Presynaptic depression of excitatory synaptic inputs to rat hypoglossal motoneurons by muscarinic M2 receptors

Journal of Neurophysiology

Volumn 76, Issue 6, 1996, Pages 3758-3770

  Bellingham, Mark C ^a,b   Berger, Albert J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBACHOL; CHOLINERGIC RECEPTOR; GLUTAMINE; METHOCTRAMINE; MUSCARINE; MUSCARINIC M2 RECEPTOR; PHYSOSTIGMINE; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CALCIUM TRANSPORT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPOGLOSSAL NERVE; MOTONEURON; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; RETICULAR FORMATION;

EID: 0030472579     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.6.3758     Document Type: Article

References (63)

1. AUBERT, I., CÉCYRE, D., GAUTHIER, S., AND QUIRION, R. Characterization and autoradiographic distribution of AF-DX 384 binding to putative muscarinic M2 receptors in the rat brain. Eur. J. Pharmacol. 217: 173-184, 1992.
2. BAYLISS, D. A., UMEMIYA, M., AND BERGER, A. J. Inhibition of N- and P-type calcium currents and the after-hyperpolarization in rat motoneurones by serotonin. J. Physiol. Lond. 485: 635-647, 1995.
3. BELLINGHAM, M. C. AND BERGER, A. J. Adenosine suppresses excitatory glutamatergic inputs to rat hypoglossal motoneurons in vitro. Neurosci. Lett. 177: 143-146, 1994.
4. BELLINGHAM, M. C. AND BERGER, A. J. Presynaptic depression of glutamatergic EPSCs in rat hypoglossal motoneurons (HMs) by muscarinic receptors is not due to inhibition of N- or P-type calcium currents. Soc. Neurosci. Abstr. 21: 925, 1995.
5. BORKE, R. C. AND NAU, M. E. The ultrastructural identification of reticulohypoglossal axon terminals anterogradely labeled with horseradish peroxidase. Brain Res. 337: 127-132, 1985.
6. BRADLEY, P. B. AND DRAY, A. Observations on the pharmacology of cholinoceptive neurones in the rat brain stem. Br. J. Pharmacol. 57: 599-602, 1976.
7. BRUNNER, H. AND MISGELD, U. Muscarinic amplification of fast excitation in hilar neurones and inhibition in granule cells in the guinea-pig hippocampus. J. Physiol. Lond. 480: 513-526, 1994.
8. CAPOGNA, M., GÄHWILER, B. H., AND THOMPSON, S. M. Presynaptic enhancement of inhibitory synaptic transmission by protein kinases A and C in the rat hippocampus in vitro. J. Neurosci. 15: 1249-1260, 1995.
9. CAULFIELD, M. P. Muscarinic receptors - characterization, coupling and function. Pharmacol. Ther. 58: 319-379, 1993.
10. CHASE, M. H. AND MORALES, F. R. The atonia and myoclonia of active (REM) sleep. Annu. Rev. Psychol. 41: 557-584, 1990.
11. CHRISTIE, M. J. AND NORTH, R. A. Agonists at mu-opioid, M2-muscarinic and GABAB-receptors increase the same potassium conductance in rat lateral parabrachial neurones. Br. J. Pharmacol. 95: 896-902, 1988.
12. CONNAUGHTON, M., PRIESTLEY, J. V., SOFRONIEW, M. V., ECKENSTEIN, F., AND CUELLO, A. C. Inputs to motoneurones in the hypoglossal nucleus of the rat: light and electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17: 205-224, 1986.
13. DOBBINS, E. G. AND FELDMAN, J. L. Differential innervation of protruder and retractor muscles of the tongue in rat. J. Comp. Neurol. 357: 376-394, 1995.
14. 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.
15. DUGGAN, A. W., HEADLEY, P. M., AND LODGE, D. Acetylcholine-sensitive cells in the caudal medulla of the rat: distribution, pharmacology and effects of pentobarbitone. Br. J. Pharmacol. 54: 23-31, 1975.
16. DUTAR, P. AND NICOLL, R. A. Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J. Neurosci. 8: 4214-4224, 1988.
17. EDMONDS, B., GIBB, A. J., AND COLQUHOUN, D. Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents. Annu. Rev. Physiol. 57: 495-519, 1995.
18. EGAN, T. M. AND NORTH, R. A. Acetylcholine hyperpolarizes central neurones by acting on an M2 muscarinic receptor. Nature Lond. 319: 405-407, 1986.
19. FREY, K. A. AND HOWLAND, M. M. Quantitative autoradiography of muscarinic cholinergic receptor binding in the rat brain: distinction of receptor subtypes in antagonist competition assays. J. Pharmacol. Exp. Ther. 263: 1391-1400, 1992.
20. 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.
21. GNADT, J. W. AND PEGRAM, G. V. Cholinergic brainstem mechanisms of REM sleep in the rat. Brain Res. 384: 29-41, 1986.
22. HASSELMO, M. E. AND BOWER, J. M. Cholinergic suppression specific to intrinsic not afferent fiber synapses in rat piriform (olfactory) cortex. J. Neurophysiol. 67: 1222-1229, 1992.
23. HOLMES, C. J., MAINVILLE, L. S., AND JONES, B. E. Distribution of cholinergic, GABAergic and serotonergic neurons in the medial medullary reticular formation and their projections studied by cytotoxic lesions in the cat. Neuroscience 62: 1155-1178, 1994.
24. HONORÉ, T. Excitatory amino acid receptor subtypes and specific antagonists. Med. Res. Rev. 9: 1-23, 1989.
25. HULME, E. C., BIRDSALL, N. J. M., AND BUCKLEY, N. J. Muscarinic receptor subtypes. Annu. Rev. Pharmacol. Toxicol. 30: 633-673, 1990.
26. JAHR, C. E. AND YOSHIOKA, K. Ia afferent excitation of motoneurones in the in vitro new-born rat spinal cord is selectively antagonized by kynurenate. J. Physiol. Lond. 370: 515-530, 1986.
27. JIANG, Z. G. AND DUN, N. J. Presynaptic suppression of excitatory postsynaptic potentials in rat ventral horn neurons by muscarinic agonists. Brain Res. 381: 182-186, 1986.
28. JONES, B. E. Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the rat. J. Comp. Neurol. 295: 485-514, 1990.
29. JONES, B. E. Paradoxical sleep and its chemical/structural substrates in the brain. Neuroscience 40: 637-656, 1991.
30. JONES, B. E. Reticular formation: cytoarchitecture, transmitters and projections. In: The Rat Nervous System, edited by G. Paxinos. San Diego, CA: Academic, 1995, p. 155-171.
31. KATZ, B. The Release of Neural Transmitter Substances. Springfield, IL: Thomas, 1969, p. 1.
32. KIMURA, H., KUBIN, L., DAVIES, R. O., AND PACK, A. I. Cholinergic stimulation of the pons depresses respiration in decerebrate cats. J. Appl. Physiol. 69: 2280-2289, 1990.
33. KUBIN, L., KIMURA, H., TOJIMA, H., DAVIES, R. O., AND PACK, A. I. Suppression of hypoglossal motoneurons during the carbachol-induced atonia of REM sleep is not caused by fast synaptic inhibition. Brain Res. 611: 300-312, 1993.
34. LAZARENO, S. AND BIRDSALL, N. J. M. Estimation of competitive antagonist affinity from functional inhibition curves using the Gaddum, Schild and Cheng-Prusoff equations. Br. J. Pharmacol. 109: 1110-1119, 1993a.
35. 35S]-GTP-gamma-S binding mediated by human muscarinic m1-m4 receptors: antagonist studies. Br. J. Pharmacol. 109: 1120-1127, 1993b.
36. Li, M., YASUDA, R. P., WALL, S. J., WELLSTEIN, A., AND WOLFE, B. B. Distribution of m2 muscarinic receptors in rat brain using antisera selective for m2 receptors. Mol. Pharmacol. 40: 28-35, 1991.
37. LOWE, A. A. The neural regulation of tongue movements. Prog. Neurobiol. 15: 295-344, 1980.
38. MALLIOS, V. J., LYDIC, R., AND BAOHDOYAN, H. A. Muscarinic receptor subtypes are differentially distributed across brain stem respiratory nuclei. Am. J. Physiol. 268 (Lung Cell. Mol Physiol. 12): L941-L949, 1995.
39. McCORMICK, D. A. AND PRINCE, D. A. Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature Lond. 319: 402-405, 1986.
40. MCCORMICK, D. A. AND PRINCE, D. A. Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J. Physiol. Lond. 392: 147-165, 1987.
41. MEGIRIAN, D., HINRICHSEN, C. F. L., AND SHERREY, J. H. Respiratory roles of genioglossus, stemothyroid, and sternohyoid muscles during sleep. Exp. Neurol. 90: 118-128, 1985.
42. PAN, Z. Z. AND WILLIAMS, J. T. Muscarine hyperpolarizes a subpopulation of neurons by activating an M2 muscarine receptor in rat nucleus raphe magnus in vitro. J. Neurosci. 14: 1332-1338, 1994.
43. PARKIS, M. A., BAYLISS, D. A., AND BERGER, A. J. Actions of norepinephrine on rat hypoglossal motoneurons. J. Neurophysiol. 74: 1911-1919, 1995.
44. 2+ channels involved? Neuropharmacology 34: 1549-1557, 1995.
45. SEGAL, M. Presynaptic cholinergic inhibition in hippocampal cultures. Synapse 4: 305-312, 1989.
46. SESSLE, B. J. Excitatory and inhibitory inputs to single neurones in the solitary tract nucleus and adjacent reticular formation. Brain Res. 53: 319-331, 1973.
47. STUART, G. J., DODT, H.-U., AND SAKMANN, B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pfluegers Arch. 423: 511-518, 1993.
48. SUGITA, S., UCHIMURA, N., JIANG, Z.-G., AND NORTH, R. A. 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.
49. TAGO, H., MCGEER, P. L., MCGEER, E. G., AKIYAMA, H., AND HERSH, L. B. Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res. 495: 271-297, 1989.
50. TAGUCHI, O., KUBIN, L., AND PACK, A. I. Evocation of postural atonia and respiratory depression by pontine carbachol in the decerebrate rat. Brain Res. 595: 107-115, 1992.
51. TRAVERS, J. B. AND NORGREN, R. Afferent projections to the oral motor nuclei in the rat. J. Comp. Neural. 220: 280-298, 1983.
52. UGOLINI, G. Specificity of rabies virus as a transneural tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J. Comp. Neurol. 356: 457-480, 1995.
53. UMEMIYA, M. AND BERGER, A. J. Activation of adenosine A1 and A2 receptors differentially modulates calcium channels and glycinergic synaptic transmission in rat brainstem. Neuron 13: 1439-1446, 1994.
54. VALENTINO, R. J. AND DINGLEDINE, R. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J. Neurosci. 1: 784-792, 1981.
55. VERTES, R. P. Brain stem gigantocellular neurons: patterns of activity during behavior and sleep in the freely moving rat. J. Neurophysiol. 42: 214-227, 1979.
56. VIDAL, C. AND CHANGEUX, J.-P. Nicotinic and muscarinic modulations of excitatory synaptic transmission in the rat prefrontal cortex in vitro. Neuroscience 56: 23-32, 1993.
57. VILARÓ, M. T., WIEDERHOLD, K. H., PALACIOS, J. M., AND MENGOD, G. Muscarinic M2 receptor mRNA expression and receptor binding in cholinergic and non-cholinergic cells in the rat brain: a correlative study using in situ hybridization histochemistry and receptor autoradiography. Neuroscience 47: 367-393, 1992a.
58. VILARÓ, M. T., WIEDERHOLD, K. H., PALACIOS, J. M., AND MENGOD, G. Muscarinic M2-selective ligands also recognize M4 receptors in the rat brain: evidence from combined in situ hybridization and receptor autoradiography. Synapse 11: 171-183, 1992b.
59. WAMSLEY, J. K., LEWIS, M. S., YOUNG, W. S., III, AND KUHAR, M. J. Autoradiographic localization of muscarinic cholinergic receptors in rat brainstem. J. Neurosci. 1: 176-190, 1981.
60. WILLIAMS, S. H. AND JOHNSTON, D. Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse. J. Neurophysiol. 64: 1089-1097, 1990.
61. WILLIAMS, S. H. AND JOHNSTON, D. Muscarinic cholinergic inhibition of glutamatergic transmission. In: Presynaptic Receptors in the Mammalian Brain, edited by T. V. Dunwiddie and D. M. Lovinger. Boston, MA: Birkhäuser, 1993, p. 27-41.
62. WOOLF, N. J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37: 475-524, 1991.
63. WOOLF, N. J. AND BUTCHER, L. L. Cholinergic systems in the rat brain. IV. Descending projections of the pontomesencephalic tegmentum. Brain Res. Bull. 23: 519-540, 1989.