Oxygen-sensing neurons in the central nervous system

Journal of Applied Physiology

Volumn 96, Issue 1, 2004, Pages 367-374

  Neubauer, Judith A ^a   Sunderram, Jagadeeshan ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Brain; C1 sympathoexcitatory region; Caudal hypothalamus; Chemosensitivity; Heme oxygenase; Ion channels; Pre B tzinger complex

Indexed keywords

HEME OXYGENASE; ION CHANNEL; NITRIC OXIDE SYNTHASE; OXYGEN; POTASSIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

ADAPTATION; ALTITUDE ACCLIMATIZATION; BRAIN FUNCTION; BRAIN OXYGEN TENSION; BRAIN REGION; BRAIN STEM; CAROTID BODY CHEMORECEPTOR; CELL FUNCTION; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; CHEMORECEPTOR; CHEMOSENSITIVITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; HEART FAILURE; HUMAN; HYPOVENTILATION; HYPOXIA; LUNG BLOOD VESSEL; NERVE PROJECTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; SLEEP APNEA SYNDROME; SMOOTH MUSCLE FIBER; SYMPATHETIC TONE; THALAMUS;

EID: 0347993707     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00831.2003     Document Type: Short Survey

References (153)

1. Ackland GL, Noble R, and Hanson MA. Red nucleus inhibits breathing during hypoxia in neonates. Respir Physiol 110: 251-260, 1997.
2. Bähring R, Milligan CJ, Vardanyan V, Engeland B, Young BA, Dannenberg J, Waldschütz R, Edwards JP, Wray D, and Pongs O. Coupling of voltage-dependent potassium channel inactivation and oxidoreductase active site of Kvβ subunits. J Biol Chem 276: 22923-22929, 2001.
3. Baker TL and Mitchell GS. Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J Physiol 529: 215-219, 2000.
4. Baker-Herman TL and Mitchell GS. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22: 6239-6246, 2002.
5. Bartlett D. Origin and regulation of spontaneous deep breaths. Respir Physiol 12: 230-238, 1971.
6. + channel expressed in brainstem respiratory neurons. Respir Physiol 129: 159-174, 2001.
7. Bayliss DA, Viana F, and Berger AJ. Effects of thyrotropin-releasing hormone on rat motoneurons are mediated by G proteins. Brain Res 668: 220-229, 1994.
8. Bendixen HH, Smith GM, and Mead J. Pattern of ventilation in young adults. J Appl Physiol 19: 195-198, 1964.
9. Berquin P, Bodineau L, Gros F, and Larnicol N. Brainstem and hypothalamic areas involved in respiratory chemoreflexes: a Fos study in adults rats. Brain Res 857: 30-40, 2000.
10. Bickler PE and Donohoe PH. Adaptive responses of vertebrate neurons to hypoxia. J Exp Biol 205: 3579-3586, 2002.
11. Bickler PE, Donohoe PH, and Buck LT. Molecular adaptations for survival during anoxia: lessons from lower vertebrates. Neuroscience 8: 234-242, 2002.
12. Bissonnette JM. Mechanisms regulating hypoxic respiratory depression during fetal and postnatal life. Am J Physiol Regul Integr Comp Physiol 278: R1391-R1400, 2000.
13. Blanco CE, Dawes GS, Hanson MA, and McCooke HB. The response to hypoxia of arterial chemoreceptors in fetal sheep and newborn lambs. J Physiol 351: 25-37, 1984.
14. Boa G, Metreveli N, Li R, Taylor A, and Fletcher EC. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J Appl Physiol 83: 95-101, 1997.
15. Bodineau L, Cayetanot F, and Frugière A. Fos study of pontomedullary areas involved in the in vitro hypoxic respiratory depression. Neuroreport 12: 3913-3916, 2001.
16. Bodineau L and Larnicol N. Brainstem and hypothalamic areas activated by tissue hypoxia: Fos-like immunoreactivity induced by carbon monoxide inhalation in the rat. Neuroscience 108: 643-653, 2001.
17. Breen S, Rees S, and Walker D. Identification of brainstem neurons responding to hypoxia in fetal and newborn sheep. Brain Res 748: 107-121, 1997.
18. Brooks D, Horner RL, Kozar LG, Render-Teixeir CL, and Phillipson EA. Obstructive sleep apnea as a cause of systemic hypertension. Evidence from a canine model. J Clin Invest 99: 106-109, 1997.
19. Buckler KJ and Vaughan-Jones RD. Effects of mitochondrial uncouplers on intracellular calcium, pH and membrane potential in rat carotid body type I cells. J Physiol 513: 819-833, 1998.
20. Buckler KJ, Williams BA, and Honore E. An oxygen-, acid- and anesthetic-sensitive TASK-like background potassium channel in rat arterial chemoreceptor cells. J Physiol 525: 135-142, 2000.
21. Carlson JT, Hedner J, Elam M, Ejnell H, Sellgren J, and Wallin BG. Augmented resting sympathetic activity in awake patients with obstructive sleep apnea. Chest 103: 1763-1768, 1993.
22. Cherniack NS, von Euler C, Glogowska M, and Homma I. Characteristics and rate of occurrence of spontaneous and evoked augmented breaths. Acta Physiol Scand 111: 349-360, 1981.
23. Connelly CA, Dobbins EG, and Feldman JL. Pre-Bötzinger complex in cats: respiratory neuronal discharge patterns. Brain Res 590: 337-340, 1992.
24. Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58: 349-362, 1996.
25. 2 sensor protein in the rat carotid body. Biochem J 272: 743-747, 1990.
26. + channel modulation. J Clin Invest 91: 608-615, 1993.
27. 2) in rostral ventrolateral medulla neurons (Abstract). FASEB J 17: A14, 2003.
28. D'Agostino D, Mazza E, Hoang-Le T, and Neubauer JA. Heme oxygenase is necessary for hypoxic excitation of rostral ventrolateral medulla (RVLM) neurons (Abstract). FASEB J 15: A818, 2001.
29. Dawes GS, Gardner WN, Johnston BM, and Walker DW. Breathing in fetal lambs: the effect of brain stem section. J Physiol 335: 535-553, 1983.
30. Del Negro CA, Johnson SM, Butera JR, and Smith JC. Models of respiratory rhythm generation in the pre-Bötzinger complex. III. Experimental tests of model predictions. J Neurophysiol 86: 59-74, 2001.
31. Dillon GH and Waldrop TG. In vitro responses of caudal hypothalamus neurons to hypoxia and hypercapnia. Neuroscience 51: 941-950, 1992.
32. Dillon GH and Waldrop TG. Responses of feline caudal hypothalamic cardiorespiratory neurons to hypoxia and hypercapnia. Exp Brain Res 96: 260-272, 1993.
33. Erickson JT and Millhorn DE. Fos-like protein is induced in neurons of the medulla oblongata after stimulation of the carotid sinus nerve in awake and anesthetized rats. Brain Res 567: 11-24, 1991.
34. Erickson JT and Millhorn DE. Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J Comp Neurol 348: 161-182, 1994.
35. Fletcher EC. The relationship between systemic hypertension and obstructive sleep apnea: facts and theory. Am J Med 98: 118-128, 1995.
36. Fletcher EC. Sympathetic activity and blood pressure in the sleep apnea syndrome. Respiration 64: 22-28, 1997.
37. Fletcher EC, Lesske J, Culman J, Miller CC, and Unger T. Sympathetic denervation blocks blood pressure elevation in episodic hypoxia. Hypertension 20: 612-619, 1992.
38. Fletcher EC, Lesske J, Qian W, Miller CC III, and Unger T. Repetitive episodic hypoxia causes elevation of blood pressure in rats. Hypertension 19: 555-561, 1992.
39. Freidman JE and Haddad GG. Anoxia induces an increase in intracellular sodium in rat central neurons in vitro. Brain Res 663: 329-334, 1994.
40. French JW, Morgan BC, and Guntheroth WG. Infant monkeys - a model for crib death. Am J Dis Child 123: 480-484, 1972.
41. Garcia N, Hopkins SR, and Powell FL. Effects of intermittent hypoxia on the isocapnic hypoxic ventilatory response and erythropoiesis in humans. Respir Physiol 123: 39-49, 2000.
42. Glogowska M, Richardson PS, Widdicombe JC, and Winning AJ. The role of the vagus nerves, peripheral chemoreceptors and other afferent pathways in the genesis of augmented breaths in cats and rabbits. Respir Physiol 16: 179-196, 1972.
43. Gozal D. Sleep-disordered breathing and school performance in children. Pediatrics 102: 616-620, 1998.
44. Gozal D and Gozal E. Episodic hypoxia enhances late hypoxic ventilation in developing rats: putative role of neuronal NO synthase. Am J Physiol Regul Integr Comp Physiol 276: R17-R22, 1999.
45. Gozal D and Gozal E. Invited Review: Respiratory plasticity following intermittent hypoxia: development interactions. J Appl Physiol 90: 1995-1999, 2001.
46. Gozal D, Gozal E, Reeves SR, and Lipton AJ. Gasping and autoresuscitation in the developing rat: effect of antecedent intermittent hypoxia. J Appl Physiol 92: 1141-1144, 2002.
47. Gozal E, Gozal D, Pierce WM, Thongboonkerd V, Scherzer JA, Sachleben LR, Brittian KR, Guo SZ, Cai J, and Klein JB. Proteomic analysis of CA1 and CA3 regions of rat hippocampus and differential susceptibility to intermittent hypoxia. J Neurochem 83: 331-345, 2002.
48. Greenberg HE, Sica A, Batson D, and Scharf SM. Chronic intermittent hypoxia increases sympathetic responsiveness to hypoxia and hypercapnia. J Appl Physiol 86: 298-305, 1999.
49. Gu XQ and Haddad GG. Decreased neuronal excitability in hippocampal neurons of mice exposed to cyclic hypoxia. J Appl Physiol 91: 1245-1250, 2001.
50. Guntheroth WG and Kawabori I. Hypoxic apnea and gasping. J Clin Invest 56: 1371-1377, 1975.
51. Guyenet PG and Brown DL. Unit activity in nucleus paragigantocellularis lateralis during cerebral ischemia in the rat. Brain Res 364: 301-314, 1986.
52. Hammarstrom AK and Gage PW. Oxygen-sensing persistent sodium channels in rat hippocampus. J Physiol 529: 107-118, 2000.
53. Hammarstrom AK and Gage PW. Hypoxia and persistent sodium current. Eur Biophys J 31: 323-330, 2002.
54. + channel. J Biol Chem 276: 26499-26508, 2001.
55. Hedner J, Ejnall H, Sellgren J, Hedner T, and Wallin G. High muscle nerve sympathetic activity in the sleep apnea syndrome. J Hypertens 6: S529-S531, 1988.
56. Hedner JA, Wilcox I, Laks L, Grunstein RR, and Sullivan CE. A specific and potent pressor effect of hypoxia in patients with sleep apnea. Am Rev Respir Dis 146: 1240-1245, 1992.
57. Hirooka Y, Polson JW, Potts PD, and Dampney RA. Hyppoxia-induced Fos expression in neurons projecting to the pressor region in the rostral ventrolateral medulla. Neuroscience 80: 1209-1224, 1997.
58. Horn EM, Kramer JM, and Waldrop TG. Development of hypoxia-induced Fos expression in rat caudal hypothalamic neurons. Neuroscience 99: 711-720, 2000.
59. Horn EM and Waldrop TG. Oxygen-sensing neurons in the caudal hypothalamus and their role in cardiorespiratory control. Respir Physiol 110: 219-228, 1997.
60. Horn EM and Waldrop TG. Suprapontine control of respiration. Respir Physiol 114: 201-211, 1998.
61. Horn EM and Waldrop TG. Hypoxic augmentation of fast-inactivating and persistent sodium currents in rat caudal hypothalamic neurons. J Neurophysiol 84: 2572-2581, 2000.
62. Issa FG and Porostocky S. Effect of sleep on changes in breathing pattern accompanying sigh breaths. Respir Physiol 93: 175-187, 1993.
63. + channel independently of cytosolic factors in rat central neurons. J Physiol 481: 15-26, 1994.
64. + channel in substantia nigra neurons. J Neurosci 14: 5590-5602, 1994.
65. Kalman D, Wong B, Horvai AE, Cline MJ, and O'Lague PH. Nerve growth factor acts through camp-dependent protein kinase to increase the number of sodium channels in PC12 cells. Neuron 2: 355-366, 1990.
66. Kawai Y, Qi J, Comer AM, Gibbons H, Win J, and Lipski J. Effects of cyanide and hypoxia on membrane currents in neurons acutely dissociated from the rostral ventrolateral medulla of the rat. Brain Res 830: 246-257, 1999.
67. Keating DJ, Rychkov GY, and Roberts ML. Oxygen sensitivity in the sheep adrenal medulla: role of SK channels. Am J Physiol Cell Physiol 281: C1434-C1441, 2001.
68. Kita I, Sato-Suzuki I, Oguri M, and Arita H. Yawning responses induced by local hypoxia in the paraventricular nucleus of the rat. Behav Brain Res 117: 119-126, 2000.
69. Koos BJ, Chau A, Matsuura M, Punla O, and Kruger L. Thalamic locus mediates hypoxic inhibition of breathing in fetal sheep. J Neurophysiol 79: 2383-2393, 1998.
70. Koos BJ and Sameshima H. Effects of hypoxemia and hypercapnia on breathing movements and sleep state in sinoaortic-denervated fetal sheep. J Dev Physiol 10: 131-144, 1988.
71. Kraiczi H, Magga J, Sun XY, Ruskoaho H, Zhao X, and Hedner J. Hypoxic pressor response, cardiac size, and natriuretic peptides are modified by long-term intermittent hypoxia. J Appl Physiol 87: 2025-2031, 1999.
72. Kramer JM, Nolan PC, and Waldrop TG. In vitro responses of neurons in the central gray to hypoxia and hypercapnia. Brain Res 835: 197-203, 1999.
73. Lahiri S, Roy A, Mokashi A, Daudu PA, Li J, Baby SM, and Buerk DG. Further evidence that oxygen sensing in the carotid body involves iron and heme proteins. In: Oxygen Sensing: Responses and Adaptation to Hypoxia, edited by Lahiri S, Semenza GL, and Prabhakar NR. New York: Marcel Dekker, 2003, p. 289-298.
74. Larnicol N, Wallois F, Berquin P, Gros F, and Rose D. C-fos-like immunoreactivity in the cat's neuraxis following moderate hypoxia or hypercapnia. J Physiol (Paris) 88: 81-88, 1994.
75. Lesser SS and Lo DC. Regulation of voltage-gated ion channels by NGF and ciliary neurotrophic factor in SK-N-SH neuroblastoma cells. J Neurosci 15: 153-161, 1995.
76. Leuenberger UA, Mawji Z, Waravdekar NV, and Zwillich CW. Sympathetic neural responses to transient hypoxia are increased in obstructive sleep apnea (Abstract). Circulation 94: 1544, 1996.
77. Ling L, Fuller DD, Bach KB, Kinkead R, Olson EB Jr, and Mitchell GS. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J Neurosci 21: 5381-5388, 2001.
78. 2 in type 1 chemoreceptor cells. Science 241: 580-582, 1988.
79. López-Barneo J, Pardal R, and Ortega-Sáenz P. Cellular mechanism of oxygen sensing. Annu Rev Physiol 63: 259-287, 2001.
80. Martin-Body RL. Brain transection demonstrate the central origin of hypoxic ventilatory depression in carotid body-denervated rats. J Physiol 407: 41-52, 1988.
81. Martin-Body RL and Johnston BM. Central origin of the hypoxic depression of breathing in the newborn. Respir Physiol 71: 25-32, 1988.
82. Mazza E Jr, Edelman NH, and Neubauer JA. Hypoxic excitation in neurons cultured from the rostral ventrolateral medulla of the neonatal rat. J Appl Physiol 88: 2319-2329, 2000.
83. Mazza E, Thakker-Varia S, Tozzi C, and Neubauer JA. Expression of heme oxygenase in the oxygen-sensing regions of the rostral ventrolateral medulla. J Appl Physiol 91: 379-385, 2001.
84. Millar JA, Barratt L, Southan AP, Page KM, Fyffe RE, Robertson B, and Mathie A. A functional role for the two-pore domain potassium channel TASK-1 in cerebellar granule neurons. Proc Natl Acad Sci USA 97: 3614-3618, 2000.
85. 2+ channels in inspiratory neurons of mice and their modulation by hypoxia. J Physiol 512: 75-87, 1998.
86. Mitra J, Dev NB, Trivedi R, Amini S, Ernsberger P, and Cherniack NS. Intramedullary sodium cyanide injection on respiratory and vasomotor responses in cats. Respir Physiol 93: 71-82, 1993.
87. Miura M, Okada K, Takayama T, and Suzuki T. Neuronal expression of Fos and Jun protein in the rat medulla and spinal cord after anoxi and hypercapnic stimulations. Neurosci Lett 178: 227-230, 1994.
88. Montoro RJ, Ureña J, Fernández-Chacón R, Álvarez de Toledo G, and López-Barneo J. Oxygen sensing by ion channels and chemotransduction in single glomus cells. J Gen Physiol 107: 133-143, 1996.
89. Moore PJ, Parkes MJ, and Hanson MA. Unilateral cooling in the region of the locus coeruleus blocks the fall in respiratory output during hypoxia in anaesthetized neonatal sheep. Exp Physiol 81: 983-994, 1996.
90. Morita T, Mitsialis SA, Koike H, Liu Y, and Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem 272: 32804-32809, 1997.
91. Morita T, Perrella MA, Lee M-E, and Kaurembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA 92: 1475-1479, 1995.
92. Narkiewicz K, van de Borne PJH, Pesek CA, Dyken ME, Montano N, and Somers VK. Selective potentiation of peripheral chemoreflex sensitivity in obstructive sleep apnea. Circulation 99: 1183-1189, 1999.
93. Neubauer JA. Invited Review: Physiological and pathophysiological responses to intermittent hypoxia. J Appl Physiol 90: 1593-1599, 2001.
94. Neubauer JA, Melton JE, and Edelman NH. Modulation of respiration during brain hypoxia. J Appl Physiol 68: 441-451, 1990.
95. Neubauer JA, Sunderram F, Ritucci N, and D'Agostino D. Oxygen sensitivity of central cardiorespiratory regions. In: Oxygen Sensing: Responses and Adaptation to Hypoxia, edited by Lahiri S, Semenza GL, and Prabhakar NR. New York: Dekker, 2003, p. 633-650.
96. Nieto FJ, Young TB, Lind BK, Shahar E, Samet J, Redline S, D'Agostino RB, Newman AB, Lebowitz MD, and Pickering TG. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study (Sleep Heart Health Study). JAMA 283: 1829-1836, 2000.
97. Nolan PC and Waldrop TG. In vivo and in vitro responses of neurons in the ventrolateral medulla to hypoxia. Brain Res 630: 101-114, 1993.
98. Nolan PC and Waldrop TG. In vitro responses of VLM neurons to hypoxia after normobaric hypoxic acclimatization. Respir Physiol 105: 23-33, 1996.
99. + channels in neuroepithelial body-derived small cell carcinoma cells of the human lung. Am J Physiol Lung Cell Mol Physiol 275: L709-L716, 1998.
100. Olson EB Jr, Bohne CJ, Dwinell MR, Podolsky A, Vidruk EH, Fuller DD, Powell FL, and Mitchell GS. Ventilatory long-term facilitation in unanesthetized rats. J Appl Physiol 91: 709-716, 2001.
101. Pascual O, Morin-Surun MP, Barna B, Denavit-Saubié M, Peqquignot JM, and Champagnat J. Progesterone reverses the neuronal responses to hypoxia in rat nucleus tractus solitarius in vitro. J Physiol 544: 511-520, 2002.
102. Patel AJ and Honore E. Molecular physiology of oxygen-sensitive channels. Eur Respir J 18: 221-227, 2001.
103. + current. Neurosci Lett 119: 253-256, 1990.
104. + channels. In: Oxygen Sensing: Responses and Adaptation to Hypoxia, edited by Lahiri S, Semenza GL, and Prabhakar NR. New York: Dekker, 2003, p. 299-314.
105. Peng Y, Kline DD, Dick TE, and Prabhakar NR. Chronic intermittent hypoxia enhances carotid body chemoreceptor response to low oxygen. Adv Exp Med Biol 499: 33-38, 2001.
106. Peppard PE, Young T, Palta M, and Skatrud J. Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 342: 1378-1384, 2000.
107. Perez-Padilla R, West P, and Kryger MH. Sighs during sleep in adult humans. Sleep 6: 234-243, 1983.
108. Pollock JD, Krempin M, and Rudy B. Differential effects of NGF, FGF, EGF, cAMP and dexamethasone onneurite outgrowth and sodium channel expression in PC12 cells. J Neurosci 10: 2626-2637, 1990.
109. Prabhakar NR. Invited Review: Oxygen sensing by the carotid body chemoreceptors. J Appl Physiol 88: 2287-2295, 2000.
110. Prabhakar NR. Invited Review: Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J Appl Physiol 90: 1986-1994, 2001.
111. Prabhakar NR, Dinerman JL, Agani FH, and Snyder SH. Carbon monoxide: a role in carotid body chemoreception. Proc Natl Acad Sci USA 92: 1994-1997, 1995.
112. Ramirez JM, Quellmalz UJA, Wilken B, and Richter DW. The hypoxic response of neurons within the in vitro mammalian respiratory network. J Physiol 507: 571-582, 1998.
113. Redline S, Strauss ME, Adams N, Winters M, Roebuck T, Spry K, Rosenberg C, and Adams K. Neuropsychological function in mild sleep-disordered breathing. Sleep 20: 160-167, 1997.
114. + channels of rat chemoreceptors cells by a membrane-restricted and CO-sensitive mechanism. Circ Res 89: 430-436, 2001.
115. Roehrs T, Merrion M, Pedrosi B, Stepanski E, Zorick F, and Roth T. Neuropsychological function in obstructive sleep apnea syndrome (OSAS) compared with chronic obstructive pulmonary disease (COPD). Sleep 18: 382-388, 1995.
116. Ross CA, Ruggiero PA, Park DH, Joh TH, Sved AF, Fernandez-Pardal J, Saacerdra JM, and Reis DJ. Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing Cl adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J Neurosci 4: 474-494, 1984.
117. Row BW, Kheirandish L, Neville JJ, and Gozal D. Impaired spatial learning and hyperactivity in developing rats exposed to intermittent hypoxia. Pediatr Res 52: 449-453, 2002.
118. Rybak IA, Ptak K, Shevtsova NA, and McCrimmon DR. Sodium currents in neurons from the rostroventrolateral medulla of the rat. J Neurophysiol 90: 1635-1642, 2003.
119. Schwarzacher SW, Smith JC, and Richter DW. Pre-Bötzinger complex in the cat. J Neurophysiol 73: 1452-1461, 1995.
120. Serebrovskaya TV, Karaban IN, Kolesnikova EE, Mishunina TM, Kuzminskaya LA, Serebrovsky AN, and Swanson RJ. Human hypoxic ventilatory response with blood dopamine content under intermittent hypoxic training. Can J Physiol Pharmacol 77: 967-973, 1999.
121. Shea SA, Horner RL, Banner NR, McKenzie E, Heaton R, Yacoub MH, and Guz A. The effect of human heart-lung transplantation upon breathing at rest and during sleep. Respir Physiol 72: 131-150, 1988.
122. Shepard JW Jr. Gas exchange and hemodynamics during sleep. Med Clin North Am 69: 1234-1263, 1985.
123. h by inhalational anaesthetic and neurotransmitters in rat brainstem motoneurones. J Physiol 541: 717-729, 2002
124. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, and Feldman JL. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
125. Solomon IC, Edelman NH, and Neubauer JA. Patterns of phrenic motor output evoked by chemical stimulation of neurons located in the pre-Bötzinger complex in vivo. J Neurophysiol 81: 1150-1161, 1999.
126. Solomon IC, Edelman NH, and Neubauer JA. The pre-Bötzinger complex functions as a central hypoxia chemoreceptor for respiration in vivo. J Neurophysiol 83: 2854-2868, 2000.
127. Somers VK, Dyken ME, Clary MP, and Abboud FM. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest 96: 1897-1904, 1995.
128. + channels and hypertrophy in chromaffin-like arterial chemoreceptors. Proc Natl Acad Sci USA 89: 9469-9473, 1992.
129. 2 chemoreceptors by chronic hypoxia and cyclic AMP in vitro. J Neurosci 15: 2192-2202, 1995.
130. Summers BA, Overholt JL, and Prabhakar NR. Augmentation of L-type calcium current by hypoxia in rabbit carotid body glomus cells: evidence for a PKC-sensitive pathway. J Neurophysiol 84: 1636-1644, 2000.
131. Sun M-K, Jeske IT, and Reis DJ. Cyanide excites medullary sympathoexcitatory neurons in rats. Am J Physiol Regul Integr Comp Physiol 262: R182-R189, 1992.
132. Sun M-K and Reis DJ. Hypoxia selectively excites vasomotor neurons of rostral ventrolateral medulla in rats. Am J Physiol Regul Integr Comp Physiol 266: R245-R256, 1994.
133. 2+ currents in pacemaker neurons of rat rostral ventrolateral medulla in vitro. J Physiol 476: 101-116, 1994.
134. Sunderram J, Pandita S, Hoang-Le T, and Neubauer JA. Differential modulation of sighs and eupnea during sustained hypoxia (Abstract). Am J Respir Crit Care Med 167: A790, 2003.
135. Szaflarski J, Burtrum D, and Silverstein FS. Cerebral hypoxia-ischemia stimulates cytokine gene expression in perinatal rats. Stroke 26: 1093-1100, 1995.
136. + channel is modulated by multiple neurotransmitters in motoneurons. Neuron 25: 399-410, 2000.
137. Talley EM, Solórzano G, Lei Q, Kim D, and Bayliss DA. CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21: 7491-7505, 2001.
138. Teppema LJ, Veening JG, Kranenburg A, Dahan A, Berkenbosch A, and Olievier C. Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 388: 169-190, 1997.
139. Thach BT and Taeusch HW Jr. Sighing in newborn human infants: role of inflation-augmenting reflex. J Appl Physiol 41: 502-507, 1976.
140. + currents and depolarizes neonatal rat adrenal chromaffin cells. J Physiol 512: 421-434, 1998.
141. Van Der Aardweg JG and Karemaker JM. Repetitive apneas induce periodic hypertension in normal subjects through hypoxia. J Appl Physiol 72: 821-827, 1992.
142. Waites BA, Ackland GL, Noble R, and Hanson MA. Red nucleus lesions abolish the biphasic respiratory response to isocapnic hypoxia in decerebrate young rabbits. J Physiol 495: 217-225, 1996.
143. Wang WJ, Cheng GF, Dinger BG, and Fidone SJ. Effects of hypoxia on cyclic nucleotide formation in rabbit carotid body in vitro. Neurosci Lett 105: 164-168, 1989.
144. Wang WJ, Cheng GF, Dinger BG, and Fidone SJ. Nitric oxide mediates chemoreceptor inhibition in the cat carotid body. Neuroscience 65: 217-229, 1995.
145. Wang G, Shou P, Repucci MA, Golanov EV, and Reis DJ. Specific actions of cyanide on membrane potential and voltage-gated ion currents in rostral ventrolateral medulla neurons in rat brainstem slices. Neurosci Lett 309: 125-129, 2001.
146. + conductance. J Neurosci 22: 1256-1265, 2002.
147. Wasicko MJ, Melton JE, Neubauer JA, Krawciw N, and Edelman NH. Cervical sympathetic and phrenic nerve responses to progressive brain hypoxia. J Appl Physiol 68: 53-58, 1990.
148. Weir EK and Archer SL. The mechanism of acute hypoxic pulmonary vasoconstriction; the tale of two channels. FASEB J 9: 183-189, 1995.
149. Wulbrand H, McNamara F, and Thach BT. Suppression of a spindle electroencephalographic activity as a measure of transient arousal after spontaneous and occlusion-evoked sighs and startles. Pediatr Res 44: 767-773, 1998.
150. + channels: differential regulation in adult versus fetal rat brain. Neuroscience 94: 1231-1243, 1999.
151. Youngston C, Nurse CA, Yeger H, and Cutz E. Oxygen sensing in airway chemoreceptors. Nature 365: 153-155, 1993.
152. Zakhary R, Gaine SP, Dinerman JL, Ruat M, Flavahan NA, and Snyder SH. Heme oxygenase 2: endothelial and neuronal localization and role in endothelium-dependant relaxation. Proc Natl Acad Sci USA 93: 795-798, 1996.
153. + current. Am J Physiol Cell Physiol 271: C658-C665, 1996.