Blockade of different muscarinic receptor subtypes changes the equilibrium between excitation and inhibition in rat visual cortex

Neuroscience

Volumn 169, Issue 4, 2010, Pages 1610-1620

  Amar, M ^a   Lucas Meunier, E ^a   Baux, G ^a   Fossier, P ^a  

^a LABORATOIRE DE NEUROBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

Author keywords

Acetylcholine; Cortical network; M1 M2 M3 M4 M5 muscarinic receptors; Pyramidal neuron

Indexed keywords

ACETYLCHOLINE; GLUTAMIC ACID; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CHOLINERGIC NERVE; CONDUCTANCE; CONTROLLED STUDY; GABAERGIC SYSTEM; INTERNEURON; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE EXCITABILITY; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VISUAL CORTEX;

EID: 77955421141     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.06.019     Document Type: Article

References (70)

1. Aramakis V.B., Bandrowski A.E., Ashe J.H. Activation of muscarinic receptors modulates NMDA receptor-mediated responses in auditory cortex. Exp Brain Res 1997, 113(3):484-496.
2. Aramakis V.B., Metherate R. Nicotine selectively enhances NMDA receptor-mediated synaptic transmission during postnatal development in sensory neocortex. J Neurosci 1998, 18:8485-8495.
3. Bannister A.P. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci Res 2005, 53:95-103.
4. Benardo L.S., Prince D.A. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 1982, 249(2):315-331.
5. Billard W., Binch H., Crosby G., McQuade R.D. Identification of the primary muscarinic autoreceptor subtype in rat striatum as m2 through a correlation of in vivo microdialysis and in vitro receptor binding data. J Pharmacol Exp Ther 1995, 273(1):273-279.
6. Blin N., Yun J., Wess J. Mapping of single amino acid residues required for selective activation of Gq/11 by the m3 muscarinic acetylcholine receptor. J Biol Chem 1995, 270(30):17741-17748.
7. Bonner T.I., Buckley N.J., Young A.C., Brann M.R. Identification of a family of muscarinic acetylcholine receptor genes. Science 1987, 237(4814):527-532. Erratum in: Science (1987) 237(4822):237.
8. Buckley N.J., Bonner T.L., Brann M.R. Localization of a family of muscarinic receptor mRNAs in rat brain. J Neurosci 1988, 8:4646-4652.
9. Caulfield M.P. Muscarinic receptors-characterization, coupling and function. Pharmacol Ther 1993, 58(3):319-379.
10. Cipolloni P.B., Kimerer L., Weintraub N.D., Smith D.V., Keller A. Distribution of inhibitory synapses on the somata of pyramidal neurons in cat motor cortex. Somatosens Mot Res 1998, 15:276-286.
11. Cox C.L., Metherate R., Weinberger N.M., Ashe J.H. Synaptic potentials and effects of amino acid antagonists in the auditory cortex. Brain Res Bull 1992, 28(3):401-410.
12. Edwards F.A., Konnerth A., Sakmann B., Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 1989, 414(5):600-612.
13. Eglen R.M., Nahorski S.R. The muscarinic M5 receptor: a silent or emerging subtype ?. Br J Pharmacol 2000, 130:13-21.
14. Fernández de Sevilla D., Buño W. Presynaptic inhibition of Schaffer collateral synapses by stimulation of hippocampal cholinergic afferent fibres. Eur J Neurosci 2003, 17(3):555-558.
15. Gil Z., Connors B.W., Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 1997, 19:679-686.
16. Gu Q. Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 2003, 80:291-301.
17. Guizzetti M., Moore N.H., Giordano G., Costa L.G. Modulation of neuritogenesis by astrocyte muscarinic receptors. J Biol Chem 2008, 283:31884-31897.
18. Hammer R., Giraldo E., Schiavi G.B., Monferini E., Ladinsky H. Binding profile of a novel cardioselective muscarine receptor antagonist, AF-DX 116, to membranes of peripheral tissues and brain in the rat. Life Sci 1986, 38(18):1653-1662.
19. Hasselmo M.E. Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav Brain Res 1995, 67:1-27.
20. Hasselmo M.E., Anderson B.P., Bower J.M. Cholinergic modulation of cortical associative memory function. J Neurophysiol 1992, 67:1230-1246.
21. Hasselmo M.E., Bower J.M. Acetylcholine and memory. Trends Neurosci 1993, 16:218-222.
22. Hille B. Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci 1994, 17(12):531-536.
23. Hounsgaard J. Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 1978, 62(3):787-797.
24. Hulme E.C., Birdsall N.J.M., Buckey N.J. Muscarinic receptors subtypes. Annu Rev Pharmacol Toxicol 1990, 30:633-673.
25. Jones S.V. m4 muscarinic receptor subtype activates an inwardly rectifying potassium conductance in AtT20 cells. Neurosci Lett 1992, 147(2):125-130.
26. Kimura F., Baughman R.W. Distinct muscarinic receptor subtypes suppress excitatory and inhibitory synaptic responses. J Neurophysiol 1997, 77(2):709-716.
27. Kimura F., Fukuda M., Tsumoto T. Acetylcholine supresses the spread of excitation in the visual cortex revealed by optical recording: possible diffential efect depending on the source of input. Eur J Neurosci 1999, 11:3597-3609.
28. Kirkwood A., Rozas C., Kirkwood J., Perez F., Bear M.F. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci 1999, 19:1599-1609.
29. Koós T., Tepper J.M. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 2002, 22(2):529-535.
30. Krejci A., Tucek S. Quantitation of mRNAs for M1 to M5 subtypes of muscarinic receptors in rat heart and brain cortex. Mol Pharmacol 2002, 61:1267-1272.
31. Larkman A., Mason A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes. J Neurosci 1990, 10:1407-1414.
32. Le Roux N., Amar M., Baux G., Fossier P. Homeostatic control of the excitation-inhibition balance in cortical layer 5 pyramidal neurons. Eur J Neurosci 2006, 24:3507-3518.
33. Le Roux N., Amar M., Moreau A., Baux G., Fossier P. Impaired GABAergic transmission disrupts normal homeostatic plasticity in rat cortical netwoks. Eur J Neurosci 2008, 27:3244-3256.
34. Levey A.I., Kitt C.A., Simonds W.F., Price D.L., Brann M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 1991, 11:3218-3226.
35. Lucas-Meunier E., Monier C., Amar M., Baux G., Frégnac Y., Fossier P. Involvement of muscarinic and nicotinic receptors in the endogenous cholinergic modulation of the balance between excitation and inhibition in the young rat visual cortex. Cereb Cortex 2009, 19:2411-2427.
36. Marino M., Rouse S.T., Levey A.I., Potter L.T., Conn P.J. Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-d-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci U S A 1998, 95:11465-11470.
37. Markram H., Lubke J., Frotscher M., Roth A., Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in tne developing rat neocortex. J Physiol 1997, 500:409-440.
38. Markram H., Segal M. Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol 1990, 427:381-393.
39. Mason A., Larkman A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J Neurosci 1990, 10:1415-1428.
40. McCormick D.A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in the neuromodulation of thalamocortical activity. Prog Neurobiol 1992, 39:337-388.
41. McCormick D.A., Connors B.W., Lighthall J.W., Prince D.A. Comparative electrophysiology of pyramidal and sparcely spiny stellate neurons of the neocortex. J Neurophysiol 1985, 54:782-806.
42. McCormick D.A., Prince D.A. Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci U S A 1985, 82(18):6344-6348.
43. McCormick D.A., Prince D.A. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 1986, 375:169-194.
44. Mentis M.J., Sunderland T., Lai J., Conolly C., Krasuski J., Levine B., Friz J., Sobti S., Shapiro M., Rapoport S.I. Muscarinic versus nicotinic modulation of a visual task. A pet study using drug probes. Neuropsychopharmacology 2001, 25:555-564.
45. Metherate R., Ashe J.H. Synaptic interactions involving acetylcholine, glutamate, and GABA in rat auditory cortex. Exp Brain Res 1995, 107:59-72.
46. Michel A.D., Stefanich E., Whiting R.L. Direct labeling of rat M3-muscarinic receptors by [3H]4DAMP. Eur J Pharmacol 1989, 166(3):459-466.
47. Michel F.J., Robillard J.M., Trudeau L.E. Regulation of rat mesencephalic GABAergic neurones through muscarinic receptors. J Physiol 2004, 556:429-445.
48. Monier C., Fournier J., Fregnac Y. In vitro and in vivo measures of evoked excitatory and inhibitory conductance dynamics in sensory cortices. J Neurosci Methods 2008, 169:323-365.
49. Murakoshi T. Cholinergic modulation of synaptic transmission in the rat visual cortex in vitro. Vision Res 1995, 35:25-35.
50. Reever C.M., Ferrari-Dileeo G., Flynn D.D. The M5/m5 receptor subtype: fact or fiction. Life Sci 1997, 60:1105-1112.
51. 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, 64:501-519.
52. Sato H., Hata Y., Masui H., Tsumoto T. A functional role of cholinergic innervation to neurons in the cat visual cortex. J Neurophysiol 1987, 58:765-780.
53. Schliebs R., Walch C., Stewart M.G. Laminar pattern of cholinergic and adrenergic receptors in rat visual cortex using quantitative receptor autoradiography. J Hirnforsch 1989, 30(3):303-311.
54. Schliebs R., Rossner S., Kumar A., Bigl V. Muscarinic acetylcholine receptor subtypes in rat visual cortex-a comparative study using quantitative receptor autoradiography and in situ hybridization. Indian J Exp Biol 1994, 32(1):25-30.
55. Segal M. Synaptic transmission between cultured rat hippocampal neurons is enhanced by activation of protein kinase-C. Neurosci Lett 1989, 101(2):169-174.
56. Sillito A.M., Kemp J.A. Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res 1983, 289(1-2):143-155.
57. Thomson A.M., Bannister A.P. Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 1998, 84:669-683.
58. Vaknin G., Teyler T.J. Ontogenesis of the depressant activity of carbachol on synaptic activity in rat visual cortex. Brain Res Bull 1991, 26:211-214.
59. Vidal C., Changeux J.P. Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience 1993, 56(1):23-32.
60. Vilaró M.T., Palacios J.M., Mengod G. Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci Lett 1990, 114(2):154-159.
61. Volpicelli L.A., Levey A.I. Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog Brain Res 2004, 145:59-66.
62. Watson N., Daniels D.V., Ford A.P., Eglen R.M., Hegde S.S. Comparative pharmacology of recombinant human M3 and M5 muscarinic receptors expressed in CHO-K1 cells. Br J Pharmacol 1999, 127(2):590-596.
63. Wehr M., Zador A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446.
64. Wehr M., Zador A.M. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 2005, 47:437-445.
65. Wess J., Liu J., Blin N., Lerche C., Kostenis E. Structural basis of receptor/G protein coupling selectivity studied with muscarinic receptors as model systems. Life Sci 1997, 60:1007-1014.
66. Williams S.H., Johnston D. Muscarinic cholinergic inhibition of glutamatergic transmission. Presynaptic receptors in the mammalian brain 1993, 27-41. Birkhauser, Boston, MA. T.B. Dunwiddie, D.M. Lovinger (Eds.).
67. Yamada M., Basile A.S., Fedorova I., Zhang W., Duttaroy A., Cui Y., Lamping K.G., Faraci F.M., Deng C.X., Wess J. Novel insights into M5 muscarinic acetylcholine receptor function by the use of gene targeting technology. Life Sci 2003, 74(2-3):345-353.
68. Yigit M., Keipert C., Backus K.H. Muscarinic acetylcholine receptors potentiate the GABAergic transmission in the developing rat inferior colliculus. Neuropharmacology 2003, 45(4):504-513.
69. Zhang L., Warren R.A. Muscarinic and nicotinic presynaptic modulation of EPSCs in the nucleus accumbens during postnatal development. J Neurophysiol 2002, 88(6):3315-3330.
70. Zilles K., Schröder H., Schröder U., Horvath E., Werner L., Luiten P.G., Maelicke A., Strosberg A.D. Distribution of cholinergic receptors in the rat and human neocortex. EXS 1989, 57:212-228.