Excitation of phrenic and sympathetic output during acute hypoxia: Contribution of medullary oxygen detectors

Respiration Physiology

Volumn 121, Issue 2-3, 2000, Pages 101-117

  Solomon, Irene C ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Control of breathing, central hypoxia; Hypoxia, medulla oblongata, phrenic, sympathetic activities; Medulla oblongata, hypoxia detecting neurons; Pattern of breathing, central hypoxia, gasping

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; BICUCULLINE METHIODIDE; EXCITATORY AMINO ACID RECEPTOR; OXYGEN; TETRODOTOXIN;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; BREATHING PATTERN; CHEMORECEPTOR REFLEX; HYPOXIA; MEDULLA OBLONGATA; NONHUMAN; PHRENIC NERVE; PRIORITY JOURNAL; RESPIRATION CONTROL; REVIEW; SYMPATHETIC NERVE;

EID: 0033849020     PISSN: 00345687     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0034-5687(00)00122-5     Document Type: Article

References (89)

1. Bainton C.R., Richter D.W., Seller H., Ballantyne D., Klein J.P. Respiratory modulation of sympathetic activity. J. Auton. Nerv. Syst. 12:1985;77-90.
2. Barman S.M., Gebber G.L. Basis for synchronization of sympathetic and phrenic nerve discharges. Am. J. Physiol. 231:1976;1601-1607.
3. Bianchi A.L., St. John W.M. Changes in antidromic latencies of medullary respiratory neurons in hypercapnia and hypoxia. J. Appl. Physiol. 59:1985;1208-1213.
4. Biscoe T.J., Duchen M.R. Electrophysiological responses of dissociated type I cells of the rabbit carotid body to cyanide. J. Physiol. (Lond.). 413:1989;447-468.
5. Bisgard G.E., Neubauer J.A. Peripheral and central effects of hypoxia. Dempsey J.A., Pack A.I. Regulation of Breathing. 1995;617-668 Marcel Dekker, New York.
6. A receptor function is regulated by phosphorylation in acutely dissociated guinea-pig hippocampal neurons. J. Physiol. (Lond.). 420:1990;207-221.
7. Chernick V, Craig R.J. Naloxone reverses neonatal depression caused by fetal asphyxia. Science. 216:1982;1252-1253.
8. Choi D.W. Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage. Trends Neurosci. 11:1988;465-469.
9. Connelly C.A., Dobbins E.G., Feldman J.L. Pre-Bötzinger complex in cats: respiratory neuronal discharge patterns. Brain Res. 590:1992;337-340.
10. Dampney R.A.L., Moon E.A. Role of ventrolateral medulla in vasomotor response to cerebral ischemia. Am. J. Physiol. 239:1980;H349-H358.
11. Di Rodriguez T.E., Bazan N.G. Changes in free fatty acids and diglycerides in mouse brain at birth and during anoxia. J. Neurochem. 41:1983;794-800.
12. Dobbins E.G., Feldman J.L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol. 347:1994;64-86.
13. Dutton R.E., Smith E.J., Ghatak P.K., Davies D.G. Dynamics of the respiratory controller during carotid body hypoxia. J. Appl. Physiol. 35:1973;844-850.
14. Ellenberger H.H., Feldman J.L. Subnuclear organization of the lateral tegmental field of the rat: I.: nucleus ambiguus and ventral respiratory group. J. Comp. Neurol. 294:1990;202-211.
15. England S.J., Melton J.E., Douse M.A., Duffun J. Activity of respiratory neurons during hypoxia in the chemodenervated cat. J. Appl. Physiol. 78:1995;856-861.
16. Erecinska M., Nelson D., Wilson D.F., Silver I.A. Neurotransmitter amino acids in the CNS. I.: regional changes in amino acid levels in rat brain during ischemia and reperfusion. Brain Res. 304:1984;9-22.
17. Eyzaguirre C., Koyano H. Effects of some pharmacological agents on chemoreceptor discharges. J. Physiol. (Lond.). 178:1965;410-437.
18. Eyzaguirre C., Zapata P. Perspectives in carotid body research. J. Appl. Physiol. 57:1984;931-957.
19. Feldman J.L., Smith J.C. Neural control of respiratory pattern in mammals: an overview. Dempsey J.A., Pack A.I. Regulation of Breathing. 1995;39-69 Marcel Dekker, New York.
20. Fidone S.J., Gonzales C. Initiation and control of chemoreceptor activity in the carotid body. Cherniack N.S., Widdicombe J.G. Handbook of Physiology - Section 3: The Respiratory System, Control of Breathing, Part 1. II: 1986;267-312 American Physiological Society, Bethesda.
21. Fitzgerald R.S., Lahiri S. Reflex response to chemoreceptor stimulation. Cherniack N.S., Widdicombe J.G. Handbook of Physiology - Section 3: The Respiratory System, Control of Breathing, Part 1. II: 1986;313-362 American Physiological Society, Bethesda.
22. Fregosi R.F., Knuth S.L., Ward D.K., Bartlett D. Jr. Hypoxia inhibits abdominal expiratory activity. J. Appl. Physiol. 63:1987;211-220.
23. Fung M.-L., St. John W.M., Tomori Z. Reflex recruitment of medullary gasping mechanisms in eupnea by pharyngeal stimulation in cats. J. Physiol. (Lond.). 475:1994;519-529.
24. Fung M.-L., Wang W., St. John W.M. Medullary loci critical for expression of gasping in adult rats. J. Physiol. (Lond.). 480:1994;597-611.
25. Gautier H., Bonora M. Possible alteration in brain monoamine metabolism during hypoxia-induced tachypnea in cats. J. Appl. Physiol. 49:1980;769-777.
26. Glaum S.R., Miller R.J. Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. J. Neurosci. 13:1993;1636-1641.
27. Goldberg M.P., Weiss J.H., Pham P., Choi D.W. N-methyl-D-aspartate receptors mediate hypoxic neuronal injury in cortical culture. J. Pharmacol. Exp. Ther. 243:1987;784-791.
28. Guntheroth W.G., Kawabori I. Hypoxic apnea and gasping. J. Clin. Invest. 56:1975;1371-1377.
29. Guyenet P.G., Brown D.L. Unit activity in nucleus paragigantocellularis lateralis during cerebral ischemia in the rat. Brain Res. 364:1986;301-314.
30. Guyenet P.G., Koshiya N. Respiratory-sympathetic integration in the medulla oblongata. Kunos G., Ciriello J. Central Neural Mechanisms in Cardiovascular Regulation. 1992;226-247 Birkhäuser, Boston.
31. Hagberg H., Lehmann A., Sandberg M., Nystrom B., Jacobsen I., Hamberger I. Ischemia-induced shift of inhibitory and excitatory amino acids from intra to extracellular compartments. J. Cereb. Blood Flow Metab. 5:1985;413-419.
32. Heistad D.D., Abboud F.M. Circulatory adjustments to hypoxia. Circulation. 61:1988;463-470.
33. Heymans C., Bouckaert J.J., Dautrebande L. Sinus carotidien et réflexes respiratoires. II.: influences respiratoires réflexes de l'acidose, de l'anoxémie, de l'anhydride carbonique, de respiratoires dans les poumons et au dela des poumons. Arch. Int. Pharmacodyn. 39:1930;400-448.
34. Huang Q., Zhou D., St. John W.M. Lesions of regions for in vitro ventilatory genesis eliminate gasping but not eupnea. Respir. Physiol. 107:1997;111-123.
35. Iversen K., Hedner T., Lundborg P. GABA concentrations and turn-over in neonatal rat brain during asphyxia and recovery. Acta Physiol. Scand. 118:1983;91-94.
36. Koshiya N., Huangfu D., Guyenet P.G. Ventrolateral medulla and sympathetic chemoreflex in the rat. Brain Res. 609:1993;174-184.
37. Lumsden T. Observation on the respiratory centres in the cat. J. Physiol. (Lond.). 57:1923;153-160.
38. MacDermott A.B., Mayer M.L., Westbrook G.L., Smith S.J., Barker J.L. NMDA-receptor activation increases cytosolic calcium concentration in cultured spinal cord neurons. Nature. 321:1986;519-522.
39. 2 sensitivity of cat phrenic neurogram during hypoxic respiratory depression. J. Appl. Physiol. 65:1988;736-743.
40. Melton J.E., Wasicko M.J., Neubauer J.A., Edelman N.H. Patterns of phrenic depression during progressive brain hypoxia. FASEB J. 2:1988;510.
41. Melton J.E., Neubauer J.A., Edelman N.H. GABA antagonism reverses hypoxic respiratory depression in the cat. J. Appl. Physiol. 69:1990;1296-1301.
42. Melton J.E., Oyer-Chae L., Neubauer J.A., Edelman N.H. Extracellular potassium homeostasis in the cat medulla during progressive brain hypoxia. J. Appl. Physiol. 40:1991;1477-1482.
43. Melton J.E., Yu Q.P., Neubauer J.A., Edelman N.H. Modulation of respiratory responses to carotid sinus nerve stimulation by brain hypoxia. J. Appl. Physiol. 73:1992;2166-2171.
44. Melton J.E., Chae L.O., Edelman N.H. Effects of respiratory afferent stimulation on phrenic neurogram during hypoxic gasping in the cat. J. Appl. Physiol. 75:1993;2091-2098.
45. Miller M.J., Tenney S.M. Hypoxia-induced tachypnea in carotid-deafferented cats. Respir. Physiol. 23:1975;31-39.
46. Mitra J., Dev N.B., Romaniuk J.R., Trivedi R., Prabhakar N.R., Cherniack N.S. Cardiorespiratory changes induced by vertebral artery injection of sodium cyanide in cats. Respir. Physiol. 87:1992;49-61.
47. Neubauer J.A., Simone A., Edelman N.H. Role of brain lactic acidosis in hypoxic depression of respiration. J. Appl. Physiol. 65:1988;1324-1331.
48. Neubauer J.A., Melton J.E., Edelman N.H. Modulation of respiration during brain hypoxia. J. Appl. Physiol. 68:1990;441-451.
49. Oyer-Chae L., Melton J.E., Neubauer J.A., Edelman N.H. Triangularis sterni and phrenic nerve responses to progressive brain hypoxia. J. Appl. Physiol. 72:1992;1522-1528.
50. Oyer-Chae L., Melton J.E., Neubauer J.A., Edelman N.H. Phrenic and sympathetic nerve responses to glutamergic blockade during normoxia and hypoxia. J. Appl. Physiol. 74:1993;1954-1963.
51. Ramirez J.M., Quellmalz U.J.A., Wilken B., Richter D.W. The hypoxic response of neurons within the in vitro mammalian respiratory network. J. Physiol. (Lond.). 507:(2):1998;571-582.
52. Ramirez J.M., Schwarzacher S.W., Pierrefiche O., Olivera B.M. Selective lesion of the cat pre-Bötzinger complex in vivo eliminates breathing but not gasping. J. Physiol. (Lond.). 507:(3):1998;895-907.
53. Reckling J.C., Feldman J.L. Pre-Bötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60:1998;385-405.
54. Richter D.W., Bischoff A., Anders K., Bellingham M., Windhorst U. Response of medullary respiratory network of the rat to hypoxia. J. Physiol. (Lond.). 443:1991;231-256.
55. Rohlicek C.V, Polosa C. Hypoxic responses of sympathetic preganglionic neurons in sino-aortic-denervated cats. Am. J. Physiol. 244:1983;H681-H686.
56. Ross C.A., Ruggiero P.A., Park D.H., Joh T.H., Sved A.F., Fernandez-Pardal J., Saacerdra J.M., Reis D.J. Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J. Neurosci. 4:1984;474-494.
57. Rothman S. Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J. Neurosci. 7:1984;1884-1891.
58. Rothman S., Olney J.W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19:1986;105-111.
59. Schwarzacher S.W., Smith J.C., Richter D.W. Pre-Bötzinger complex in the cat. J. Neurophysiol. 73:1995;1452-1461.
60. A receptor by intracellular ATP in disassociated nucleus tractus solitarii neurones of rat. J. Physiol. (Lond.). 449:1992;551-572.
61. Siesjö B.K., Nilsson L. The influence of arterial hypoxemia upon labile phosphates and upon extracellular and intracellular lactate and pyruvate concentration in the rat brain. Scand. J. Clin. Lab. Invest. 27:1971;83-96.
62. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., Feldman J.L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science. 254:1991;726-729.
63. Smith J.C., Funk G.D., Johnson S.M., Feldman J.L. Cellular mechanisms generating respiratory rhythm: insights from in vitro and computational studies. Trouth C.O., Millis R., Kiwull-Schone H., Schlaefke M. Ventral Brainstem Mechanisms and Control of Respiration and Blood Pressure. 1995;463-496 Marcel Dekker, New York.
64. A but not glycine receptors in the Pre-Bötzinger region produces an augmented or gasp-like pattern in the phrenic neurogram in cats. Neurosci. Abstr. 21:1995;1877.
65. Solomon I.C., Edelman N.H., Neubauer J.A. Hypoxia stimulates ventilation following disinhibition of neurons in the pre-Bötzinger complex. Physiologist. 39:1996;185.
66. Solomon I.C., Neubauer J.A., Edelman N.H. Role of the pre-Bötzinger complex in the production of hypoxia-induced gasping. FASEB J. 12:1998;A497.
67. Solomon I.C., Edelman N.H., Neubauer J.A. Patterns of phrenic motor output evoked by chemical stimulation of neurons located in the pre-Bötzinger complex in vivo. J. Neurophysiol. 81:1999;1150-1161.
68. Solomon I.C., Edelman N.H., Neubauer J.A. Pre-Bötzinger complex functions as a central hypoxia chemosensor for respiration in vivo. J. Neurophysiol. 83:2000;2854-2868.
69. Stefani A., Pisani A., Mecuri N.B., Bernardi G., Calabresi P. Activation of metabotropic glutamate receptors inhibits calcium currents and GABA-mediated synaptic potentials in striatal neurons. J. Neurosci. 14:1994;6734-6743.
70. Stelzer A., Kay A.R., Wong R.K.S. GABA-receptor functions in hippocampal cells is maintained by phosphorylation factors. Science. 241:1988;339-341.
71. St. John W.M., Wang S.C. Response of medullary respiratory neurons to hypercapnia and isocapnic hypoxia. J. Appl. Physiol. 43:1977;812-822.
72. St. John W.M., Knuth K.V. A characterization of the respiratory pattern of gasping. J. Appl. Physiol. 50:1981;984-993.
73. St. John W.M., Bledsoe T.A., Sokol H.W. Identification of medullary loci critical for neurogenesis of gasping. J. Appl. Physiol. 56:1984;1008-1019.
74. St. John W.M., Bledsoe T.A., Tenney S.M. Characterization by stimulation of medullary mechanisms underlying gasping neurogenesis. J. Appl. Physiol. 58:1985;121-128.
75. St. John W.M. Medullary regions for neurogenesis of gasping: noeud vital or noeuds vitals? (invited review). J. Appl. Physiol. 81:1996;1865-1877.
76. Sun M.-K., Spyer K.M. Responses of rostral ventrolateral medulla spinal vasomotor neurons to chemoreceptor stimulation in rats. J. Auton. Nerv. Syst. 33:1991;79-84.
77. Sun M.-K., Jeske I.T., Reis D.J. Cyanide excites medullary sympathoexcitatory neurons in rats. Am. J. Physiol. 262:1992;R182-R189.
78. Sun M.-K., Reis D.J. Differential responses of barosensitive neurons of the rostral ventrolateral medulla to hypoxia in rats. Brain Res. 609:1993;333-337.
79. Sun M.-K., Reis D.J. Hypoxic excitation of medullary vasomotor neurons in rats are not mediated by glutamate or nitric oxide. Neurosci. Lett. 157:1993;219-222.
80. Sun M.-K., Reis D.J. Central neural mechanisms mediating excitation of sympathetic neurons by hypoxia. Prog. Neurobiol. 44:1994;197-219.
81. 2+ currents in pacemaker neurones of rat rostral ventrolateral medulla in vitro. J. Physiol. (Lond.). 476:1994;101-116.
82. Sun M.-K., Reis D.J. Hypoxia selectively excites vasomotor neurons of the rostral ventrolateral medulla in rats. Am. J. Physiol. 266:1994;R245-R256.
83. 2. Respir. Physiol. 29:1976;81-92.
84. Tomori Z., Fung M.-L., Donic V., Donicova V., St. John W.M. Power spectral analysis of respiratory responses to pharyngeal stimulation in cats: comparisons with eupnoea and gasping. J. Physiol. (Lond.). 485:1995;551-559.
85. Wasicko M.J., Neubauer J.A., Melton J.E., Harangozo A.M., Edelman N.H. The effect of progressive brain hypoxia on respiratory activity of the hypoglossal nerve. Fed. Proc. 46:1987;1418.
86. Wasicko M.J., Melton J.E., Neubauer J.A., Krawciw N., Edelman N.H. Cervical sympathetic and phrenic nerve responses to progressive brain hypoxia. J. Appl. Physiol. 68:1990;53-58.
87. Wood J.D., Watson W.J., Drucker A.J. The effect of hypoxia on brain gamma-aminobutyric acid levels. J. Neurochem. 15:1968;603-608.
88. Zhou D., Wasicko M.J., Hu J.-M., St. John W.M. Differing activities of medullary respiratory neurons in eupnea and gasping. J. Appl. Physiol. 70:1991;1265-1270.
89. Zorumski C.F., Thio L.L. Properties of vertebrate glutamate receptors: calcium mobilization and desensitization. Prog. Neurobiol. 39:1992;295-336.