Baroreflex and chemoreflex controls of sympathetic activity following intermittent hypoxia

Autonomic Neuroscience: Basic and Clinical

Volumn 174, Issue 1-2, 2013, Pages 8-14

  Freet, Christopher S ^a   Stoner, James F ^a   Tang, Xiaorui ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Baroreflex; Chemoreflex; Hypoxia; Sympathetic activity

Indexed keywords

ADRENERGIC TRANSMISSION; ARTERIAL PRESSURE; BLOOD GAS; BLOOD PRESSURE REGULATION; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR FUNCTION; CHEMORECEPTOR REFLEX; COMORBIDITY; HUMAN; HYPERTENSION; INTERMITTENT HYPOXIA; PH; PHRENIC NERVE; PREGANGLIONIC NERVE CELL; PRESSORECEPTOR; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RESPIRATORY FUNCTION; REVIEW; SLEEP DISORDERED BREATHING; SYMPATHETIC NERVE; SYMPATHETIC TONE;

ANIMALS; ANOXIA; BAROREFLEX; CHEMORECEPTOR CELLS; COMORBIDITY; HUMANS; HYPERTENSION; HYPOXIA, BRAIN; SLEEP APNEA, OBSTRUCTIVE; SYMPATHETIC NERVOUS SYSTEM;

EID: 84875263398     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2012.12.005     Document Type: Review

References (113)

1. Adrian E.D., Bronk D.W., Phillips G. Discharges in mammalian sympathetic nerves. J. Physiol. 1932, 74:115-133.
2. Agarwal S.K., Calaresu F.R. Monosynaptic connection from caudal to rostral ventrolateral medulla in the baroreceptor reflex pathway. Brain Res. 1991, 555:70-74.
3. Bach K.B., Mitchell G.S. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir. Physiol. 1996, 104:251-260.
4. Baekey D.M., Molkov Y.I., Paton J.F., Rybak I.A., Dick T.E. Effect of baroreceptor stimulation on the respiratory pattern: insights into respiratory-sympathetic interactions. Respir. Physiol. Neurobiol. 2010, 174:135-145.
5. Baker T., Mitchell G.S. Episodic hypoxia, but not continuous hypoxia, leads to long term facilitation of phrenic nerve activity in rats. FASEB J. 1999, 13:A166.
6. Baker T.L., Mitchell G.S. Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J. Physiol. 2000, 529(Pt 1):215-219.
7. Bao G., Metreveli N., Li R., Taylor A., Fletcher E.C. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J. Appl. Physiol. 1997, 83:95-101.
8. Barman S.M., Gebber G.L. Sympathetic nerve rhythm of brain stem origin. Am. J. Physiol. 1980, 239:R42-R47.
9. Bernstein-Goral H., Bohn M.C. Phenylethanolamine N-methyltransferase-immunoreactive terminals synapse on adrenal preganglionic neurons in the rat spinal cord. Neuroscience 1989, 32:521-537.
10. Bixler E.O., Vgontzas A.N., Lin H.M., Ten Have T., Leiby B.E., Vela-Bueno A., Kales A. Association of hypertension and sleep-disordered breathing. Arch. Intern. Med. 2000, 160:2289-2295.
11. Bodineau L., Frugiere A., Marlot D., Wallois F. Connections between retrotrapezoid nucleus and nucleus tractus solitarii in cat. Neurosci. Lett. 2000, 280:111-114.
12. Bonsignore M.R., Parati G., Insalaco G., Marrone O., Castiglioni P., Romano S., Di Rienzo M., Mancia G., Bonsignore G. Continuous positive airway pressure treatment improves baroreflex control of heart rate during sleep in severe obstructive sleep apnea syndrome. Am. J. Respir. Crit. Care Med. 2002, 166:279-286.
13. Braga V.A., Soriano R.N., Machado B.H. Sympathoexcitatory response to peripheral chemoreflex activation is enhanced in juvenile rats exposed to chronic intermittent hypoxia. Exp. Physiol. 2006, 91:1025-1031.
14. Braga V.A., Burmeister M.A., Sharma R.V., Davisson R.L. Cardiovascular responses to peripheral chemoreflex activation and comparison of different methods to evaluate baroreflex gain in conscious mice using telemetry. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R1168-R1174.
15. Carlson J.T., Hedner J.A., Sellgren J., Elam M., Gunnar B. Depressed baroreflex sensitivity in patients with obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 1996, 154:1490-1496.
16. Chiocchio S.R., Biscardi A.M., Tramezzani J.H. Catecholamines in the carotid body of the cat. Nature 1966, 212:834-835.
17. Claps A., Torrealba F. The carotid body connections: a WGA-HRP study in the cat. Brain Res. 1988, 455:123-133.
18. Cravo S.L., Morrison S.F. The caudal ventrolateral medulla is a source of tonic sympathoinhibition. Brain Res. 1993, 621:133-136.
19. Davies R.O., Kalia M. Carotid sinus nerve projections to the brain stem in the cat. Brain Res. Bull. 1981, 6:531-541.
20. De Castro F. The discovery of sensory nature of the carotid bodies - invited article. Adv. Exp. Med. Biol. 2009, 648:1-18.
21. de Paula P.M., Tolstykh G., Mifflin S. Chronic intermittent hypoxia alters NMDA and AMPA-evoked currents in NTS neurons receiving carotid body chemoreceptor inputs. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R2259-R2265.
22. Del Rio R., Moya E.A., Iturriaga R. Carotid body and cardiorespiratory alterations in intermittent hypoxia: the oxidative link. Eur. Respir. J. 2010, 36:143-150.
23. Deuchars S.A., Spyer K.M., Gilbey M.P. Stimulation within the rostral ventrolateral medulla can evoke monosynaptic GABAergic IPSPs in sympathetic preganglionic neurons in vitro. J. Neurophysiol. 1997, 77:229-235.
24. Dick T.E., Hsieh Y.H., Wang N., Prabhakar N. Acute intermittent hypoxia increases both phrenic and sympathetic nerve activities in the rat. Exp. Physiol. 2007, 92:87-97.
25. Dyken M.E., Somers V.K., Yamada T., Ren Z.Y., Zimmerman M.B. Investigating the relationship between stroke and obstructive sleep apnea. Stroke 1996, 27:401-407.
26. Fan W., Andresen M.C. Differential frequency-dependent reflex integration of myelinated and nonmyelinated rat aortic baroreceptors. Am. J. Physiol. 1998, 275:H632-H640.
27. Fan W., Schild J.H., Andresen M.C. Graded and dynamic reflex summation of myelinated and unmyelinated rat aortic baroreceptors. Am. J. Physiol. 1999, 277:R748-R756.
28. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 2003, 26:239-266.
29. Feng J., Zhang D., Chen B. Endothelial mechanisms of endothelial dysfunction in patients with obstructive sleep apnea. Sleep Breath 2012, 16:283-294.
30. Fernandes L.G., Antunes V.R., Bonagamba L.G., Machado B.H. Pressor response to chemoreflex activation in awake rats: role of vasopressin and adrenal medulla. Physiol. Behav. 2005, 84:39-44.
31. Fitzgerald R.S. Oxygen and carotid body chemotransduction: the cholinergic hypothesis - a brief history and new evaluation. Respir. Physiol. 2000, 120:89-104.
32. Fletcher E.C., Lesske J., Behm R., Miller C.C., Stauss H., Unger T. Carotid chemoreceptors, systemic blood pressure, and chronic episodic hypoxia mimicking sleep apnea. J. Appl. Physiol. 1992, 72:1978-1984.
33. Fletcher E.C., Lesske J., Culman J., Miller C.C., Unger T. Sympathetic denervation blocks blood pressure elevation in episodic hypoxia. Hypertension 1992, 20:612-619.
34. Fletcher E.C., Bao G., Li R. Renin activity and blood pressure in response to chronic episodic hypoxia. Hypertension 1999, 34:309-314.
35. Fletcher E.C., Orolinova N., Bader M. Blood pressure response to chronic episodic hypoxia: the renin-angiotensin system. J. Appl. Physiol. 2002, 92:627-633.
36. Foster G.E., Brugniaux J.V., Pialoux V., Duggan C.T., Hanly P.J., Ahmed S.B., Poulin M.J. Cardiovascular and cerebrovascular responses to acute hypoxia following exposure to intermittent hypoxia in healthy humans. J. Physiol. 2009, 587:3287-3299.
37. Foster G.E., Hanly P.J., Ahmed S.B., Beaudin A.E., Pialoux V., Poulin M.J. Intermittent hypoxia increases arterial blood pressure in humans through a renin-angiotensin system-dependent mechanism. Hypertension 2010, 56:369-377.
38. Fu Q., Townsend N.E., Shiller S.M., Martini E.R., Okazaki K., Shibata S., Truijens M.J., Rodriguez F.A., Gore C.J., Stray-Gundersen J., Levine B.D. Intermittent hypobaric hypoxia exposure does not cause sustained alterations in autonomic control of blood pressure in young athletes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R1977-R1984.
39. Fuller D.D., Bach K.B., Baker T.L., Kinkead R., Mitchell G.S. Long term facilitation of phrenic motor output. Respir. Physiol. 2000, 121:135-146.
40. Gonzalez C., Almaraz L., Obeso A., Rigual R. Oxygen and acid chemoreception in the carotid body chemoreceptors. Trends Neurosci. 1992, 15:146-153.
41. Gonzalez C., Almaraz L., Obeso A., Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol. Rev. 1994, 74:829-898.
42. Greenberg H.E., Sica A., Batson D., Scharf S.M. Chronic intermittent hypoxia increases sympathetic responsiveness to hypoxia and hypercapnia. J. Appl. Physiol. 1999, 86:298-305.
43. Grimes P.A., Mokashi A., Stone R.A., Lahiri S. Nitric oxide synthase in autonomic innervation of the cat carotid body. J. Auton. Nerv. Syst. 1995, 54:80-86.
44. Grote L., Hedner J., Peter J.H. Mean blood pressure, pulse pressure and grade of hypertension in untreated hypertensive patients with sleep-related breathing disorder. J. Hypertens. 2001, 19:683-690.
45. Gu H., Lin M., Liu J., Gozal D., Scrogin K.E., Wurster R., Chapleau M.W., Ma X., Cheng Z.J. Selective impairment of central mediation of baroreflex in anesthetized young adult Fischer 344 rats after chronic intermittent hypoxia. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H2809-H2818.
46. Guyenet P.G., Stornetta R.L., Bayliss D.A. Retrotrapezoid nucleus and central chemoreception. J. Physiol. 2008, 586:2043-2048.
47. Habler H.J., Janig W., Michaelis M. Respiratory modulation in the activity of sympathetic neurones. Prog. Neurobiol. 1994, 43:567-606.
48. Halliwill J.R., Morgan B.J., Charkoudian N. Peripheral chemoreflex and baroreflex interactions in cardiovascular regulation in humans. J. Physiol. 2003, 552:295-302.
49. Housley G.D., Martin-Body R.L., Dawson N.J., Sinclair J.D. Brain stem projections of the glossopharyngeal nerve and its carotid sinus branch in the rat. Neuroscience 1987, 22:237-250.
50. Huang J., Lusina S., Xie T., Ji E., Xiang S., Liu Y., Weiss J.W. Sympathetic response to chemostimulation in conscious rats exposed to chronic intermittent hypoxia. Respir. Physiol. Neurobiol. 2009, 166:102-106.
51. Hudson S., Johnson C.D., Marshall J.M. Changes in muscle sympathetic nerve activity and vascular responses evoked in the spinotrapezius muscle of the rat by systemic hypoxia. J. Physiol. 2011, 589:2401-2414.
52. Imadojemu V.A., Mawji Z., Kunselman A., Gray K.S., Hogeman C.S., Leuenberger U.A. Sympathetic chemoreflex responses in obstructive sleep apnea and effects of continuous positive airway pressure therapy. Chest 2007, 131:1406-1413.
53. Janig W., Habler H.J. Neurophysiological analysis of target-related sympathetic pathways - from animal to human: similarities and differences. Acta Physiol. Scand. 2003, 177:255-274.
54. Jeske I., Reis D.J., Milner T.A. Neurons in the barosensory area of the caudal ventrolateral medulla project monosynaptically on to sympathoexcitatory bulbospinal neurons in the rostral ventrolateral medulla. Neuroscience 1995, 65:343-353.
55. Kimoff R.J., Brooks D., Horner R.L., Kozar L.F., Render-Teixeira C.L., Champagne V., Mayer P., Phillipson E.A. Ventilatory and arousal responses to hypoxia and hypercapnia in a canine model of obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 1997, 156:886-894.
56. Kline D.D. Chronic intermittent hypoxia affects integration of sensory input by neurons in the nucleus tractus solitarii. Respir. Physiol. Neurobiol. 2010, 174:29-36.
57. Kubo T., Kihara M., Misu Y. Ipsilateral but not contralateral blockade of excitatory amino acid receptors in the caudal ventrolateral medulla inhibits aortic baroreceptor reflex in rats. Naunyn Schmiedebergs Arch. Pharmacol. 1991, 343:46-51.
58. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., Prabhakar N.R. Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 2006, 91:249-286.
59. Lai C.J., Yang C.C., Hsu Y.Y., Lin Y.N., Kuo T.B. Enhanced sympathetic outflow and decreased baroreflex sensitivity are associated with intermittent hypoxia-induced systemic hypertension in conscious rats. J. Appl. Physiol. 2006, 100:1974-1982.
60. Lee K.D., Mayou R.A., Torrance R.W. The effect of blood pressure upon chemoreceptor discharge to hypoxia, and the modification of this effect by the sympathetic-adrenal system. Q. J. Exp. Physiol. Cogn. Med. Sci. 1964, 49:171-183.
61. Leuenberger U.A., Brubaker D., Quraishi S., Hogeman C.S., Imadojemu V.A., Gray K.S. Effects of intermittent hypoxia on sympathetic activity and blood pressure in humans. Auton. Neurosci. 2005, 121:87-93.
62. Lever J.D., Boyd J.D. Osmiophile granules in the glomus cells of the rabbit carotid body. Nature 1957, 179:1082-1083.
63. Ling L., Fuller D.D., Bach K.B., Kinkead R., Olson E.B., Mitchell G.S. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J. Neurosci. 2001, 21:5381-5388.
64. Lipski J., Merrill E.G. Electrophysiological demonstration of the projection from expiratory neurones in rostral medulla to contralateral dorsal respiratory group. Brain Res. 1980, 197:521-524.
65. Loeschcke H.H. Central chemosensitivity and the reaction theory. J. Physiol. 1982, 332:1-24.
66. Lohmeier T.E. The sympathetic nervous system and long-term blood pressure regulation. Am. J. Hypertens. 2001, 14:147S-154S.
67. Lohmeier T.E., Irwin E.D., Rossing M.A., Serdar D.J., Kieval R.S. Prolonged activation of the baroreflex produces sustained hypotension. Hypertension 2004, 43:306-311.
68. Lohmeier T.E., Barrett A.M., Irwin E.D. Prolonged activation of the baroreflex: a viable approach for the treatment of hypertension?. Curr. Hypertens. Rep. 2005, 7:193-198.
69. MacFarlane P.M., Mitchell G.S. Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neuroscience 2008, 152:189-197.
70. Malone S., Liu P.P., Holloway R., Rutherford R., Xie A., Bradley T.D. Obstructive sleep apnoea in patients with dilated cardiomyopathy: effects of continuous positive airway pressure. Lancet 1991, 338:1480-1484.
71. Mandel D.A., Schreihofer A.M. Central respiratory modulation of barosensitive neurones in rat caudal ventrolateral medulla. J. Physiol. 2006, 572:881-896.
72. Mandel D.A., Schreihofer A.M. Modulation of the sympathetic response to acute hypoxia by the caudal ventrolateral medulla in rats. J. Physiol. 2009, 587:461-475.
73. Marcus N.J., Li Y.L., Bird C.E., Schultz H.D., Morgan B.J. Chronic intermittent hypoxia augments chemoreflex control of sympathetic activity: role of the angiotensin II type 1 receptor. Respir. Physiol. Neurobiol. 2010, 171:36-45.
74. Mifflin S.W., Spyer K.M., Withington-Wray D.J. Baroreceptor inputs to the nucleus tractus solitarius in the cat: postsynaptic actions and the influence of respiration. J. Physiol. 1988, 399:349-367.
75. Millhorn D.E. Neural respiratory and circulatory interaction during chemoreceptor stimulation and cooling of ventral medulla in cats. J. Physiol. 1986, 370:217-231.
76. Minson J.B., Llewellyn-Smith I.J., Arnolda L.F., Pilowsky P.M., Chalmers J.P. C-fos expression in central neurons mediating the arterial baroreceptor reflex. Clin. Exp. Hypertens. 1997, 19:631-643.
77. Mitchell G.S., Baker T.L., Nanda S.A., Fuller D.D., Zabka A.G., Hodgeman B.A., Bavis R.W., Mack K.J., Olson E.B. Invited review: intermittent hypoxia and respiratory plasticity. J. Appl. Physiol. 2001, 90:2466-2475.
78. Mohsenin V. Sleep-related breathing disorders and risk of stroke. Stroke 2001, 32:1271-1278.
79. Monahan K.D., Leuenberger U.A., Ray C.A. Effect of repetitive hypoxic apnoeas on baroreflex function in humans. J. Physiol. 2006, 574:605-613.
80. Mooe T., Franklin K.A., Holmstrom K., Rabben T., Wiklund U. Sleep-disordered breathing and coronary artery disease: long-term prognosis. Am. J. Respir. Crit. Care Med. 2001, 164:1910-1913.
81. Morrison S.F., Callaway J., Milner T.A., Reis D.J. Glutamate in the spinal sympathetic intermediolateral nucleus: localization by light and electron microscopy. Brain Res. 1989, 503:5-15.
82. Narkiewicz K., Kato M., Phillips B.G., Pesek C.A., Davison D.E., Somers V.K. Nocturnal continuous positive airway pressure decreases daytime sympathetic traffic in obstructive sleep apnea. Circulation 1999, 100:2332-2335.
83. Nattie E. Why do we have both peripheral and central chemoreceptors?. J. Appl. Physiol. 2006, 100:9-10.
84. Nattie E., Li A. Central chemoreception 2005: a brief review. Auton. Neurosci. 2006, 126-127:332-338.
85. Nishida Y., Tandai-Hiruma M., Kemuriyama T., Hagisawa K. Long-term blood pressure control: is there a set-point in the brain?. J. Physiol. Sci. 2012, 62:147-161.
86. Osanai S., Akiba Y., Fujiuchi S., Nakano H., Matsumoto H., Ohsaki Y., Kikuchi K. Depression of peripheral chemosensitivity by a dopaminergic mechanism in patients with obstructive sleep apnoea syndrome. Eur. Respir. J. 1999, 13:418-423.
87. Oshima N., McMullan S., Goodchild A.K., Pilowsky P.M. A monosynaptic connection between baroinhibited neurons in the RVLM and IML in Sprague-Dawley rats. Brain Res. 2006, 1089:153-161.
88. Peng Y.J., Prabhakar N.R. Effect of two paradigms of chronic intermittent hypoxia on carotid body sensory activity. J. Appl. Physiol. 2004, 96:1236-1242. (discussion 1196).
89. Peppard P.E., Young T., Palta M., Skatrud J. Prospective study of the association between sleep-disordered breathing and hypertension. N. Engl. J. Med. 2000, 342:1378-1384.
90. Pialoux V., Hanly P.J., Foster G.E., Brugniaux J.V., Beaudin A.E., Hartmann S.E., Pun M., Duggan C.T., Poulin M.J. Effects of exposure to intermittent hypoxia on oxidative stress and acute hypoxic ventilatory response in humans. Am. J. Respir. Crit. Care Med. 2009, 180:1002-1009.
91. Pilowsky P. Good vibrations? Respiratory rhythms in the central control of blood pressure. Clin. Exp. Pharmacol. Physiol. 1995, 22:594-604.
92. Prabhakar N.R., Kumar G.K. Mechanisms of sympathetic activation and blood pressure elevation by intermittent hypoxia. Respir. Physiol. Neurobiol. 2010, 174:156-161.
93. Prabhakar N.R., Dinerman J.L., Agani F.H., Snyder S.H. Carbon monoxide: a role in carotid body chemoreception. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:1994-1997.
94. Prabhakar N.R., Kumar G.K., Nanduri J. Intermittent hypoxia augments acute hypoxic sensing via HIF-mediated ROS. Respir. Physiol. Neurobiol. 2010, 174:230-234.
95. Querido J.S., Kennedy P.M., Sheel A.W. Hyperoxia attenuates muscle sympathetic nerve activity following isocapnic hypoxia in humans. J. Appl. Physiol. 2010, 108:906-912.
96. Ramirez J.M., Schwarzacher S.W., Pierrefiche O., Olivera B.M., Richter D.W. Selective lesioning of the cat pre-Botzinger complex in vivo eliminates breathing but not gasping. J. Physiol. 1998, 507(Pt 3):895-907.
97. Reeves S.R., Gozal E., Guo S.Z., Sachleben L.R., Brittian K.R., Lipton A.J., Gozal D. Effect of long-term intermittent and sustained hypoxia on hypoxic ventilatory and metabolic responses in the adult rat. J. Appl. Physiol. 2003, 95:1767-1774.
98. Rey S., Del Rio R., Alcayaga J., Iturriaga R. Chronic intermittent hypoxia enhances cat chemosensory and ventilatory responses to hypoxia. J. Physiol. 2004, 560:577-586.
99. Sapru H.N., Krieger A.J. Carotid and aortic chemoreceptor function in the rat. J. Appl. Physiol. 1977, 42:344-348.
100. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., Feldman J.L. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 1991, 254:726-729.
101. Somers V.K., Mark A.L., Zavala D.C., Abboud F.M. Contrasting effects of hypoxia and hypercapnia on ventilation and sympathetic activity in humans. J. Appl. Physiol. 1989, 67:2101-2106.
102. Somers V.K., Mark A.L., Abboud F.M. Interaction of baroreceptor and chemoreceptor reflex control of sympathetic nerve activity in normal humans. J. Clin. Invest. 1991, 87:1953-1957.
103. Somogyi P., Minson J.B., Morilak D., Llewellyn-Smith I., McIlhinney J.R., Chalmers J. Evidence for an excitatory amino acid pathway in the brainstem and for its involvement in cardiovascular control. Brain Res. 1989, 496:401-407.
104. Sved A.F., Cano G., Card J.P. Neuroanatomical specificity of the circuits controlling sympathetic outflow to different targets. Clin. Exp. Pharmacol. Physiol. 2001, 28:115-119.
105. Tamisier R., Pepin J.L., Remy J., Baguet J.P., Taylor J.A., Weiss J.W., Levy P. 14 nights of intermittent hypoxia elevate daytime blood pressure and sympathetic activity in healthy humans. Eur. Respir. J. 2011, 37:119-128.
106. Tkacova R., Rankin F., Fitzgerald F.S., Floras J.S., Bradley T.D. Effects of continuous positive airway pressure on obstructive sleep apnea and left ventricular afterload in patients with heart failure. Circulation 1998, 98:2269-2275.
107. Turner D.L., Mitchell G.S. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J. Physiol. 1997, 499(Pt 2):543-550.
108. Vitela M., Herrera-Rosales M., Haywood J.R., Mifflin S.W. Baroreflex regulation of renal sympathetic nerve activity and heart rate in renal wrap hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R856-R862.
109. Waradekar N.V., Sinoway L.I., Zwillich C.W., Leuenberger U.A. Influence of treatment on muscle sympathetic nerve activity in sleep apnea. Am. J. Respir. Crit. Care Med. 1996, 153:1333-1338.
110. Xing T., Pilowsky P.M. Acute intermittent hypoxia in rat in vivo elicits a robust increase in tonic sympathetic nerve activity that is independent of respiratory drive. J. Physiol. 2010, 588:3075-3088.
111. Zoccal D.B., Bonagamba L.G., Oliveira F.R., Antunes-Rodrigues J., Machado B.H. Increased sympathetic activity in rats submitted to chronic intermittent hypoxia. Exp. Physiol. 2007, 92:79-85.
112. Zoccal D.B., Simms A.E., Bonagamba L.G., Braga V.A., Pickering A.E., Paton J.F., Machado B.H. Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J. Physiol. 2008, 586:3253-3265.
113. Zoccal D.B., Bonagamba L.G., Paton J.F., Machado B.H. Sympathetic-mediated hypertension of awake juvenile rats submitted to chronic intermittent hypoxia is not linked to baroreflex dysfunction. Exp. Physiol. 2009, 94:972-983.