Respiratory modulation of premotor cardiac vagal neurons in the brainstem

Respiratory Physiology and Neurobiology

Volumn 174, Issue 1-2, 2010, Pages 102-110

  Dergacheva, Olga ^a   Griffioen, Kathleen J ^a   Neff, Robert A ^a   Mendelowitz, David ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Brainstem; Cardiac vagal activity; Heart; Respiratory modulation

Indexed keywords

AMBIGUUS NUCLEUS; BRAIN STEM; HUMAN; MEDULLA OBLONGATA; NONHUMAN; PARASYMPATHETIC TONE; PRESSORECEPTOR; PRIORITY JOURNAL; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; REVIEW; SOLITARY TRACT NUCLEUS; SYMPATHETIC FUNCTION; VAGUS NERVE;

ANIMALS; BRAIN STEM; HEART; HUMANS; MEDULLA OBLONGATA; MOTOR NEURONS; RESPIRATION; VAGUS NERVE;

EID: 78049366137     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2010.05.005     Document Type: Review

References (146)

1. Ajiki K., Murakawa Y., Yanagisawa-Miwa A., Usui M., Yamashita T., Oikawa N., Inoue H. Autonomic nervous system activity in idiopathic dilated cardiomyopathy and in hypertrophic cardiomyopathy. Am. J. Cardiol. 1993, 71:1316-1320.
2. Anderson, R.N., 2002. Deaths: Leading Causes for 2000. National Vital Statistics Reports 50.
3. Anrep G.V., Pascual F., Rossler R. Respiratory variations of the heart rate II-the central mechanism of the respiratory sinus arrythmia and the inter-relations between the central and the reflex mechanisms. Proc. R. Soc. 1936, 119:218-230.
4. Anrep G.V., Pascual F., Rossler R. Respiratory variations of the heart rate I-the reflex mechanism of the respiratory sinus arrhythmia. Proc. R. Soc. 1936, 119:191-217.
5. Baird T.M. Clinical correlates, natural history and outcome of neonatal apnoea. Semin. Neonatol. 2004, 9:205-211.
6. Bamford O., Carroll J. Dynamic ventilatory responses in rats: normal development and effects of prenatal nicotine exposure. Respir. Physiol. 1999, 117:29-40.
7. Bazzano L.A., Khan Z., Reynolds K., He J. Effect of nocturnal nasal continuous positive airway pressure on blood pressure in obstructive sleep apnea. Hypertension 2007, 50:417-423.
8. Berk J.L., Levy M.N. Profound reflex bradycardia produced by transient hypoxia or hypercapnia in man. Eur. Surg. Res. 1977, 9:75-84.
9. Berne R.M., Levy M.N. Cardiovascular Physiology 1997, Mosby, St. Louis.
10. Bocchiaro C.M., Feldman J.L. Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:4292-4295.
11. Boddy K., Dawes G.S., Fisher R., Pinter S., Robinson J.S. Foetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sheep. J. Physiol. 1974, 243:599-618.
12. Bonsignore M.R., Parati G., Insalaco G., Castiglioni P., Marrone O., Romano S., Salvaggio A., Mancia G., Bonsignore G., Di Rienzo M. Baroreflex control of heart rate during sleep in severe obstructive sleep apnoea: effects of acute CPAP. Eur. Respir. J. 2006, 27:128-135.
13. 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.
14. Bouairi E., Neff R., Evans C., Gold A., Andresen M.C., Mendelowitz D. Respiratory sinus arrhythmia in freely moving and anesthetized rats. J. Appl. Physiol. 2004, 97:1431-1436.
15. Bradley T.D., Floras J.S. Obstructive sleep apnoea and its cardiovascular consequences. Lancet 2009, 373:82-93.
16. Carlson J.T., Hedner J.A., Sellgren J., Elam M., Wallin B.G. Depressed baroreflex sensitivity in patients with obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 1996, 154:1490-1496.
17. Castellini M.A., Rea L.D., Sanders J.L., Castellini J.M., Zenteno-Savin T. Developmental changes in cardiorespiratory patterns of sleep-associated apnea in northern elephant seals. Am. J. Physiol. 1994, 267:R1294-R1301.
18. Cheng Z., Powley T.L. Nucleus ambiguus projections to cardiac ganglia of rat atria: an anterograde tracing study. J. Comp. Neurol. 2000, 424:588-606.
19. Cohn H.E., Piasecki G.J., Jackson B.T. The effect of fetal heart rate on cardiovascular function during hypoxemia. Am. J. Obstet. Gynecol. 1980, 138:1190-1199.
20. Coleman T.G. Arterial baroreflex control of heart rate in the conscious rat. Am. J. Physiol. 1980, 238:H515-H520.
21. Daly M.B., Korner P.I., Angell-James J.E., Oliver J.R. Cardiovascular-respiratory reflex interactions between carotid bodies and upper-airways receptors in the monkey. Am. J. Physiol. 1978, 234:H293-H299.
22. Daly M.D. Some reflex cardioinhibitory responses in the cat and their modulation by central inspiratory neuronal activity. J. Physiol. 1991, 439:559-577.
23. Davidson N.S., Goldner S., McCloskey D.I. Respiratory modulation of barareceptor and chemoreceptor reflexes affecting heart rate and cardiac vagal efferent nerve activity. J. Physiol. 1976, 259:523-530.
24. de Burgh Daly M., Elsner R., Angell-James J.E. Cardiorespiratory control by carotid chemoreceptors during experimental dives in the seal. Am. J. Physiol. 1977, 232:H508-H516.
25. Dergacheva O., Griffioen K.J., Wang X., Kamendi H., Gorini C., Mendelowitz D. 5-HT(2) receptor subtypes mediate different long-term changes in GABAergic activity to parasympathetic cardiac vagal neurons in the nucleus ambiguus. Neuroscience 2007, 149:696-705.
26. Dergacheva O., Kamendi H., Wang X., Pinol R.A., Frank J., Gorini C., Jameson H., Lovett-Barr M.R., Mendelowitz D. 5-HT2 receptors modulate excitatory neurotransmission to cardiac vagal neurons within the nucleus ambiguus evoked during and after hypoxia. Neuroscience 2009, 164:1191-1198.
27. Dergacheva O., Kamendi H., Wang X., Pinol R.M., Frank J., Jameson H., Gorini C., Mendelowitz D. The role of 5-HT3 and other excitatory receptors in central cardiorespiratory responses to hypoxia: implications for sudden infant death syndrome. Pediatr. Res. 2009, 65:625-630.
28. Deshpande P., Khurana A., Hansen P., Wilkins D., Thach B.T. Failure of autoresuscitation in weanling mice: significance of cardiac glycogen and heart rate regulation. J. Appl. Physiol. 1999, 87:203-210.
29. Eckberg D.L. Human sinus arrhythmia as an index of vagal cardiac outflow. J. Appl. Physiol. 1983, 54:961-966.
30. Eckberg D.L. The human respiratory gate. J. Physiol. 2003, 548:339-352.
31. Eckberg D.L., Drabinsky M., Braunwald E. Defective cardiac parasympathetic control in patients with heart disease. N. Engl. J. Med. 1971, 285:877-883.
32. Eckberg D.L., Orshan C.R. Respiratory and baroreceptor reflex interactions in man. J. Clin. Invest. 1977, 59:780-785.
33. Elghozi J.L., Laude D., Girard A. Effects of respiration on blood pressure and heart rate variability in humans. Clin. Exp. Pharmacol. Physiol. 1991, 18:735-742.
34. Erickson J.T., Millhorn D.E. 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. 1994, 348:161-182.
35. Evans C., Baxi S., Neff R.A., Venkatesan P., Mendelowitz D. Synaptic activation of cardiac vagal neurons by capsaicin sensitive and insensitive sensory neurons. Brain Res. 2003, 979:210-215.
36. Evans C., Wang J., Neff R., Mendelowitz D. Hypoxia recruits a respiratory-related excitatory pathway to brainstem premotor cardiac vagal neurons in animals exposed to prenatal nicotine. Neuroscience 2005, 133:1073-1079.
37. Evrengul H., Tanriverdi H., Kose S., Amasyali B., Kilic A., Celik T., Turhan H. The relationship between heart rate recovery and heart rate variability in coronary artery disease. Ann. Noninvasive Electrocardiol. 2006, 11:154-162.
38. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 2003, 26:239-266.
39. Ferguson D.W., Berg W.J., Sanders J.S. Clinical and hemodynamic correlates of sympathetic nerve activity in normal humans and patients with heart failure: evidence from direct microneurographic recordings. J. Am. Coll. Cardiol. 1990, 16:1125-1134.
40. Fewell J.E., Smith F.G. Perinatal nicotine exposure impairs ability of newborn rats to autoresuscitate from apnea during hypoxia. J. Appl. Physiol. 1998, 85:2066-2074.
41. Fewell J.E., Smith F.G., Vienna K.Y.N. Prenatal exposure to nicotine impairs protective responses of rat pups to hypoxia in an age dependent manner. Respir. Physiol. 2001, 127:61-73.
42. Frank J.G., Jameson H.S., Gorini C., Mendelowitz D. Mapping and identification of GABAergic neurons in transgenic mice projecting to cardiac vagal neurons in the nucleus ambiguus using photo-uncaging. J. Neurophysiol. 2009, 101:1755-1760.
43. Fuller D.D., Zabka A.G., Baker T.L., Mitchell G.S. Physiological and genomic consequences of intermittent hypoxia selected contribution: phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. 2001, 90:2001-2006.
44. Gargaglioni L.H., Bicego K.C., Nucci T.B., Branco L.G. Serotoninergic receptors in the anteroventral preoptic region modulate the hypoxic ventilatory response. Respir. Physiol. Neurobiol. 2006, 153:1-13.
45. Gennser G., Marsal K., Brantmark B. Maternal smoking and fetal breathing movements. Am. J. Obstet. Gynecol. 1975, 123:861-867.
46. Gilbey M.P., Jordan D., Richter D.W., Spyer K.M. Synaptic mechanisms involved in the inspiratory modulation of vagal cardio-inhibitory neurones in the cat. J. Physiol. 1984, 356:65-78.
47. Griffioen K.J., Gorini C., Jameson H., Mendelowitz D. Purinergic P2X receptors mediate excitatory transmission to cardiac vagal neurons in the nucleus ambiguus after hypoxia. Hypertension 2007, 50:75-81.
48. Griffioen K.J., Kamendi H.W., Gorini C.J., Bouairi E., Mendelowitz D. Reactive oxygen species mediate central cardiorespiratory network responses to acute intermittent hypoxia. J. Neurophysiol. 2007, 97:2059-2066.
49. 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.
50. Guntheroth W.G., Kawabori I. Hypoxic apnea and gasping. J. Clin. Invest. 1975, 56:1371-1377.
51. Haglund B., Cnattingius S. Cigarette smoking as a risk factor for sudden infant death syndrome: a population-based study. Am. J. Public Health 1990, 80:29-32.
52. Hathorn M.K. Respiratory sinus arrhythmia in new-born infants. J. Physiol. 1987, 385:1-12.
53. Hayano J., Yasuma F., Okada A., Mukai S., Fujinami T. Respiratory sinus arrhythmia. A phenomenon improving pulmonary gas exchange and circulatory efficiency. Circulation 1996, 94:842-847.
54. Hayashi M., Nagasaka T. Hypoxic tachycardia in hypoxia-acclimated rats. Jpn. J. Physiol. 1982, 32:149-152.
55. Hellman L.M., Johnson H.L., Tolles W.E., Jones E.H. Some factors affecting the fetal heart rate. Am. J. Obstet. Gynecol. 1961, 82:1055-1063.
56. Heymans, C., Neil, E., 1958. Reflexogenic Areas of the Cardiovascular System. Churchill, London.
57. Hirsch J.A., Bishop B. Respiratory sinus arrhythmia in humans: how breathing pattern modulates heart rate. Am. J. Physiol. 1981, 241:H620-H629.
58. Hrushesky W.J. Quantitative respiratory sinus arrhythmia analysis. A simple noninvasive, reimbursable measure of cardiac wellness and dysfunction. Ann. N. Y. Acad. Sci. 1991, 618:67-101.
59. Huang Z.G., Griffioen K.J., Wang X., Dergacheva O., Kamendi H., Gorini C., Bouairi E., Mendelowitz D. Differential control of central cardiorespiratory interactions by hypercapnia and the effect of prenatal nicotine. J. Neurosci. 2006, 26:21-29.
60. Huang Z.G., Griffioen K.J., Wang X., Dergacheva O., Kamendi H., Gorini C., Mendelowitz D. Nicotinic receptor activation occludes purinergic control of central cardiorespiratory network responses to hypoxia/hypercapnia. J. Neurophysiol. 2007, 98:2429-2438.
61. Hull S.S., Vanoli E., Adamson P.B., De Ferrari G.M., Foreman R.D., Schwartz P.J. Do increases in markers of vagal activity imply protection from sudden death? The case of scopolamine. Circulation 1995, 91:2516-2519.
62. Ikenoue T., Martin C.B., Murata Y., Ettinger B.B., Lu P.S. Effect of acute hypoxemia and respiratory acidosis on the fetal heart rate in monkeys. Am. J. Obstet. Gynecol. 1981, 141:797-806.
63. Inoue K., Miyake S., Kumashiro M., Ogata H., Yoshimura O. Power spectral analysis of heart rate variability in traumatic quadriplegic humans. Am. J. Physiol. 1990, 258:H1722-H1726.
64. Inukai T., Kobayashi I., Kobayashi T., Ishii A., Yamaguchi T., Yamaguchi Y., Iwashita A., Ohshima K., Shimomura Y., Kobayashi S. Parasympathetic nervous system activity in hypothyroidism determined by R-R interval variations on electrocardiogram. J. Intern. Med. 1990, 228:431-434.
65. Izzo P.N., Deuchars J., Spyer K.M. Localization of cardiac vagal preganglionic motoneurones in the rat: immunocytochemical evidence of synaptic inputs containing 5-hydroxytryptamine. J. Comp. Neurol. 1993, 327:572-583.
66. Jordan D., Khalid M.E., Schneiderman N., Spyer K.M. The location and properties of preganglionic vagal cardiomotor neurones in the rabbit. Pflugers Arch. 1982, 395:244-250.
67. Julius S., Valentini M. Consequences of the increased autonomic nervous drive in hypertension, heart failure and diabetes. Blood Press. Suppl. 1998, 3:5-13.
68. Kamendi H.W., Cheng Q., Dergacheva O., Gorini C., Jameson H.S., Wang X., McIntosh J.M., Mendelowitz D. Abolishment of serotonergic neurotransmission to cardiac vagal neurons during and after hypoxia and hypercapnia with prenatal nicotine exposure. J. Neurophysiol. 2009, 101:1141-1150.
69. Kato M., Adachi T., Koshino Y., Somers V.K. Obstructive sleep apnea and cardiovascular disease. Circ. J. 2009, 73:1363-1370.
70. Kollai M., Koizumi K. Reciprocal and non-reciprocal action of the vagal and sympathetic nerves innervating the heart. J. Auton. Nerv. Syst. 1979, 1:33-52.
71. Kunze D.L. Reflex discharge patterns of cardiac vagal efferent fibres. J. Physiol. 1972, 222:1-15.
72. La Rovere M.T., Specchia G., Mortara A., Schwartz P.J. Baroreflex sensitivity, clinical correlates, and cardiovascular mortality among patients with a first myocardial infarction. A prospective study. Circulation 1988, 78:816-824.
73. 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.
74. Levy M.N., Zieske H. Autonomic control of cardiac pacemaker activity and atrioventricular transmission. J. Appl. Physiol. 1969, 27:465-470.
75. Lewis A.B., Donovan M., Platzker A.C. Cardiovascular responses to autonomic blockade in hypoxemic fetal lambs. Biol. Neonate 1980, 37:233-242.
76. Lin M., Ai J., Li L., Huang C., Chapleau M.W., Liu R., Gozal D., Wead W.B., Wurster R.D., Cheng Z.J. Structural remodeling of nucleus ambiguus projections to cardiac ganglia following chronic intermittent hypoxia in C57BL/6J mice. J. Comp. Neurol. 2008, 509:103-117.
77. Lin M., Liu R., Gozal D., Wead W.B., Chapleau M.W., Wurster R., Cheng Z.J. Chronic intermittent hypoxia impairs baroreflex control of heart rate but enhances heart rate responses to vagal efferent stimulation in anesthetized mice. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H997-H1006.
78. Loewy A.D., Spyer K.M. Central Regulation of Autonomic Functions 1990, Oxford University Press.
79. Loewy A.D., Spyer K.M. Vagal preganglionic neurons. Central Regulation of Autonomic Functions 1990, 68-87. Oxford University Press, New York. K.M. Spyer (Ed.).
80. Machado B.H., Brody M.J. Role of the nucleus ambiguus in the regulation of heart rate and arterial pressure. Hypertension 1988, 11:602-607.
81. Madden B.P., Shenoy V., Dalrymple-Hay M., Griffiths T., Millard J., Backhouse L., Clarke J., Murday A. Absence of bradycardic response to apnea and hypoxia in heart transplant recipients with obstructive sleep apnea. J. Heart Lung Transplant. 1997, 16:394-397.
82. Marin J.M., Carrizo S.J., Vicente E., Agusti A.G. Long-term cardiovascular outcomes in men with obstructive sleep apnoea-hypopnoea with or without treatment with continuous positive airway pressure: an observational study. Lancet 2005, 365:1046-1053.
83. Martin R.J., Abu-Shaweesh J.M., Baird T.M. Apnoea of prematurity. Paediatr. Respir. Rev. 2004, 5(Suppl. A):S377-S382.
84. McAllen R.M., Spyer K.M. The baroreceptor input to cardiac vagal motoneurones. J. Physiol. 1978, 282:365-374.
85. McGuire M., Zhang Y., White D.P., Ling L. Serotonin receptor subtypes required for ventilatory long-term facilitation and its enhancement after chronic intermittent hypoxia in awake rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R334-R341.
86. Mendelowitz D. Firing properties of identified parasympathetic cardiac neurons in nucleus ambiguus. Am. J. Physiol. 1996, 271:H2609-H2614.
87. Mendelowitz D. Advances in parasympathetic control of heart rate and cardiac function. News Physiol. Sci. 1999, 14:155-161.
88. Mendelowitz D., Kunze D.L. Identification and dissociation of cardiovascular neurons from the medulla for patch clamp analysis. Neurosci. Lett. 1991, 132:217-221.
89. Meny R.G., Carroll J.L., Carbone M.T., Kelly D.H. Cardiorespiratory recordings from infants dying suddenly and unexpectedly at home. Pediatrics 1994, 93:44-49.
90. Mihalevich M., Neff R.A., Mendelowitz D. Voltage-gated currents in identified parasympathetic cardiac neurons in the nucleus ambiguus. Brain Res. 1996, 739:258-262.
91. Milerad J., Rajs J., Gidlund E. Nicotine and cotinine levels in pericardial fluid in victims of SIDS. Acta Paediatr. 1994, 83:59-62.
92. Mitchell E.A., Ford R.P., Stewart A.W., Taylor B.J., Becroft D.M., Thompson J.M., Scragg R., Hassall I.B., Barry D.M., Allen E.M., et al. Smoking and the sudden infant death syndrome. Pediatrics 1993, 91:893-896.
93. Motte S., Mathieu M., Brimioulle S., Pensis A., Ray L., Ketelslegers J.M., Montano N., Naeije R., van de Borne P., Entee K.M. Respiratory-related heart rate variability in progressive experimental heart failure. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H1729-H1735.
94. Myers M.M., Fifer W., Haiken J., Stark R.I. Relationships between breathing activity and heart rate in fetal baboons. Am. J. Physiol. 1990, 258:R1479-R1485.
95. Nachmanoff D.B., Panigrahy A., Filiano J.J., Mandell F., Sleeper L.A., Valdes-Dapena M., Krous H.F., White W.F., Kinney H.C. Brainstem 3H-nicotine receptor binding in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1998, 57:1018-1025.
96. Narkiewicz K., Somers V.K. Sympathetic nerve activity in obstructive sleep apnoea. Acta Physiol. Scand. 2003, 177:385-390.
97. Neff R.A., Mihalevich M., Mendelowitz D. Stimulation of NTS activates NMDA and non-NMDA receptors in rat cardiac vagal neurons in the nucleus ambiguus. Brain Res. 1998, 792:277-282.
98. Neff R.A., Simmens S.J., Evans C., Mendelowitz D. Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J. Neurosci. 2004, 24:9261-9268.
99. Neff R.A., Wang J., Baxi S., Evans C., Mendelowitz D. Respiratory sinus arrhythmia: endogenous activation of nicotinic receptors mediates respiratory modulation of brainstem cardioinhibitory parasympathetic neurons. Circ. Res. 2003, 93:565-572.
100. Nishime E.O., Cole C.R., Blackstone E.H., Pashkow F.J., Lauer M.S. Heart rate recovery and treadmill exercise score as predictors of mortality in patients referred for exercise ECG. JAMA 2000, 284:1392-1398.
101. Nosaka S., Yamamoto T., Yasunaga K. Localization of vagal cardioinhibitory preganglionic neurons with rat brain stem. J. Comp. Neurol. 1979, 186:79-92.
102. Nucci T.B., Branco L.G., Gargaglioni L.H. 5-HT1A, but not 5-HT2 and 5-HT7, receptors in the nucleus raphe magnus modulate hypoxia-induced hyperpnoea. Acta Physiol. (Oxf) 2008, 193:403-414.
103. O'Donnell C.P., Bower E.A. Heart rate changes evoked by hypoxia in the anaesthetized, artificially ventilated cat. Exp. Physiol. 1992, 77:271-283.
104. Oka H., Mochio S., Sato K., Sato H., Katayama K. Prolongation of QTc interval and autonomic nervous dysfunction in diabetic patients. Diabetes Res. Clin. Pract. 1996, 31:63-70.
105. Parati G., Lombardi C., Narkiewicz K. Sleep apnea: epidemiology, pathophysiology, and relation to cardiovascular risk. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R1671-R1683.
106. Pardini B.J., Patel K.P., Schmid P.G., Lund D.D. Location, distribution and projections of intracardiac ganglion cells in the rat. J. Auton. Nerv. Syst. 1987, 20:91-101.
107. Pichot V., Roche F., Gaspoz J.M., Enjolras F., Antoniadis A., Minini P., Costes F., Busso T., Lacour J.R., Barthelemy J.C. Relation between heart rate variability and training load in middle-distance runners. Med. Sci. Sports Exerc. 2000, 32:1729-1736.
108. Pickering T.G., Gribbin B., Petersen E.S., Cunningham D.J., Sleight P. Effects of autonomic blockade on the baroreflex in man at rest and during exercise. Circ. Res. 1972, 30:177-185.
109. Poets C.F., Meny R.G., Chobanian M.R., Bonofiglo R.E. Gasping and other cardiorespiratory patterns during sudden infant deaths. Pediatr. Res. 1999, 45:350-354.
110. Potter E.K., McCloskey D.I. Effects of hypoxia on cardiac vagal efferent activity and on the action of the vagus nerve at the heart in the dog. J. Auton. Nerv. Syst. 1986, 17:325-329.
111. Przybylski J., Trzebski A., Przybyszewski A. Circulatory responses to acute hypoxia in spontaneously hypertensive and normotensive rats. Acta Physiol. Pol. 1980, 31:463-468.
112. Punjabi N.M. The epidemiology of adult obstructive sleep apnea. Proc. Am. Thorac. Soc. 2008, 5:136-143.
113. Rardon D.P., Bailey J.C. Parasympathetic effects on electrophysiologic properties of cardiac ventricular tissue. J. Am. Coll. Cardiol. 1983, 2:1200-1209.
114. Rentero N., Cividjian A., Trevaks D., Pequignot J.M., Quintin L., McAllen R.M. Activity patterns of cardiac vagal motoneurons in rat nucleus ambiguus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R1327-R1334.
115. Richter D.W., Schmidt-Garcon P., Pierrefiche O., Bischoff A.M., Lalley P.M. Neurotransmitters and neuromodulators controlling the hypoxic respiratory response in anaesthetized cats. J. Physiol. 1999, 514(Pt 2):567-578.
116. Richter D.W., Spyer K.M. Cardiorespiratory control. Central Regulation of Autonomic Function 1990, 189-207. Oxford University Press, New York. K.M. Spyer (Ed.).
117. Roche F., Reynaud C., Garet M., Pichot V., Costes F., Barthelemy J.C. Cardiac baroreflex control in humans during and immediately after brief exposure to simulated high altitude. Clin. Physiol. Funct. Imaging 2002, 22:301-306.
118. Routledge H.C., Chowdhary S., Townend J.N. Heart rate variability-a therapeutic target?. J. Clin. Pharm. Ther. 2002, 27:85-92.
119. Scher A.M., Young A.C. Reflex control of heart rate in the unanesthetized dog. Am. J. Physiol. 1970, 218:780-789.
120. Schuen J.N., Bamford O.S., Carroll J.L. The cardiorespiratory response to anoxia: normal development and the effect of nicotine. Respir. Physiol. 1997, 109:231-239.
121. Scremin A.M., Scremin O.U., Brechner T. Survival under hypoxia. Age dependence and effect of cholinergic drugs. Stroke 1980, 11:548-552.
122. Serani A., Lavados M., Zapata P. Cardiovascular responses to hypoxia in the spontaneously breathing cat: reflexes originating from carotid and aortic bodies. Arch. Biol. Med. Exp. (Santiago) 1983, 16:29-41.
123. Shykoff B.E., Naqvi S.S., Menon A.S., Slutsky A.S. Respiratory sinus arrhythmia in dogs. Effects of phasic afferents and chemostimulation. J. Clin. Invest. 1991, 87:1621-1627.
124. Slotkin T.A., Saleh J.L., McCook E.C., Seidler F.J. Impaired cardiac function during postnatal hypoxia in rats exposed to nicotine prenatally: implications for perinatal morbidity and mortality, and for sudden infant death syndrome. Teratology 1997, 55:177-184.
125. Slotkin T.A., Seidler F.J., Qiao D., Aldridge J.E., Tate C.A., Cousins M.M., Proskocil B.J., Sekhon H.S., Clark J.A., Lupo S.L., Spindel E.R. Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology 2005, 30:129-144.
126. Somers V.K., Dyken M.E., Mark A.L., Abboud F.M. Parasympathetic hyperresponsiveness and bradyarrhythmias during apnoea in hypertension. Clin. Auton. Res. 1992, 2:171-176.
127. Sontag L.W., Wallace R.F. The effect of cigarette smoking during pregnancy upon the fetal heart rate. Am. J. Obstet. Gynecol. 1935, 29:77-83.
128. Soukhova-O'Hare G.K., Cheng Z.J., Roberts A.M., Gozal D. Postnatal intermittent hypoxia alters baroreflex function in adult rats. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H1157-H1164.
129. Spyer K.M. Neural organisation and control of the baroreceptor reflex. Rev. Physiol. Biochem. Pharmacol. 1981, 88:24-124.
130. Spyer K.M., Gilbey M.P. Cardiorespiratory interactions in heart-rate control. Ann. N. Y. Acad. Sci. 1988, 533:350-357.
131. St-John W.M., Leiter J.C. Maternal nicotine depresses eupneic ventilation of neonatal rats. Neurosci. Lett. 1999, 267:206-208.
132. St-John W.M., Leiter J.C. Maintenance of gasping and restoration of eupnea after hypoxia is impaired following blockers of {alpha}-1 adrenergic receptors and serotonin 5HT2 receptors. J. Appl. Physiol. 2008, 104(3):665-673.
133. Stornetta R.L., Guyenet P.G., McCarty R.C. Autonomic nervous system control of heart rate during baroreceptor activation in conscious and anesthetized rats. J. Auton. Nerv. Syst. 1987, 20:121-127.
134. Takeuchi Y., Kojima M., Matsuura T., Sano Y. Serotonergic innervation on the motoneurons in the mammalian brainstem. Light and electron microscopic immunohistochemistry. Anat. Embryol. (Berl) 1983, 167:321-333.
135. Taylor E.W., Butler P.J. Nervous control of heart rate: activity in the cardiac vagus of the dogfish. J. Appl. Physiol. 1982, 53:1330-1335.
136. Teppema L.J., Veening J.G., Kranenburg A., Dahan A., Berkenbosch A., Olievier C. Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J. Comp. Neurol. 1997, 388:169-190.
137. Tryba A.K., Pena F., Ramirez J.M. Gasping activity in vitro: a rhythm dependent on 5-HT2A receptors. J. Neurosci. 2006, 26:2623-2634.
138. Vanoli E., De Ferrari G.M., Stramba-Badiale M., Hull S.S., Foreman R.D., Schwartz P.J. Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. Circ. Res. 1991, 68:1471-1481.
139. Wakamori M., Ikemoto Y., Akaike N. Effects of two volatile anesthetics and a volatile convulsant on the excitatory and inhibitory amino acid responses in dissociated CNS neurons of the rat. J. Neurophysiol. 1991, 66:2014-2021.
140. Wang J., Irnaten M., Mendelowitz D. Characteristics of spontaneous and evoked GABAergic synaptic currents in cardiac vagal neurons in rats. Brain Res. 2001, 889:78-83.
141. Wang J., Wang X., Irnaten M., Venkatesan P., Evans C., Baxi S., Mendelowitz D. Endogenous acetylcholine and nicotine activation enhances GABAergic and glycinergic inputs to cardiac vagal neurons. J. Neurophysiol. 2003, 89:2473-2481.
142. Wang X., Dergacheva O., Kamendi H., Gorini C., Mendelowitz D. 5-Hydroxytryptamine 1A/7 and 4alpha receptors differentially prevent opioid-induced inhibition of brain stem cardiorespiratory function. Hypertension 2007, 50:368-376.
143. Warner M.R., deTarnowsky J.M., Whitson C.C., Loeb J.M. Beat-by-beat modulation of AV conduction. II. Autonomic neural mechanisms. Am. J. Physiol. 1986, 251:H1134-H1142.
144. Yan B., Li L., Harden S.W., Gozal D., Lin Y., Wead W.B., Wurster R.D., Cheng Z.J. Chronic intermittent hypoxia impairs heart rate responses to AMPA and NMDA and induces loss of glutamate receptor neurons in nucleus ambiguous of F344 rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R299-R308.
145. Yan B., Soukhova-O'Hare G.K., Li L., Lin Y., Gozal D., Wead W.B., Wurster R.D., Cheng Z.J. Attenuation of heart rate control and neural degeneration in nucleus ambiguus following chronic intermittent hypoxia in young adult Fischer 344 rats. Neuroscience 2008, 153:709-720.
146. Yu Z.Y., Lumbers E.R., Gibson K.J., Stevens A.D. Effects on hypoxaemia on foetal heart rate, variability and cardiac rhythm. Clin. Exp. Pharmacol. Physiol. 1998, 25:577-584.