclic nucleotide-gated channels contribute to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons. J. Neurosci. 21 (2001) 8707-8714
21. Kuzmiski J.B., Barr W., Zamponi G.W., and MacVicar B.A. Topiramate inhibits the initiation of plateau potentials in CA1 neurons by depressing R-type calcium channels. Epilepsia 46 (2005) 481-489
22. MacVicar B.A., and Tse F.W.Y. Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices. J. Physiol. 417 (1989) 197-212
23. Maggi L., Sher E., and Cherubini E. Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J. Physiol. 536 (2001) 89-100
24. Matsushima N., Hirose S., Iwata H., Fukuma G., Yonetani M., Nagayama C., Hamanaka W., Matsunaka Y., Ito M., Kaneko S., Mitsudome A., and Sugiyama H. Mutation (Ser284Leu) of neuronal nicotinic acetylcholine receptor α4 subunit associated with frontal lobe epilepsy causes faster desensitization of the rat receptor expressed in oocytes. Epilepsy Res. 48 (2002) 181-186
25. McColl C.D., Horne M.K., Finkelstein D.I., Wong J.Y., Berkovic S.F., and Drago J. Electroencephalographic characterisation of pentylenetetrazole-induced seizures in mice lacking the alpha 4 subunit of the neuronal nicotinic receptor. Neuropharmacology 44 (2003) 234-243
26. McMahon L.L., Williams J.H., and Kauer J.A. Functionally distinct groups of interneurons identified during rhythmic carbachol oscillations in hippocampus in vitro. J. Neurosci. 18 (1998) 5640-5651
27. Nagao T., Alonso A., and Avoli M. Epileptiform activity induced by pilocarpine in the rat hippocampal-entorhinal slice preparation. Neuroscience 72 (1996) 399-404
28. 2+-activated non-selective cation channels in rat hippocampal neurones in vitro. J. Physiol. 521 (1999) 617-627
29. Reid C.A., and Clements J.D. Postsynaptic expression of long-term potentiation in the rat dentate gyrus demonstrated by variance-mean analysis. J. Physiol. 518 (1999) 121-130
30. Ross S.A., Wong J.Y., Clifford J.J., Kinsella A., Massalas J.S., Horne M.K., Scheffer I.E., Kola I., Waddington J.L., Berkovic S.F., and Drago J. Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J. Neurosci. 20 (2000) 6431-6441
31. 2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol. 532 (2001) 205-216
32. Sansig G., Bushell T.J., Clarke V.R.J., Rozov A., Burnashev N., Portet C., Gasparini F., Schmutz M., Klebs K., Shigemoto R., Flor P.J., Kuhn R., Knoepfel T., Schroeder M., Hampson D.R., Collett V.J., Zhang C., Duvoisin R.M., Collingridge G.L., and van der Putten H. Increased seizure susceptibility in mice lacking metabotropic glutamate receptor 7. J. Neurosci. 21 (2001) 8734-8745
33. Schiller Y. Activation of a calcium-activated cation current during epileptiform discharges and its possible role in sustaining seizure-like events in neocortical slices. J. Neurophysiol. 92 (2004) 862-872
34. A conductances in hippocampal neurons. J. Neurosci. 22 (2002) RC223, 1-5
35. Su H., Alroy G., Kirson E.D., and Yaari Y. Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J. Neurosci. 21 (2001) 4173-4182
36. 2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J. Neurosci. 22 (2002) 3645-3655
37. Sudweeks S.N., and Yakel J.L. Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J. Physiol. 527 (2000) 515-528
38. Traub R.D., Miles R., and Buzsáki G. Computer simulation of carbachol-driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus. J. Physiol. 451 (1992) 653-672
39. Williams J.H., and Kauer J.A. Properties of carbachol-induced oscillatory activity in rat hippocampus. J. Neurophysiol. 78 (1997) 2631-2640
40. Wong R.K., and Traub R.D. Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J. Neurophysiol. 49 (1983) 442-458
41. Wong J.Y., Ross S.A., McColl C., Massalas J.S., Powney E., Finkelstein D.I., Clark M., Horne M.K., Berkovic S.F., and Drago J. Proconvulsant-induced seizures in alpha(4) nicotinic acetylcholine receptor subunit knockout mice. Neuropharmacology 43 (2002) 55-64
42. Yue C., and Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 24 (2004) 4614-4624
43. Zoli M., Lena C., Picciotto M.R., and Changeux J.P. Identification of four classes of brain nicotinic receptors using β2 mutant mice. J. Neurosci. 18 (1998) 4461-4472