Cholinergic control of firing pattern and neurotransmission in rat neostriatal projection neurons: Role of CaV2.1 and CaV2.2 Ca2+ channels

Journal of Neurophysiology

Volumn 93, Issue 5, 2005, Pages 2507-2519

  Perez Rosello, Tamara ^a   Figueroa, Alejandra ^a   Salgado, Humberto ^a   Vilchis, Carmen ^a   Tecuapetla, Fatuel ^a   Guzman, Jaime N ^a   Galarraga, Elvira ^a   Bargas, Jose ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CALCIUM; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; MUSCARINE; MUSCARINIC AGENT; MUSCARINIC M1 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC RECEPTOR BLOCKING AGENT; VOLTAGE GATED CALCIUM CHANNEL;

4 AMINOBUTYRIC ACID RELEASE; AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CHOLINERGIC ACTIVITY; CHOLINERGIC SYSTEM; CONTROLLED STUDY; GABAERGIC SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MODULATION; NEOSTRIATUM; NERVE CELL; NERVE FIBER; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC INHIBITION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CALCIUM CHANNEL BLOCKERS; CAVEOLIN 2; CAVEOLINS; CELLS, CULTURED; DRUG INTERACTIONS; ELECTRIC STIMULATION; MALE; MEMBRANE POTENTIALS; MUSCARINE; MUSCARINIC AGONISTS; NEOSTRIATUM; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; SYNAPTIC TRANSMISSION;

EID: 17644413790     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00853.2004     Document Type: Article

References (74)

1. 2+ current in rat magnocellular cholinergic basal forebrain neurones. J Physiol 466: 173-189, 1993.
2. 2+-activated outward currents in neostriatal neurons. Neuroscience 88: 479-488, 1999.
3. 2+ currents in acutely-isolated, adult rat neostriatal neurons. J Neurosci 14: 6667-6686, 1994.
4. 2+ channels. Brain Res Bull 49: 285-289, 1999.
5. Bernard V, Normand E, and Bloch B. Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes. J Neurosci 12: 3591-3600, 1992.
6. 2+ current and M current in rat sympathetic neurons. Proc Natl Acad Sci USA 89: 9544-9548, 1992.
7. Bolam JP, Wainer BH, and Smith AD. Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy. Neuroscience 12: 711-718, 1984.
8. Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G, and Bernardi G. Synaptic transmission in the striatum: from plasticity to neurodegeneration. Prog Neurobiol 61: 231-265, 2000.
9. 1-like muscarinic receptors and PKC activation. Eur J Neurosci 10: 2887-2895, 1998.
10. 2+ channels and their role in neurotransmitter release. Cell Calcium 24: 307-323, 1998.
11. Caulfield MP and Birdsall NJM. International union pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50: 279-290, 1998.
12. Chameau P, Van de Vrede Y, Fossier P, and Baux G. Ryanodine-, IP3- and NAADP-dependent calcium stores control acetylcholine release. Pfluegers Arch 443: 289-296, 2001.
13. 4 muscarinic receptor activation modulates calcium channel currents in rat intracardiac neurons. J Neurophysiol 78: 1903-1912, 1997.
14. Currie KP and Fox AP. Differential facilitation of N- and P/Q-type calcium channels during trains of action potential-like waveforms. J Physiol 539: 419-431, 2002.
15. Figueroa A, Galarraga E, and Bargas J. Muscarinic receptors involved in the subthreshold cholinergic actions of neostriatal spiny neurons. Synapse 46: 215-223, 2002.
16. Galarraga E, Bargas J, Sierra A, and Aceves J. The role of calcium in the repetitive firing of neostriatal neurons. Exp Brain Res 75: 157-168, 1989.
17. Galarraga E, Hernández-López S, Reyes A, Miranda I, Bermudez-Rattoni F, Vilchis C, and Bargas J. Cholinergic modulation of neostriatal output: a functional antagonism between different types of muscarinic receptors. J Neurosci 19: 3629-3638, 1999.
18. Guzman JN, Hernandez A, Galarraga E, Tapia D, Laville A, Vergara R, Aceves J, and Bargas J. Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum. J Neurosci 23: 8931-8940, 2003.
19. Harsing LG and Zigmond MJ. Postsynaptic integration of cholinergic and dopaminergic signals on medium-sized GABAergic projection neurons in the neostriatum. Brain Res Bull 45: 607-613, 1998.
20. Hasselmo ME and McGaughy J. High acetylcholine levels set circuit dynamics for attention and encoding and low levels set dynamics for consolidation. Prog Brain Res 145: 207-231, 2004.
21. Hernandez-Echeagaray E, Galarraga E, and Bargas J. 3-α-Chloro- imperialine, a potent blocker of cholinergic presynaptic modulation of glutamatergic afferents in the rat neostriatum. Neuropharmacology 37: 1493-1502, 1998.
22. 3-calcineurin-signaling cascade. J Neurosci 20: 8987-8995, 2000.
23. Hersch SM and Levey AI. Diverse pre- and post-synaptic expression of ml-m4 muscarinic receptor proteins in neurons and afferents in the rat neostriatum. Life Sci 56: 931-938, 1995.
24. 2+ currents in rat striatal neurons through parallel pathways. J Neurosci 15: 458-469, 1995.
25. 1-like muscarinic receptors. Neuroscience 73: 751-760, 1996.
26. Iwasaki S, Momiyama A, Uchitel OD, and Takahashi T. Developmental changes in calcium channel types mediating central synaptic transmission. J Neurosci 20: 59-65, 2000.
27. Jerusalinsky D, Cervenasky C, Pena C, Raskovsky S, and Dajas F. Two polypeptides from Dendroaspis angusticeps venom selectively inhibit the binding of central muscarinic cholinergic receptor ligands. Neurochem Int 20: 237-246, 1992.
28. Jerusalinsky D and Harvey AL. Toxins from mamba venoms: small proteins with selectivities for different subtypes of muscarinic acetylcholine receptors. Trends Pharmacol Sci 15: 424-433, 1994.
29. Jones SVP. Muscarinic receptors subtypes: modulation of ion channels. Life Sci 52: 457-464, 1993.
30. Karlsson E, Jolkkonen M, Mulugeta E, Onali P, and Adem A. Snake toxins with high selectivity for subtypes of muscarinic acetylcholine receptors. Biochimie 82: 793-806, 2000.
31. 3HGABA release in the rat substantia nigra through muscarinic receptors localized on striatonigral terminals. Neuroscience 63: 989-1002, 1994.
32. Kimura F and Baughman RW. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses in cortical neurons. J Neurophysiol 77: 709-716, 1997.
33. Kornisiuk E, Sanchez G, Cerveñansky C, Duran R, and Jerusalinsky D. Muscarinic toxins and their actions on muscarinic inhibition of adenylyl cyclase activity. J Neurochem 78, Suppl 1: BP18-BP37, 2001.
34. 3H]GABA release from striatal slices by presynaptic autoreceptor. J Neurochem 42: 943-950, 1984.
35. Liu L and Rittenhouse AR. Pharmacological discrimination between muscarinic receptor signal transduction cascades with bethanechol chloride. Br J Pharmacol 138: 1259-1270, 2003.
36. Marino MJ, Rouse ST, Levey AI, Potter LT, and Conn PJ. Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci USA 95: 11465-11470, 1998.
37. 2+ channels reconstituted in a human cell line. J Physiol 532: 337-347, 2001.
38. Misgeld U, Calabresi P, and Dodt HU. Muscarinic modulation of calcium dependent potentials in rat neostriatal neurons. Pfluegers Arch 407: 482-487, 1986.
39. Momiyama T. Dopamine receptors and calcium channels regulating striatal inhibitory synaptic transmission. Nippon Yakurigaku Zasshi 120: 61P-63P, 2002.
40. 2+ channels to reduce GABA release onto rat striatal cholinergic interneurones. J Physiol 533: 479-492, 2001.
41. Murai Y, Ishibashi H, Akaike N, and Ito Y. Acetylcholine modulation of high-voltage-activated calcium channels in the neurones acutely dissociated from rat paratracheal ganglia. Br J Pharmacol 123: 1441-1449, 1998.
42. Murakami N, Ishibashi H, Katsurabayashi S, and Akaike N. Calcium channel subtypes on single GABAergic presynaptic terminal projecting to rat hippocampal neurons. Brain Res 951: 121-129, 2002.
43. Olianas MC, Adem A, Karlsson E, and Onali P. Rat striatal muscarinic receptors coupled to the inhibition of adenylyl cyclase activity: potent block by the selective m4 ligand muscarinic toxin 3 (MT3). Br J Pharmacol 118: 283-288, 1996.
44. Olson PA, Platzer J, Streissnig J, Miller RJ, and Surmeier DJ. Cav 1.3 channels are primary determinants of L-type calcium currents in striatal medium spiny neurons. Soc Neurosci Abstr 31: 67.12, 2001.
45. 2+ channels in the repetitive firing of striatal projection neurons. Neuroreport 14: 1253-1256. 2003.
46. 2+ currents in neostriatal projection neurons. Soc Neurosci Abstr 30: 740.5, 2000.
47. V2.2 currents of neostriatal projection neurons. Soc Neurosci Abstr 33: 705.4, 2003.
48. 1 type muscarinic receptors via a Gq11/ PLC/DAG/PKC signaling cascade. Soc Neurosci Abstr 34: 593.1, 2004.
49. Pineda JC, Bargas J, Flores-Hernández J, and Galarraga E. Muscarinic receptors modulate the afterhyperpolarizing potential in neostriatal neurons. Eur J Pharmacol 281: 271-277, 1995.
50. Pineda JC, Galarraga E, Bargas J, Cristancho M, and Aceves J. Charybdotoxin and apamin sensitivity of the calcium-dependent repolarization and the afterhyperpolarization in neostriatal neurons. J Neurophysiol 68: 287-294, 1992.
51. Potter LT, Flynn DD, Liang JS, and McCollum MH. Studies of muscarinic neurotransmission with antimuscarinic toxins. Prog Brain Res 145: 121-128, 2004.
52. Purkerson SL and Potter LT. Use of antimuscarinic toxins to facilitate studies of striatal muscarinic receptors. J Pharmacol Exp Ther 284: 707-713, 1998.
53. Raiteri M, Marchi M, Paudice P, and Pittaluga A. Muscarinic receptors mediating inhibition of γ-aminobutyric acid release in rat corpus striatum and their pharmacological characterization. J Pharmacol Exp Ther 254: 496-550, 1990.
54. Rakhilin SV, Olson PA, Nishi A, Starkova NN, Fienberg AA, Nairn AC, Surmeier DJ, and Greengard P. A network of control mediated by regulator of calcium/calmodulin-dependent signaling. Science 306: 698-701, 2004.
55. Reuter H. Diversity and function of presynaptic calcium channels in the brain. Curr Opin Neurobiol 6: 331-337, 1996.
56. Rhee JS, Ishibashi H, and Akaike N. Calcium channels in the GABAergic presynaptic nerve terminals projecting to Meynert neurons of the rat. J Neurochem 72: 800-807, 1999.
57. 2+ channels by using knockout mice. Proc Natl Acad Sci USA 96: 10899-10904, 1999.
58. Smolders I, Bogaert L, Ebinger G, and Michotte Y. Muscarinic modulation of striatal dopamine, glutamate, and GABA release, as measured with in vivo microdialysis. J Neurochem. 68: 1942-1948, 1997.
59. Sugita S, Uchimura N, Jiang ZG, and North RA. Distinct muscarinic receptors inhibit release of gamma-aminobutyric acid and excitatory amino acids in mammalian brain. Proc Natl Acad Sci USA 88: 2608-2611, 1991.
60. Tan Y, Hori N, and Carpenter DO. The mechanism of presynaptic long-term depression mediated by group I metabotropic glutamate receptors. Cell Mol Neurobiol 23: 187-203, 2003.
61. Tecuapetla F, Carrillo-Reid L, Guzmán JN, Galarraga E, and Bargas J. Different inhibitory inputs onto neostriatal projection neurons as revealed by field stimulation. J Neurophysiol 93: 1119-1126, 2005.
62. Urbano FJ, Rosato-Siri MD, and Uchitel OD. Calcium channels involved in neurotransmitter release at adult, neonatal and P/Q-type deficient neuromuscular junctions. Mol Membr Biol 19: 293-300, 2002.
63. Vilaro MT, Wiederhold KH, Palacios JM, and Mengod G. Muscarinic cholinergic receptors in the rat caudate-putamen and olfactory tubercle belong predominantly to the m4 class: in situ hybridization and receptor autoradiography evidence. Neuroscience 40: 159-167, 1991.
64. + currents in neostriatal neurons. Neuroscience 95: 745-752, 2000.
65. 2+ currents in neostriatal neurons. Neuroscience 109: 555-567, 2002.
66. Volpicelli LA and Levey AI. Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog Brain Res 145: 59-66, 2004.
67. 2+ currents in rat sensory neurons: channel and receptor types, dose-response relationships and cross-talk pathways. Eur J Neurosci 6: 381-391, 1994.
68. 2+ channels in supporting hippocampal synaptic transmission. Science 264: 107-111, 1994.
69. Wickens JR and Oorschot DE. Neural dynamics and surround inhibition in the neostriatum: a possible connection. In: Brain Dynamics and the Striatal Complex, edited by Miller R and Wickens JR. Amsterdam: Hardwood Academic, 2000, p. 141-149.
70. Wu LG and Saggau P. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J Neurosci 14: 5613-5622, 1994.
71. Yan Z, Flores-Hernández J, and Surmeier DJ. Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons. Neuroscience 103: 1017-1024, 2001.
72. 2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane-delimited, G-protein pathway. J Neurosci 16: 2592-2604, 1996.
73. Yang F, He X, Feng L, Mizuno K, Liu XW, Russell J, Xiong WC, and Lu B. PI-3 kinase and IP3 are both necessary and sufficient to mediate NT3-induced synaptic potentiation. Nat Neurosci 4: 19-28, 2001.
74. Zhou FM, Wilson C, and Dani JA. Muscarinic and nicotinic cholinergic mechanisms in the mesostriatal dopamine systems. Neuroscientist 9: 23-36, 2003.