Atropine-sensitive hippocampal theta oscillations are mediated by Cav2.3 R-type Ca2+ channels

Neuroscience

Volumn 205, Issue , 2012, Pages 125-139

  Muller R ^a   Struck, H ^a   Ho, M S P ^a   Brockhaus Dumke, A ^a,b   Klosterkotter J ^a   Broich, K ^c   Hescheler, J ^a   Schneider, T ^a   Weiergraber M ^a,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b University of Cologne ^*  (Germany)

^c FEDERAL INSTITUTE FOR DRUGS AND MEDICAL DEVICES   (Germany)

Author keywords

Calcium; Cognition; Theta

Indexed keywords

ATROPINE; PHOSPHOLIPASE C BETA1; PHOSPHOLIPASE C BETA4; UNCLASSIFIED DRUG; URETHAN; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV2.3;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; FREQUENCY MODULATION; GENETIC VARIABILITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; MOLECULAR DYNAMICS; MOUSE; NEUROMODULATION; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TELEMETRY; TEMPORAL LOBE;

ANIMALS; ATROPINE; BIOLOGICAL CLOCKS; CALCIUM CHANNELS, R-TYPE; CATION TRANSPORT PROTEINS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; THETA RHYTHM;

EID: 84858002841     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.12.032     Document Type: Article

References (80)

1. Abe Y., Toyosawa K. Age-related changes in rat hippocampal theta rhythms: a difference between type 1 and type 2 theta. J Vet Med Sci 1999, 61:543-548.
2. 2+ channels by G(alpha)q/11-coupled muscarinic receptors. Mol Pharmacol 2004, 65:381-388.
3. Beier S.M., Barish M.E. Cholinergic stimulation enhances cytosolic calcium ion accumulation in mouse hippocampal CA1 pyramidal neurones during short action potential trains. J Physiol 2000, 526:129-142.
4. Bland B.H., Colom L.V. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 1993, 41:157-208.
5. Borhegyi Z., Varga V., Szilágyi N., Fabo D., Freund T.F. Phase segregation of medial septal GABAergic neurons during hippocampal theta activity. J Neurosci 2004, 24:8470-8479.
6. Brown D.A. Muscarinic acetylcholine receptors (mAChRs) in the nervous system: some functions and mechanisms. J Mol Neurosci 2010, 41:340-346.
7. + current in a vertebrate neurone. Nature 1980, 283:673-676.
8. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
9. Buzsaki G., Buhl D.L., Harris K.D., Csicsvari J., Czéh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 2003, 116:201-211.
10. 2+ dynamics of inhibitory interneurons in the rat visual cortex. J Neurophysiol 2010, 104:840-853.
11. 2+ influx. J Neurophysiol 1995, 73:2553-2557.
12. 1 signaling. J Neurosci 2001, 21:6387-6394.
13. Colino A., Halliwell J.V. Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur J Neurosci 1993, 5:1198-1209.
14. Colom L.V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. J Neurochem 2006, 96:609-623.
15. Fisahn A., Yamada M., Duttaroy A., Gan J.W., Deng C.X., McBain C.J., Wess J. Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 2002, 33:615-624.
16. Gahwiler B.H., Brown D.A. Muscarine affects calcium-currents in rat hippocampal pyramidal cells in vitro. Neurosci Lett 1987, 76:301-306.
17. Gillies M.J., Traub R.D., LeBeau F.E., Davies C.H., Gloveli T., Buhl E.H., Whittington M.A. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 2002, 543:779-793.
18. Goutagny R., Jackson J., Williams S. Self-generated theta oscillations in the hippocampus. Nat Neurosci 2009, 12:1491-1493.
19. Halliwell J.V., Adams P.R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 1982, 250:71-92.
20. Hangya B., Borhegyi Z., Szilágyi N., Freund T.F., Varga V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J Neurosci 2009, 29:8094-8102.
21. Hara K., Harris R.A. The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 2002, 94:313-318.
22. Henke H., Lang W. Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non-neurological and senile dementia of Alzheimer-type patients. Brain Res 1983, 267:281-291.
23. Hochberg Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika 1988, 75:800-802.
24. 2+-sensitivity of synaptic plasticity in apical dendrites of hippocampal CA1 pyramidal cells. J Neurophysiol 2002, 87:1169-1174.
25. Kahana M.J., Seelig D., Madsen J.R. Theta returns. Curr Opin Neurobiol 2001, 11:739-744.
26. Kamatchi G.L., Franke R., Lynch C., Sando J.J. Identification of sites responsible for potentiation of type 2.3 calcium currents by acetyl-beta-methylcholine. J Biol Chem 2004, 279:4102-4109.
27. Kamondi A., Acsády L., Wang X.J., Buzsáki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 1998, 8:244-261.
28. Kar S., Slowikowski S.P., Westaway D., Mount H.T. Interactions between beta-amyloid and central cholinergic neurons: implications for Alzheimer's disease. J Psychiatry Neurosci 2004, 29:427-441.
29. 2+ channel activity. Eur J Neurosci 2004, 19:2659-2668.
30. Kohler C., Chan-Palay V., Wu J.Y. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat Embryol (Berl) 1984, 169:41-44.
31. Kronland-Martinet R., Morlet J., Grossman A. Analysis of sound patterns through wavelet transform. Int J Pattern Recognit Artif Intell 1987, 1(2):273-302.
32. Krzywkowski P., De Bilbao F., Senut M.C., Lamour Y. Age-related changes in parvalbumin- and GABA-immunoreactive cells in the rat septum. Neurobiol Aging 1995, 16:29-40.
33. Kuzmiski J.B., Barr W., Zamponi G.W., MacVicar B.A. Topiramate inhibits the initiation of plateau potentials in CA1 neurons by depressing R-type calcium channels. Epilepsia 2005, 46:481-489.
34. Lee S.C., Choi S., Lee T., Kim H.L., Chin H., Shin H.S. Molecular basis of R-type calcium channels in central amygdala neurons of the mouse. Proc Natl Acad Sci U S A 2002, 99:3276-3281.
35. 2+ channel activity depends on an arginine rich region in the cytosolic II-III loop. Eur J Neurosci 2003, 18:841-855.
36. Leung L.W., Yim C.Y. Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 1991, 553:261-274.
37. Levey A.I., Edmunds S.M., Koliatsos V., Wiley R.G., Heilman C.J. Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 1995, 15:4077-4092.
38. 2+ channel family. Neuron 2003, 39:951-960.
39. Madison D.V., Lancaster B., Nicoll R.A. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 1987, 7:733-741.
40. Magee J.C., Carruth M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 1999, 82:1895-1901.
41. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol (Lond) 1995, 487:67-90.
42. Manseau F., Goutagny R., Danik M., Williams S. The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: an investigation using a complete septohippocampal preparation in vitro. J Neurosci 2008, 28:4096-4107.
43. McNamara R.K., Wees E.A., Lenox R.H. Differential subcellular redistribution of protein kinase C isozymes in the rat hippocampus induced by kainic acid. J Neurochem 1999, 72:1735-1743.
44. Mehrke G., Pereverzev A., Grabsch H., Hescheler J., Schneider T. Receptor-mediated modulation of recombinant neuronal class E calcium channels. FEBS Lett 1997, 408:261-270.
45. 1. J Neurosci 2000, 20:7167-7173.
46. 1E Ca channels by distinct signaling pathways coupled to M2 muscarinic acetylcholine receptors. J Neurosci 1999, 19:6806-6817.
47. Miller J.W., Turner G.M., Gray B.C. Anticonvulsant effects of the experimental induction of hippocampal theta activity. Epilepsy Res 1994, 18:195-204.
48. Montgomery S.M., Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci U S A 2007, 104:14495-14500.
49. 2+ changes in hippocampal neurons. Neuron 1991, 6:901-905.
50. 2+ signalling in postsynaptic dendrites and spines of mammalian neurons in brain slice. J Physiol Paris 1992, 86:57-66.
51. Naik M.U., Benedikz E., Hernandez I., Libien J., Hrabe J., Valsamis M., Dow-Edwards D., Osman M., Sacktor T.C. Distribution of protein kinase Mzeta and the complete protein kinase C isoform family in rat brain. J Comp Neurol 2000, 426:243-258.
52. Rouse S.T., Marino M.J., Potter L.T., Conn P.J., Levey A.I. Muscarinic receptor subtypes involved in hippocampal circuits. Life Sci 1999, 64:501-509.
53. Sabatini B.L., Svoboda K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 2000, 408:589-593.
54. Sceniak M.P., Maciver M.B. Cellular actions of urethane on rat visual cortical neurons in vitro. J Neurophysiol 2006, 95:3865-3874.
55. + channel activity in sympathetic neurons. Life Sci 2001, 68:2481-2487.
56. Shapiro M.S., Loose M.D., Hamilton S.E., Nathanson N.M., Gomeza J., Wess J., Hille B. Assignment of muscarinic receptor subtypes mediating G-protein modulation of Ca(2+) channels by using knockout mice. Proc Natl Acad Sci U S A 1999, 96:10899-10904.
57. Shin J., Gireesh G., Kim S.W., Kim D.S., Lee S., Kim Y.S., Watanabe M., Shin H.S. Phospholipase C beta 4 in the medial septum controls cholinergic theta oscillations and anxiety behaviors. J Neurosci 2009, 29:15375-15385.
58. Shin J., Kim D., Bianchi R., Wong R.K., Shin H.S. Genetic dissection of theta rhythm heterogeneity in mice. Proc Natl Acad Sci U S A 2005, 102:18165-18170.
59. 2+ currents in rat CA1 hippocampal pyramidal neurons. Neuroscience 2003, 116:629-638.
60. 1E calcium channel subunit underlies R-type calcium current in hippocampal and cortical pyramidal neurons. J Physiol 2002, 542:699-710.
61. 2+ channel currents in rat sensorimotor pyramidal cells via two distinct pathways. J Neurophysiol 1999, 81:72-84.
62. Suzuki T., Delgado-Escueta A.V., Aguan K., Alonso M.E., Shi J., Hara Y., Nishida M., Numata T., Medina M.T., Takeuchi T., Morita R., Bai D., Ganesh S., Sugimoto Y., Inazawa J., Bailey J.N., Ochoa A., Jara-Prado A., Rasmussen A., Ramos-Peek J., Cordova S., Rubio-Donnadieu F., Inoue Y., Osawa M., Kaneko S., Oguni H., Mori Y., Yamakawa K. Mutations in EFHC1 cause juvenile myoclonic epilepsy. Nat Genet 2004, 36:842-849.
63. Tai C., Kuzmiski J.B., MacVicar B.A. Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons. J Neurosci 2006, 26:6249-6258.
64. Takano Y., Hanada Y. The driving system for hippocampal theta in the brainstem: an examination by single neuron recording in urethane-anesthetized rats. Neurosci Lett 2009, 455:65-69.
65. Tang F.R., Lee W.L., Gao H., Chen Y., Loh Y.T., Chia S.C. Expression of different isoforms of protein kinase C in the rat hippocampus after pilocarpine-induced status epilepticus with special reference to CA1 area and the dentate gyrus. Hippocampus 2004, 14:87-98.
66. Timmermann D.B., Westenbroek R.E., Schousboe A., Catterall W.A. Distribution of high-voltage-activated calcium channels in cultured gamma-aminobutyric acidergic neurons from mouse cerebral cortex. J Neurosci Res 2002, 67:48-61.
67. Tsubokawa H., Ross W.N. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 1997, 17:5782-5791.
68. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 1969, 26:407-418.
69. Varga V., Hangya B., Kránitz K., Ludányi A., Zemankovics R., Katona I., Shigemoto R., Freund T.F., Borhegyi Z. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J Physiol 2008, 586:3893-3915.
70. Vilaro M.T., Mengod G., Palacios G., Palacios J.M. Receptor distribution in the human and animal hippocampus: focus on muscarinic acetylcholine receptors. Hippocampus 1993, 3:149-156.
71. Weiergraber M., Henry M., Hescheler J., Smyth N., Schneider T. Electrocorticographic and deep intracerebral EEG recording in mice using a telemetry system. Brain Res Brain Res Protoc 2005, 14:154-164.
72. v2.3 deficient mice. Mol Cell Neurosci 2008, 39:605-618.
73. 2+ channel. Epilepsia 2006, 47:839-850.
74. v2.3 E/R-type voltage-gated calcium channel. J Neurophysiol 2007, 97:3660-3669.
75. v2.3 voltage-gated calcium channel in epileptogenesis. Shedding new light on an enigmatic channel. Neurosci Biobehav Rev 2006, 30:1122-1144.
76. Wilson S.M., Toth P.T., Oh S.B., Gillard S.E., Volsen S., Ren D., Philipson L.H., Lee E.C., Fletcher C.F., Tessarollo L., Copeland N.G., Jenkins N.A., Miller R.J. The status of voltage-dependent calcium channels in alpha1E knock-out mice. J Neurosci 2000, 20:8566-8571.
77. Yamaguchi Y., Kawashima S. Effects of amyloid-beta-(25-35) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat. Eur J Pharmacol 2001, 412:265-272.
78. Yasuda R., Sabatini B.L., Svoboda K. Plasticity of calcium channels in dendritic spines. Nat Neurosci 2003, 6:948-955.
79. v2.3 channels are critical for oscillatory burst discharges in the reticular thalamus and absence epilepsy. Neuron 2011, 70:95-108.
80. Zhang H., Lin S.C., Nicolelis M.A. Spatiotemporal coupling between hippocampal acetylcholine release and theta oscillations in vivo. J Neurosci 2010, 30:13431-13440.