Amplified respiratory-sympathetic coupling in the spontaneously hypertensive rat: Does it contribute to hypertension?

Journal of Physiology

Volumn 587, Issue 3, 2009, Pages 597-610

  Simms, Annabel E ^a   Paton, Julian F R ^b   Pickering, Anthony E ^b   Allen, Andrew M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; ESSENTIAL HYPERTENSION; GROUPS BY AGE; HEART BRAINSTEM PREPARATION; HYPERCAPNIA; HYPOCAPNIA; NONHUMAN; ONTOGENY; PERFUSION PRESSURE; PHRENIC NERVE; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PULSE WAVE; RAT; RESPIRATORY BURST; RESPIRATORY FUNCTION; RESPIRATORY SYMPATHETIC COUPLING; SPONTANEOUSLY HYPERTENSIVE RAT; STRAIN DIFFERENCE; TISSUE PREPARATION; TRAUBE HERING PRESSURE WAVE; VASCULAR RESISTANCE; WISTAR KYOTO RAT; APNEA; AUGMENTED RESPIRATORY SYMPATHETIC COUPLING; BRAIN STEM; CHEMOSENSITIVITY; DISEASE COURSE; HYPERTENSION; MALE; NERVE CONDUCTION; NEUROMODULATION; NEWBORN; PATHOPHYSIOLOGY; PERINATAL PERIOD; RESPIRATORY SYSTEM; SYMPATHETIC TONE;

ANIMALS; BAROREFLEX; BLOOD PRESSURE; CELL RESPIRATION; HYPERCAPNIA; HYPERTENSION; HYPOCAPNIA; MALE; PHRENIC NERVE; RATS; RATS, INBRED SHR; RATS, INBRED WKY; SYMPATHETIC NERVOUS SYSTEM; VASCULAR RESISTANCE;

EID: 59749088675     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.165902     Document Type: Article

References (53)

1. Adams MA, Bobik A & Korner PI (1989). Differential development of vascular and cardiac hypertrophy in genetic hypertension. Relation to sympathetic function. Hypertension 14, 191-202.
2. Adrian E, Bronk D & Philips G (1932). Discharges in mammalian sympathetic nerves. J Physiol 74, 115-133.
3. Almog Y, Eldor S, Oz O & Akselrod S (1998). Beat-to-beat fluctuations in the BP related signals in rats: Can it contribute to the understanding of the development of hypertension? J Auton Nerv Syst 69, 39-48.
4. Badra LJ, Cooke WH, Hoag JB, Crossman AA, Kuusela TA, Tahvanainen KU & Eckberg DL (2001). Respiratory modulation of human autonomic rhythms. Am J Physiol Heart Circ Physiol 280, H2674-H2688.
5. Barman SM & Gebber GL (1976). Basis for synchronization of sympathetic and phrenic nerve discharges. Am J Physiol 231, 1601-1607.
6. Boczek-Funcke A, Habler HJ, Janig W & Michaelis M (1992). Respiratory modulation of the activity in sympathetic neurones supplying muscle, skin and pelvic organs in the cat. J Physiol 449, 333-361.
7. Boscan P, Allen AM & Paton JF (2001). Baroreflex inhibition of cardiac sympathetic outflow is attenuated by angiotensin II in the nucleus of the solitary tract. Neuroscience 103, 153-160.
8. Cabassi A, Vinci S, Calzolari M, Bruschi G & Borghetti A (1998). Regional sympathetic activity in pre-hypertensive phase of spontaneously hypertensive rats. Life Sci 62, 1111-1118.
9. Czyzyk-Krzeska MF & Trzebski A (1990). Respiratory-related discharge pattern of sympathetic nerve activity in the spontaneously hypertensive rat. J Physiol 426, 355-368.
10. Darnall RA & Guyenet P (1990). Respiratory modulation of pre- and postganglionic lumbar vasomotor sympathetic neurons in the rat. Neurosci Lett 119, 148-152.
11. CO2 modulates phrenic responses to specific carotid body hypoxia in an in situ dual perfused rat preparation. J Physiol 578, 843-857.
12. Dempsey JA, Sheel AW, St Croix CM & Morgan BJ (2002). Respiratory influences on sympathetic vasomotor outflow in humans. Resp Physiol Neurobiol 130, 3-20.
13. Dick TE, Hsieh YH, Morrison S, Coles SK & Prabhakar N (2004). Entrainment pattern between sympathetic and phrenic nerve activities in the Sprague-Dawley rat: Hypoxia-evoked sympathetic activity during expiration. Am J Physiol Regul Integr Comp Physiol 286, R1121-R1128.
14. Eckberg DL, Nerhed C & Wallin BG (1985). Respiratory modulation of muscle sympathetic and vagal cardiac outflow in man. J Physiol 365, 181-196.
15. Esler M (2000). The sympathetic system and hypertension. Am J Hypertens 13, 99S-105S.
16. Esler M, Rumantir M, Kaye D, Jennings G, Hastings J, Socratous F & Lambert G (2001). Sympathetic nerve biology in essential hypertension. Clin Exp Pharmacol Physiol 28, 986-989.
17. Gilbey MP (2001). Multiple oscillators, dynamic synchronization and sympathetic control. Clin Exp Pharmacol Physiol 28, 130-137.
18. Grassi G (1998). Role of the sympathetic nervous system in human hypertension. J Hypertens 16, 1979-1987.
19. Grassi G (2006). Sympathetic overdrive as an independent predictor of left ventricular hypertrophy: Prospective evidence. J Hypertens 24, 815-817.
20. Grisk O, Exner J, Schmidt M & Honig A (1996). Effects of acute hypoxia and hyperoxia on ventilation in spontaneously hypertensive and normotensive rat. J Auton Nerv Syst 57, 177-180.
21. Guyenet PG (2006). The sympathetic control of blood pressure. Nat Rev Neurosci 7, 335-346.
22. Habler HJ, Bartsch T & Janig W (1996). Two distinct mechanisms generate the respiratory modulation in fibre activity of the rat cervical sympathetic trunk. J Auton Nerv Syst 61, 116-122.
23. Habler HJ, Janig W, Krummel M & Peters OA (1994a). Reflex patterns in postganglionic neurons supplying skin and skeletal muscle of the rat hindlimb. J Neurophysiol 72, 2222-2236.
24. Habler HJ, Janig W & Michaelis M (1994b). Respiratory modulation in the activity of sympathetic neurones. Prog Neurobiol 43, 567-606.
25. Hardebo JE (1992). Influence of impulse pattern on noradrenaline release from sympathetic nerves in cerebral and some peripheral vessels. Acta Physiol Scand 144, 333-339.
26. Haselton JR & Guyenet PG (1989). Central respiratory modulation of medullary sympathoexcitatory neurons in rat. Am J Physiol Regul Integr Comp Physiol 256, R739-R750.
27. Hayward LF, Johnson AK & Felder RB (1999). Arterial chemoreflex in conscious normotensive and hypertensive adult rats. Am J Physiol Heart Circ Physiol 276, H1215-H1222.
28. Head GA (1995). Baroreflexes and cardiovascular regulation in hypertension. J Cardiovasc Pharmacol 26 (Suppl. 2), S7-S16.
29. Janig W (2006). The Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis. Cambridge University Press, Cambridge, UK.
30. Judy WV & Farrell SK (1979). Arterial baroreceptor reflex control of sympathetic nerve activity in the spontaneously hypertensive rat. Hypertension 1, 605-614.
31. Julius S, Krause L, Schork NJ, Mejia AD, Jones KA, van de Ven C, Johnson EH, Sekkarie MA, Kjeldsen SE, Petrin J, et al. (1991). Hyperkinetic borderline hypertension in Tecumseh, Michigan. J Hypertens 9, 77-84.
32. Korner P, Bobik A, Oddie C & Friberg P (1993). Sympathoadrenal system is critical for structural changes in genetic hypertension. Hypertension 22, 243-252.
33. Lundin S, Ricksten SE & Thoren P (1984). Renal sympathetic activity in spontaneously hypertensive rats and normotensive controls, as studied by three different methods. Acta Physiol Scand 120, 265-272.
34. Malpas SC (1998). The rhythmicity of sympathetic nerve activity. Prog Neurobiol 56, 65-96.
35. Mancia G, Grassi G, Giannattasio C & Seravalle G (1999). Sympathetic activation in the pathogenesis of hypertension and progression of organ damage. Hypertension 34, 724-728.
36. Mandel DA & Schreihofer AM (2006). Central respiratory modulation of barosensitive neurones in rat caudal ventrolateral medulla. J Physiol 572, 881-896.
37. Miao CY, Xie HH, Zhan LS & Su DF (2006). Blood pressure variability is more important than blood pressure level in determination of end-organ damage in rats. J Hypertens 24, 1125-1135.
38. Miyawaki T, Goodchild AK & Pilowsky PM (2002). Evidence for a tonic GABA-ergic inhibition of excitatory respiratory-related afferents to presympathetic neurons in the rostral ventrolateral medulla. Brain Res 924, 56-62.
39. Numao Y, Koshiya N, Gilbey MP & Spyer KM (1987). Central respiratory drive-related activity in sympathetic nerves of the rat: The regional differences. Neurosci Lett 81, 279-284.
40. Paton JF (1996). A working heart-brainstem preparation of the mouse. J Neurosci Methods 65, 63-68.
41. Pickering AE, Boscan P & Paton JF (2003). Nociception attenuates parasympathetic but not sympathetic baroreflex via NK1 receptors in the rat nucleus tractus solitarii. J Physiol 551, 589-599.
42. Pickering AE & Paton JF (2006). A decerebrate, artificially-perfused in situ preparation of rat: Utility for the study of autonomic and nociceptive processing. J Neurosci Methods 155, 260-271.
43. Pickering AE, Simms AE & Paton JF (2008). Dominant role of aortic baroreceptors in the cardiac baroreflex of the rat in situ. Auton Neurosci 142, 32-39.
44. Pilowsky P, Llewellyn-Smith IJ, Lipski J, Minson J, Arnolda L & Chalmers J (1994). Projections from inspiratory neurons of the ventral respiratory group to the subretrofacial nucleus of the cat. Brain Res 633, 63-71.
45. Richter DW & Spyer KM (1990). Cardiorespiratory control. In Central Regulation of Autonomic Functions, ed. Loewy AM & Spyer KM, pp. 189-207. Oxford University Press, New York.
46. Schlaich MP, Lambert E, Kaye DM, Krozowski Z, Campbell DJ, Lambert G, Hastings J, Aggarwal A & Esler MD (2004). Sympathetic augmentation in hypertension: Role of nerve firing, norepinephrine reuptake, and angiotensin neuromodulation. Hypertension 43, 169-175.
47. Simms AE, Paton JF & Pickering AE (2007). Hierarchical recruitment of the sympathetic and parasympathetic limbs of the baroreflex in normotensive and spontaneously hypertensive rats. J Physiol 579, 473-486.
48. St-John WM & Paton JF (2000). Characterizations of eupnea, apneusis and gasping in a perfused rat preparation. Resp Physiol 123, 201-213.
49. Strand AH, Gudmundsdottir H, Os I, Smith G, Westheim AS, Bjornerheim R & Kjeldsen SE (2006). Arterial plasma noradrenaline predicts left ventricular mass independently of blood pressure and body build in men who develop hypertension over 20 years. J Hypertens 24, 905-913.
50. Struyker-Boudier HA, Evenwel RT, Smits JF & Van Essen H (1982). Baroreflex sensitivity during the development of spontaneous hypertension in rats. Clin Sci (Lond) 62, 589-594.
51. Tatasciore A, Renda G, Zimarino M, Soccio M, Bilo G, Parati G, Schillaci G & De Caterina R (2007). Awake systolic blood pressure variability correlates with target-organ damage in hypertensive subjects. Hypertension 50, 325-332.
52. Zicha J & Kunes J (1999). Ontogenetic aspects of hypertension development: Analysis in the rat. Physiol Rev 79, 1227-1282.
53. Zoccal DB, Simms AE, Bonagamba LG, Braga VA, Pickering AE, Paton JF & Machado BH (2008). Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J Physiol 586, 3253-3265.