Noradrenergic modulation of XII motoneuron inspiratory activity does not involve α2-receptor inhibition of the Ih current or presynaptic glutamate release

Journal of Applied Physiology

Volumn 98, Issue 4, 2005, Pages 1297-1308

  Adachi, Tadafumi ^a   Robinson, Dean M ^a   Miles, Gareth B ^a   Funk, Gregory D ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

2 adrenoceptor; Airway control; Clonidine; Hyperpolarization activated inward current; Rat; Whole cell recording

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; ALPHA ADRENERGIC RECEPTOR; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; BICUCULLINE; BRIMONIDINE; CLONIDINE; EFAROXAN; GLUTAMIC ACID; IMIDAZOLINE; IMIDAZOLINE DERIVATIVE; NORADRENALIN;

ACTION POTENTIAL; AMINO ACID METABOLISM; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPOGLOSSAL NERVE; INHIBITION KINETICS; MOTONEURON; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; PRESYNAPTIC INHIBITION; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; RECEPTOR BINDING;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CLONIDINE; GLUTAMIC ACID; HYPOGLOSSAL NERVE; INHALATION; MEMBRANE POTENTIALS; MOTOR NEURONS; NOREPINEPHRINE; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, ALPHA-2; SYNAPTIC TRANSMISSION;

EID: 15444380719     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00977.2004     Document Type: Article

References (69)

1. Aldes LD, Chapman ME, Chronister RB, and Haycock JW. Sources of noradrenergic afferents to the hypoglossal nucleus in the rat. Brain Res Bull 29: 931-942, 1992.
2. 2-adrenergic selectivity and differing affinities for GTP. Life Sci 43: 1805-1812, 1988.
3. Bach KB and Mitchell GS. Hypercapnia-induced long-term depression of respiratory activity requires alpha2-adrenergic receptors. J Appl Physiol 84: 2099-2105, 1998.
4. Bartlett DJ, Leiter JC, and Knuth SL. Control and actions of the genioglossus muscle. In: Sleep and Respiration, edited by Suratt FG and Remmers JE. New York: Wiley-Liss, 1990, p. 99-108.
5. Bayliss DA, Viana F, Bellingham MC, and Berger AJ. Characteristics and postnatal development of a hyperpolarization-activated inward current in rat hypoglossal motoneurons in vitro. J Neurophysiol 71: 119-128, 1994.
6. 2-adrenoceptors inhibit excitatory synaptic transmission in rat brain stem. Am J Physiol Gastrointest Liver Physiol 212: G654-G661, 1997.
7. 2-adrenoceptors control excitatory, but not inhibitory, transmission at rat hippocampal synapses. J Physiol 519: 439-449, 1999.
8. Cathala L, Guyon A, Eugene D, and Paupardin-Tritsch D. Alpha2-adrenoceptor activation increases a cationic conductance and spontaneous GABAergic synaptic activity in dopaminergic neurones of the rat substantia nigra. Neuroscience 115: 1059-1065, 2002.
9. Chen C. ZD7288 inhibits postsynaptic glutamate receptor-mediated responses at hippocampal perforant path-granule cell synapses. Eur J Neurosci 19: 643-649, 2004.
10. Czesnik D, Nezlin L, Rabba J, Müller B, and Schild D. Noradrenergic modulation of calcium currents and synaptic transmission in the olfactory bulb of Xenopus laevis tadpoles. Eur J Neurosci 13: 1093-1100, 2001.
11. 1A receptors in human frontal cortex membranes. Eur J Pharmacol 201: 1-8, 1991.
12. Denavit-Saubie M, Champagnat J, and Rondouin G. Central effect of adrenergic compounds on cat respiratory mechanisms. In: Central Adrenaline Neurons: Basic Aspects and Their Role in Cardiovascular Functions, edited by Fuxe K, Goldstein M, Hokfelt B, and Hokfelt T. Oxford, UK: Pergamon, 1980, p. 277-287.
13. Erne-Brand F, Jirounek P, Drewe J, Hampl K, and Schneider MC. Mechanism of antinociceptive action of clonidine in nonmyelinated nerve fibers. Eur J Pharmacol 383: 1-8, 1999.
14. Errchidi S, Hilaire G, and Monteau R. Permanent release of noradrenaline modulates respiratory frequency in the newborn rat: an in vitro study. J Physiol 429: 497-510, 1990.
15. Errchidi S, Monteau R, and Hilaire G. Noradrenergic modulation of the medullary respiratory rhythm generator in the newborn rat: an in vitro study. J Physiol 443: 477-398, 1991.
16. Farsang C and Kapocsi J. Imidazoline receptors: from discovery to antihypertensive therapy (facts and doubts). Brain Res Bull 49: 317-331, 1999.
17. 2+ channel activity and regulates sperm function. Biochem Biophys Res Commun 311: 187-192, 2003.
18. Franco P, Szliwowski H, Dramaix M, and Kahn A. Decreased autonomic responses to obstructive sleep events in future victims of sudden infant death syndrome. Pediatr Res 46: 33-39, 1999.
19. Fukuda A, Minami T, Nabekura J, and Oomura Y. The effects of noradrenaline on neurones in the rat dorsal motor nucleus of the vagus, in vitro. J Physiol 393: 213-231, 1987.
20. Funk GD, Smith JC, and Feldman JL. Development of thyrotropin-releasing hormone and norepinephrine potentiation of inspiratory-related hypoglossal motoneuron discharge in neonatal and juvenile mice in vitro. J Neurophysiol 72: 2538-2541, 1994.
21. Funk GD, Smith JC, and Feldman JL. Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70: 1497-1515, 1993.
22. Gaumann DM, Brunet PC, and Jirounek P. Clonidine enhances the effects of lidocaine on C-fiber action potential. Anesth Analg 74: 719-725, 1992.
23. Ghamari-Langroudi M and Bourque CW. Excitatory role of the hyperpolarization-activated inward current in phasic and tonic firing of rat supraoptic neurons. J Neurosci 20: 4855-4863, 2000.
24. Golowasch G and Marder E. Ionic current of the lateral pyloric neuron of the stomatogastric ganglion of the crab. J Neurophysiol 67: 318-331, 1992.
25. Hieble JP and Ruffalo RR Jr. Possible structural and functional relationships between imidazoline receptors and alpha2-adrenoceptors. Ann NY Acad Sci 763: 8-21, 1995.
26. Inokuchi H, Yoshimura M, Polosa C, and Nishi S. Adrenergic receptors (alpha 1 and alpha 2) modulate different potassium conductances in sympathetic preganglionic neurons. Can J Physiol Pharmacol 70, Suppl: S92-S97, 1992.
27. Johnson SM, Smith JC, and Feldman JL. Modulation of respiratory rhythm in vitro: role of Gi/o protein-mediated mechanisms. J Appl Physiol 80: 2120-2133, 1996.
28. 2 adrenoceptors inhibit glutamate release from rat spinal cord synaptosomes. J Neurochem 60: 522-526, 1993.
29. Katakura N and Chandler SH. Iontophoretic analysis of the pharmacologic mechanisms responsible for initiation and modulation of trigeminal motoneuronal discharge evoked by intra-oral afferent stimulation. Brain Res 549: 66-77, 1991.
30. Kawasaki Y, Kumamoto E, Furue H, and Yoshimura M. Alpha2 adrenoceptor-mediated presynaptic inhibition of primary afferent glutamatergic transmission in rat substantia gelatinosa neurons. Anesthesiology 98: 682-689, 2003.
31. 3H]rilmenidine. Brain Res 675: 264-278, 1995.
32. + channels in caudal raphe neurons. Neuroscience 82: 753-765, 1998.
33. Lindsay AD, Greer JJ, and Feldman JL. Phrenic motoneuron morphology in the neonatal rat. J Comp Neurol 308: 169-179, 1991.
34. Liu G, Feldman JL, and Smith JC. Excitatory amino acid-mediated transmission of inspiratory drive to phrenic motoneurons. J Neurophysiol 64: 423-436, 1990.
35. Llado J, Esteban S, and Garcia-Sevilla JA. The α2-adrenoceptor antagonist idazoxan is an agonist at 5-HT1A autoreceptors modulating serotonin synthesis in the rat brain in vivo. Neurosci Lett 218: 111-114, 1996.
36. 2 sensitivity in vitro. Respir Physiol Neurobiol 142: 27-42, 2004.
37. h. Neuron 20: 553-563, 1998.
38. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497: 119-130, 1996.
39. McCormick DA and Pape HC. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurons. J Physiol 431: 291-318, 1990.
40. 3 receptors. Significance for the modulation of frontocortical monoaminergic transmission and depressive states. Synapse 35: 79-95, 2000.
41. h, in inspiratory brainstem neurons and its inhibition by hypoxia. Eur J Neurosci 12: 520-526, 2000.
42. Miyazaki T, Kobayashi H, and Tosaka T. Presynaptic inhibition by noradrenaline of the EPSC evoked in neonatal rat sympathetic preganglionic neurons. Brain Res 790: 170-177, 1998.
43. Nicholson C. Diffusion of an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 333: 325-329, 1985.
44. North RA and Yoshimura M. The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J Physiol 349: 43-55, 1984.
45. Pack AI. Obstructive sleep apnoea. Adv Intern Med 39: 517-567, 1994.
46. 2-adrenergic receptors. J Neurophysiol 87: 1938-1947, 2002.
47. Pape HC. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58: 299-327, 1996.
48. 3H]clonidine binding. Mol Pharmacol 35: 345-354, 1989.
49. Parkis MA, Bayliss DA, and Berger AJ. Actions of norepinephrine on rat hypoglossal motoneurons. J Neurophysiol 74: 1911-1919, 1995.
50. h) in rat hypoglossal motoneurons. Brain Res 769: 108-118, 1997.
51. Rekling J, Funk GD, Bayliss D, Dong X, and Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
52. Remmers JE, Degroot WJ, Sauerland EK, and Anch AM. Pathogenesis of upper airway occlusion during sleep. J Appl Physiol 44: 931-938, 1978.
53. Roda F, Gestreau C, and Bianchi AL. Discharge patterns of hypoglossal motoneurons during fictive breathing, coughing, and swallowing. J Neurophysiol 87: 1703-1711, 2001.
54. Rosin DL, Talley EM, Lee A, Stornetta RL, Gaylinn BD, Guyenet PG, and Lynch KR. Distribution of alpha 2C-adrenergic receptor-like immunoreactivity in the rat central nervous system. J Comp Neurol 12: 135-165, 1996.
55. Sauerland EK and Harper RM. The human tongue during sleep: electromyographic activity of the genioglossus muscle. Exp Neurol 51: 160-170, 1976.
56. Saywell SA and Feldman JL. Dynamic interactions of excitatory and inhibitory inputs in hypoglossal motoneurons: respiratory phasing and modulation by PKA. J Physiol 554: 879-889, 2003.
57. Schofield GG. Norepinephrine blocks a calcium current of adult rat sympathetic neurons via an alpha 2-adrenoceptor. Eur J Pharmacol 180: 37-47, 1990.
58. Selvaratnam SR, Parkis MA, and Funk GD. Developmental modulation of mouse hypoglossal nerve inspiratory output in vitro by noradrenergic receptor agonists. Brain Res 805: 104-115, 1998.
59. Singer JH, Bellingham MC, and Berger AJ. Presynaptic inhibition of glutamatergic synaptic transmission to rat motoneurons by serotonin. J Neurophysiol 76: 799-807, 1996.
60. Singer JH, Talley EM, Bayliss DA, and Berger AJ. Development of glycinergic synaptic transmission to rat brain stem motoneurons. J Neurophysiol 80: 2608-2620, 1998.
61. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, and Feldman JL. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
62. Steinschneider A, Weinstein SL, and Diamond E. The sudden infant death syndrome and apnea/obstruction during neonatal sleep and feeding. Pediatrics 70: 858-863, 1982.
63. Talley EM, Rosin DL, Lee A, Guyenet PG, and Lynch KR. Distribution of alpha 2A-adrenergic receptor-like immunoreactivity in the rat central nervous system. J Comp Neurol 12: 111-134, 1996.
64. Thoby-Brisson M, Telgkamp P, and Ramirez JM. The role of the hyperpolarization-activated current in modulating rhythmic activity in the isolated respiratory network of mice. J Neurosci 20: 2994-3005, 2000.
65. Tremblay LE and Bedard PJ. Effect of clonidine on motoneuron excitability in spinalized rats. Neuropharmacology 25: 41-46, 1986.
66. Ueda M, Oyama T, Kuraishi Y, Akaike A, and Satoh M. Alpha2-adrenoceptor- mediated inhibition of capsaicin-evoked release of glutamate from spinal dorsal horn slices. Neurosci Lett 188: 137-139, 1995.
67. Viana F, Bayliss DA, and Berger AJ. Postnatal changes in rat hypoglossal motoneuron membrane properties. Neuroscience 59: 131-148, 1994.
68. Yasuda K, Robinson DM, Walsh CW, Selvaratnam SR, McMorland AJC, and Funk GD. Modulation of hypoglossal motoneuron activity by SP in neonatal mice in vitro: cellular and synaptic mechanisms. J Physiol 534: 447-464, 2001.
69. Zanger SZ. 25 years since the discovery of presynaptic receptors: present knowledge and future perspectives. TIPS 18: 95-99, 1997.