Acetylcholine modulates respiratory pattern: Effects mediated by M3-like receptors in preBotzinger complex inspiratory neurons

Journal of Neurophysiology

Volumn 83, Issue 3, 2000, Pages 1243-1252

  Shao, X M ^a   Feldman, J L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 DIPHENYLACETOXY 1 METHYLPIPERIDINE; ACETYLCHOLINE; ATROPINE; CARBACHOL; GALLAMINE; MUSCARINE; MUSCARINIC M3 RECEPTOR; PIRENZEPINE; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; HYPOGLOSSAL NERVE; MEMBRANE CONDUCTANCE; NERVE CELL; NERVE CONDUCTION; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; RESPIRATORY SYSTEM; VOLTAGE CLAMP;

EID: 0034060317     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.3.1243     Document Type: Article

References (74)

1. BENSON, D. M., BLITZER, R. D., AND LANDAU, E. M. An analysis of depolarization produced in guinea-pig hippocampus by cholinergic receptor stimulation. J. Physiol. (Lond.) 404: 479-496, 1988.
2. BÖHMER, G., SCHMID, K., AND BAUMANN, M. Evidence for a respiration-modulated cholinergic action on the activity of medullary respiration-related neurons in the rabbit. An iontophoretic study. Pflügers Arch Arch. Eur. J. Physiol. 415: 72-80, 1989.
3. BÖHMER, G., SCHMID, K., SCHMIDT, P., AND STEHLE, J. Cholinergic effects on spike-density and burst-duration of medullary respiration-related neurones in the rabbit: an iontophoretic study. Neuropharmacology 26: 1561-1572, 1987.
4. BONNER, T. I., BUCKLEY, N. J., YOUNG, A. C., AND BRANN, M. R. Identification of a family of muscarinic acetylcholine receptor genes. Science 237: 527-532, 1987.
5. BONNER, T. I., YOUNG, A. C., BRANN, M. R., AND BUCKLEY, N. J. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron 1: 403-410, 1988.
6. BRADLEY, P. B. AND LUCY, A. P. Cholinoceptive properties of respiratory neurones in the rat medulla. Neuropharmacology 22: 853-858, 1983.
7. + current in a vertebrate neurone. Nature 283: 673-676, 1980.
8. BÜNEMANN, M AND HOSEY M. M. G-protein coupled receptor kinases as modulators of G-protein signalling. J. Physiol. (Lond.) 517: 5-23, 1999.
9. BURTON, M. D., JOHNSON, D. C., AND KAZEMI, H. The central respiratory effects of acetylcholine vary with CSF pH. J. Auton. Nerv. Syst. 62: 27-32, 1997.
10. BURTON, M. D., NOURI, K., BAICHOO, S., SAMUELS-TOYLOY, N., AND KAZEMI, H. Ventilatory output and acetylcholine: perturbations in release and muscarinic receptor activation. J. Appl. Physiol. 77: 2275-2284, 1994.
11. BURTON, M. D., NOURI, M., AND KAZEMI, H. Acetylcholine and central respiratory control: perturbations of acetylcholine synthesis in the isolated brainstem of the neonatal rat. Brain Res. 670: 39-47, 1995.
12. CAULFIELD, M. P. AND BIRDSALL, N.J.M. International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev. 50: 279-290, 1998.
13. COGGAN, J. S., PURNYN, S. L., KNOPER, S. R., AND KREULEN, D. L. Muscarinic inhibition of two potassium currents in guinea-pig prevertebral neurons: differentiation by extracellular cesium. Neuroscience 59: 349-361, 1994.
14. CONNELLY, C. A., DOBBINS, E. G., AND FELDMAN, J. L. Pre-Bötzinger complex in cats: respiratory neuronal discharge patterns. Brain Res. 590: 337-340, 1992.
15. DELMAS, P., NIEL, J. P., AND GOLA, M. Muscarinic activation of a novel voltage-sensitive inward current in rabbit prevertebral sympathetic neurons. Eur. J. Neurosci. 8: 598-610, 1996.
16. DEV, N. B. AND LOESCHCKE, H. H. A cholinergic mechanism involved in the respiratory chemosensitivity of the medulla oblongata in the cat. Pflügers Arch. 379: 29-36, 1979.
17. DOODS, H. N., MATHY, M.-J., DAVIDESKO, D., VAN CHARLDORP, K. J., DE JONGE, A., AND VAN ZWIETEN, P. A. Selectivity of muscarinic antagonists in radioligand and in vivo experiments for the putative M1, M2 and M3 receptors. J. Pharmacol. Exp. Ther. 242: 257-262, 1987.
18. DÖRJE, F., WESS, J., LAMBRECHT, G., TACKE, R., MUTSCHLER, E., AND BRANN, M. R. Antagonist binding profiles of five cloned human muscarinic receptor subtypes. J. Pharmacol. Exp. Ther. 256: 727-733, 1991.
19. FELDMAN, J. L. AND SMITH, J. C. Cellular mechanisms underlying modulation of breathing pattern in mammals. Ann. NY Acad, Sci. 563: 114-130, 1989.
20. FELDMAN, J. L, SMITH, J. C., ELENBERGER, H. H., CONNELLY, C. A., LIU, G., GREER, J, J. LINDSAY, A. D., AND OTTO, M. R. Neurogenesis of respiratory rhythm and pattern: emerging concepts. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 259: R879-R886, 1990.
21. FOUTZ, A. S., BOUDINOT, E., AND DENAVIT-SAUBIÉ, M. Central respiratory depression induced by acetylcholinesterase inhibition: involvement of anaesthesia. Eur. J. Pharmacol. 142: 207-213, 1987.
22. FRASER, D. D. AND MACVICAR, B. A. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J. Neurosci. 16: 4113-4128, 1996.
23. FUKUDA, Y. AND LOESCHCKE, H. H. A cholinergic mechanism involved in the neuronal excitation by H+ in the respiratory chemosensitive structures of the ventral medulla oblongata of rats in vitro. Pflügers Arch. 379: 125-135, 1979.
24. FUNK, G. D., SMITH, J. C., AND FELDMAN, J. L. Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J. Neurophysiol. 70: 1497-1515, 1993.
25. GESELL, R., HANSEN, E. T., AND WORZNIAK, J. J. Humoral intermediation of nerve cell activation in the central nervous system. Am J. Physiol. 138: 776-791, 1943.
26. GILLIS, R. A., WALTON, D. P., QUEST, J. A., NAMATH, I. J., HAMOSH, P., AND DRETCHEN, K. L. Cadiorespiratory effects produced by activation of cholinergic muscarinic receptors on the ventral surface of the medulla. J. Pharmacol. Exp. Therap. 247: 765-773, 1988.
27. GOLA, M., DELMAS, P., AND CHAGNEUX, H. Encoding properties induced by a persistent voltage-gated muscarinic sodium current in rabbit sympathetic neurones. J. Physiol. (Lond.) 510: 387-399, 1998.
28. GOLDMAN, D. E. Potential impedance and rectification in membranes. J. Gen. Physiol. 27: 37-60, 1943.
29. GONSALVES, S. F. AND BORISON, H. L. Atropine-resistant central respiratory stimulation by bethanechol in cats. J. Pharmacol. Exp. Ther. 214: 297-305, 1980.
30. GRAY, P. A., REKLING, J. C., BOCCHIARO, C. M., AND FELDMAN, J. L. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286: 1566-1568, 1999.
31. GUÉRINEAU, N. C., BUSSO, J.-L., GÄHWILER, B. H., AND GERBER, U. Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J. Neurosci. 15: 4395-4407, 1995.
32. HAJ-DAHMAME, S. AND ANDRADE, R. Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J. Neurosci. 16: 3848-3861, 1996.
33. HAJI, A., FURUICHI, S., AND TAKEDA, R. Effects of iontophoretically applied acetylcholine on membrane potential and synaptic activity of bulbar respiratory neurones in decerebrate cats. Neuropharmacology 35: 195-203, 1996.
34. HAXHIU, M. A., MITRA, J., VAN LUNTEREN, E., BRUCE E. N., AND CHERNIACK, N. S. Hypoglossal and phrenic responses to cholinergic agents applied to ventral medullary surface. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 247: R939-R944, 1984.
35. HODGKIN, A. L. AND KATZ, B. The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. (Lond.) 108: 37-77, 1949.
36. HULME, E. C., BIRDSALL, N. J., AND BUCKLEY, N. J. Muscarinic receptor subtypes. Annu. Rev. Pharmacol. Toxicol. 30: 633-673, 1990.
37. JOHNSON, S. M., SMITH, J. C., FUNK, G. D., AND FELDMAN J. L. Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat. J. Neurophysiol. 72: 2598-2608, 1994.
38. JORDAN, D., AND SPYER, K. M. Effects of acetylcholine on respiratory neurones in the nucleus ambiguus-retroambigualis complex of the cat. J. Physiol. (Lond.) 320: 103-111, 1981.
39. KINNEY, H. C., FILLIANO, J. J., SLEEPER, L. A., MANDELL, F., VALDES-DAPENA, M., AND WHITE, W. F. Decreased muscarinic receptor binding in the arcuate nucleus in sudden infant death syndrome. Science 269: 1446-1450, 1995a.
40. 3H]quinuclidinyl benzilate binding to muscarinic cholinergic receptors in the developing human brainstem. J. Comp. Neurol. 362: 350-367, 1995b.
41. KIRSTEN, E. B., SATAYAVIVAD, J., ST. JOHN, W. M., AND WANG, S. C. Alteration of medullary respiratory unit discharge by iontophoretic application of putative neurotransmitters. Br. J. Pharmacol. 63: 275-281, 1978.
42. KLINK, R. AND ALONSO, A. Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J. Neurophysiol. 77: 1813-1828, 1997a.
43. KLINK, R. AND ALONSO, A. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol. 77: 1829-1843, 1997b.
44. KOSHIYA, N. AND GUYENET, P. G. Tonic sympathetic chmoreflex after blockade of respiratory rhythmogenesis in the rat. J. Physiol. (Lond.) 491: 859-869, 1996.
45. KOSHIYA, N. AND SMITH, J. C. Neuronal pacemaker for breathing visualized in vitro. Nature 400: 360-363, 1999.
46. KUBO, T., FUKUDA, K., MIKAMI, A., MAEDA, A., TAKAHASHI, H., MISHINA, M., HAGA, T., HAGA, K., ICHIYAMA, A., KANGAWA, K., KOJIMA, M., MATSUO, H., HIROSE, T., AND NUMA, S. Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature 323: 411-416, 1986.
47. 35S]-GTP gamma S binding mediated by human muscarinic m1-m4 receptors: antagonist studies. Br. J. Pharmacol. 109: 1120-1127, 1993.
48. LAZARENO, S., BUCKLEY, N. J., AND ROBERTS, F. F. Characterization of muscarinic M4 binding sites in rabbit lung, chicken heart, and NG108-15 cells. Mol. Pharmacol. 38: 805-815, 1990.
49. LOTTI, M. Treatment of acute organophosphate poisoning. Med. J. Aust. 154: 51-55, 1991.
50. MADISON, D. V., LANCASTER, B., AND NICOLL, R. A. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci. 7: 733-741, 1987.
51. MALLIOS, V., LYDIC, R., AND BAGHDOYAN, H. A. Muscarinic receptor subtypes are differentially distributed across brain stem respiratory nuclei. Am. J. Physiol. Lung Cell Mol. Physiol. 268: L941-L949, 1995.
52. MCCORMICK, D. A. AND PRINCE, D. A. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J. Physiol. (Lond.) 375: 169-194, 1986a.
53. MCCORMICK, D. A. AND PRINCE, D. A. Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319: 402-405 1986b.
54. METZ, B. Brain acetylcholinesterase and a respiratory reflex. Am. J. Physiol. 192: 101-105, 1958.
55. MONTEAU, R., MORIN, D., AND HILAIRE, G. Acetylcholine and central chemosensitivity: in vitro study in the newborn rat. Respir. Physiol. 81: 241-253, 1990.
56. MURAKOSHI, T., SUZUE, T., AND TAMAI, S. A pharmacological study on respiratory rhythm in the isolated brainstem-spinal cord preparation of the newborn rat. Br. J. Pharmacol. 86: 95-104, 1985.
57. NATTIE, E. E. AND LI, A. Ventral medulla sites of muscarinic receptor subtypes involved in cardiorespiratory control. J. Appl. Physiol. 69: 33-41, 1990.
58. NATTIE, E. E., WOOD, J., MEGA, A., AND GORITSKI, W. Rostral ventrolateral medulla muscarinic receptor involvement in central ventilatory chemosensitivity. J. Appl. Physiol. 66: 1462-1470, 1989.
59. RAMIREZ, J. M., QUELLMALZ, U.J.A., AND RICHTER, D. W. Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice. J. Physiol. (Lond.) 491: 799-812, 1996.
60. RAMIREZ, J. M., SCHWARZACHER, S. W., PIERREFICHE, O., OLIVERA, B. M., AND RICHTER, D. W. Selective lesioning of the cat pre-Bötzinger complex in vivo eliminates breathing but not gasping. J. Physiol. (Lond.) 507: 895-907, 1998.
61. REKLING, J. C. AND FELDMAN, J. L. Calcium-dependent plateau potentials in rostral ambiguus neurons in the newborn mouse brain stem in vitro. J. Neurophysiol. 78: 2483-2492, 1997.
62. REKLING, J. C. AND FELDMAN, J. L. PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60: 385-405, 1998.
63. SALMOIRAGHI, G. C. AND STEINER, F. A. Acetylcholine sensitivity of cat's medullary neurons. J. Neurophysiol. 26: 581-597, 1963.
64. SCHWARZACHER, S. W., SMITH, J. C., AND RICHTER, D. W. PreBötzinger complex in the cat. J. Neurophysiol. 73: 1452-1461, 1995.
65. SHAO, X. M. AND FELDMAN J. L. Respiratory rhythm generation and synaptic inhibition of expiratory neurons in preBötzinger complex: differential roles of glycinergic and GABAergic neural transmission. J. Neurophysiol. 77: 1853-1860, 1997.
66. SHAO, X. M. AND FELDMAN J. L. Modulation of respiratory pattern by acetylcholine (ACh): postsynaptic effects on preBötzinger complex (preBötC) inspiratory neurons mediated by muscarinic M3 receptors. Soc. Neurosci. Abstr. 24: 519, 1998.
67. SHEN, K.-Z. AND NORTH, R. A. Muscarine increases cation conductance and decreases potassium conductance in rat locus coeruleus neurones. J. Physiol. (Lond.) 455: 471-485, 1992.
68. SMITH, J. C., ELLENBERGER, H. H., BALLANYI, K., RICHTER, D. W., AND FELDMAN, J. L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 716-719, 1991.
69. SOLOMON, I. C., EDELMAN, N. G., AND NEUBAUER, J. A. Patterns of phrenic motor output evoked by chemical stimulation of neurons located in the preBötzinger complex in vivo. J. Neurophysiol. 81: 1150-1161, 1999.
70. UCHIMURA, N. AND NORTH, R. A. Muscarine reduces inwardly rectifying potassium conductance in rat nucleus accumbens neurones. J. Physiol. (Lond.) 422: 369-380, 1990.
71. VOGALIS, F. AND SANDERS, K. M. Cholinergic stimulation activates a non-selective cation current in canine pyloric circular muscle cells. J. Physiol. (Lond.) 429: 223-236, 1990.
72. WAELBROECK, M., TASTENOY, M., CAMUS, J., AND CHRISTOPHE, J. Binding of selective antagonists to four muscarinic receptors (M1 to M4) in rat forebrain. Mol. Pharmacol. 38: 267-273, 1990.
73. WANG, H.-S. AND MEKINNON, D. Modulation of inwardly rectifying currents in rat sympathetic neurones by muscarinic receptors. J. Physiol. (Lond.) 492: 467-478, 1996.
74. WEINSTOCK, M., ROLL, D., AND ZILBERMAN, Y. An analysis of the respiratory stimulant effect of physostigmine and neostigmine in the conscious rabbit. Clin. Exp. Pharmacol. Physiol. 8: 151-158, 1981.