Nitric oxide inhibition in paraventricular nucleus on cardiovascular and autonomic modulation after exercise training in unanesthetized rats

Brain Research

Volumn 1375, Issue , 2011, Pages 68-76

  Mastelari, Rosiane Batista ^a   De Souza, Hugo Celso Dutra ^b   Lenhard, Adriane ^a   De Aguiar Corrêa, Fernando Morgan ^b   Martins Pinge, Marli Cardoso ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Arterial pressure; Brain; Heart rate variability; l NAME; Swimming; Sympathetic

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM FUNCTION; BRADYCARDIA; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR PARAMETERS; CONTROLLED STUDY; EXERCISE; FEMORAL ARTERY; HEART RATE; HEART RATE VARIABILITY; HIGH FREQUENCY OSCILLATION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; LOW FREQUENCY OSCILLATION; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SWIMMING; SYSTOLIC BLOOD PRESSURE;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; ENZYME INHIBITORS; HEART RATE; HEMODYNAMICS; MALE; MICROINJECTIONS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; SWIMMING;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 79651473048     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.12.049     Document Type: Article

References (63)

1. S. Askelrod, D. Gordon, F.A. Ubel, D.C. Shannon, A.C. Barger, and R.J. Cohen Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat to beat cardiovascular control Science 213 1981 220 222 (Pubitemid 11060568)
2. J.S. Bains, and A.V. Ferguson Nitric oxide regulates NMDA-driven GABAergic inputs to type I neurones of the rat paraventricular nucleus J. Physiol. 499 1997 733 746 (Pubitemid 27153595)
3. L.K. Becker, R.A. Santos, and M.J. Campagnole-Santos Cardiovascular effects of angiotensin II and angiotensin-(1-7) at the RVLM of trained normotensive rats Brain Res. 1040 1-2 2005 121 128 (Pubitemid 40459627)
4. C. Busnardo, C.C. Crestani, R.F. Tavares, L.B. Resstel, and F.M. Correa Cardiovascular responses to L-glutamate microinjection into the hypothalamic paraventricular nucleus are mediated by a local nitric oxide-guanylate cyclase mechanism Brain Res. 1344 2010 87 95
5. C. Cerutti, M.P. Gustin, C.Z. Paultre, M. Lo, C. Julien, M. Vincent, and J. Sassard Autonomic nervous system and cardiovascular variability in rats: a spectral analysis approach Am. J. Physiol. Heart Circ. Physiol. 261 1991 H1292 H1299
6. J.H. Coote Cardiovascular function of the paraventricular nucleus of the hypothalamus Biol. Signals 4 1995 142 149 (Pubitemid 26008685)
7. A. Daffonchio, C. Franzelli, A. Radaelli, P. Castiglioni, M. Di Rienzo, G. Mancia, and A.U. Ferrari Sympathectomy and cardiovascular spectral components in conscious normotensive rats Hypertension 25 6 1995 1287 1293
8. R.A. Dampney Functional organization of central pathways regulating the cardiovascular system Physiol. Rev. 74 1994 323 364 (Pubitemid 24127645)
9. S.B. De Abreu, A. Lenhard, A. Mehanna, H.C. de Souza, F.M. Correa, E.M. Hasser, and M.C. Martins-Pinge Role of paraventricular nucleus in exercise training-induced autonomic modulation in conscious rats Auton. Neurosci. 148 1-2 2009 28 35
10. C.G. De Souza, L.C. Michelini, and D.R. Fior-Chadi Receptor changes in the nucleus tractus solitarii of the rat after exercise training Med. Sci. Sports Exerc. 33 9 2001 1471 1476 (Pubitemid 32831435)
11. S. Di Francescomarino, A. Sciartilli, V. Di Valerio, A. Di Baldassarre, and S. Gallina The effect of physical exercise on endothelial function Sports Med. 39 10 2009 797 812
12. F.M. Dos Santos, D.P. Martins Dias, C.A. da Silva, R. Fazan Jr., and H.C. Salgado Sympathetic activity is not increased in l-NAME hypertensive rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 298 1 2010 R89 R95
13. N.J. Dun, S.L. Dun, and U. Forstermann Nitric oxide synthase immunoreactivity in rat pontine medullary neurons Neuroscience 59 1994 429 445 (Pubitemid 24098800)
14. N.J. Dun, S.L. Dun, L.L. Hwang, and U. Forstermann Infrequent co-existence of nitric oxide synthase and parvalbumin, calbindin and calretinin immunoreactivity in rat pontine neurons Neurosci. Lett. 191 1995 165 168
15. D.L. Eckberg Point:counterpoint: respiratory sinus arrhythmia is due to a central mechanism vs. respiratory sinus arrhythmia is due to the baroreflex mechanism J. Appl. Physiol. 106 5 2009 1740 1742
16. F.S. Evangelista, S.E. Martuchi, C.E. Negrão, and P.C. Brum Loss of resting bradycardia with detraining is associated with intrinsic heart rate changes Braz. J. Med. Biol. Res. 38 7 2005 1141 1146 (Pubitemid 41078976)
17. R. Furlan, S. Guzetti, and W. Crivellaro Continuous 24-hours assessment of the neural regulation os systemic arterial pressure and RR variabilities in ambulant subjects Circulation 81 1990 537 547 (Pubitemid 20055962)
18. H. Hashiguchi, S.H. Ye, F. Ross-Cisneros, and N. Alexander Central nitric oxide donors attenuate cardiovascular and central norepinephrine responses to stress Am. J. Physiol. 272 1997 R1447 R1453
19. J.P. Herman, O. Eyigor, D.R. Ziegler, and L. Jennes Expression of ionotropic glutamate receptor subunit mRNAs in the hypothalamic paraventricular nucleus of the rat J. Comp. Neurol. 422 2000 352 362 (Pubitemid 30387667)
20. J.A. Hirsh, and B. Bishop Respiratory sinus arrhythmia in humans: how breathing pattern modulates heart rate American Journal of Physiology 241 1981 H620 H629
21. T. Horn, P.M. Smith, B.E. McLaughlin, L. Bauce, G.S. Marks, Q.J. Pittman, and A.V. Ferguson Nitric oxide actions in paraventriuclar nucleus: cardiovascular and neurochemical implications Am. J. Physiol. 266 1994 306 313
22. R.M. Ichiyama, A.B. Gilber, T.G. Waldrop, and G.A. Iwamoto Changes in exercise activation of diencephalic and brainstem cardiorespiratory areas after training Brain Res. 947 2002 225 233
23. K. Jackson, H.M. Silva, W. Zhang, L.C. Michelini, and J.E. Stern Exercise training differentially affects intrinsic excitability of autonomic and neuroendocrine neurons in the hypothalamic paraventricular nucleus J. Neurophysiol. 94 2005 3211 3220 (Pubitemid 41504763)
24. R. Jankord, R.M. McAllister, V.K. Ganjam, and M.H. Laughlin Chronic inhibition of nitric oxides synthase augments the ACTH response to exercise Am. J. Physiol. Regul. Integr. Comp. Physiol. 296 2009 R728 R734
25. N. Japundzic, M.L. Grichois, P. Zitoun, D. Laude, and J.L. Elghozi Spectral analysis of blood pressure and heart rate in conscious rats: effects of autonomic blockers J. Auton. Nerv. Syst. 30 2 1990 91 100 (Pubitemid 20192822)
26. A.C. Kleiber, H. Zheng, H.D. Schultz, J.D. Peuler, and K.P. Patel Exercise training normalizes enhanced glutamate-mediated sympathetic activation from the PVN in heart failure Am. J. Physiol. Regul. Integr. Comp. Physiol. 2 2008 1 43
27. O. Kuru, U.K. Senturk, G. Koçer, S. Ozdem, O.K. Baskurt, A. Çetin, A. Vesilkaya, and F. Gunduz Effect of exercise training on resistance arteries in rats with chronic NOS inhibition J. Appl. Physiol. 107 2009 896 902
28. Y.F. Li, W.G. Mayhan, and K.P. Patel NMDA-mediated increase in renal sympathetic nerve discharge within the PVN: role of nitric oxide Am. J. Physiol. Heart Circ. Physiol. 281 2001 H2328 H2336
29. Y.F. Li, S.K. Roy, K.M. Channon, I.H. Zucker, and K.P. Patel Effect of in vivo gene transfer of nNOS in the PVN on renal nerve discharge in rats Am. J. Physiol. Heart Circ. Physiol. 282 2002 H594 H601
30. Malik Heart rate variability European Heart Journal 17 1996 354 381
31. A. Malliani, M. Pagani, F. Lombardi, and S. Cerutti Cardiovascular neuro regulation explored in the frequency domain Circulation 84 1991 1482 1494
32. A. Malliani, C. Julien, G.E. Billman, S. Cerutti, M.F. Piepoli, L. Bernardi, P. Sleight, M.A. Cohen, C.O. Tan, D. Laude, M. Elstad, K. Toska, J.M. Evans, and D.L. Eckberg Cardiovascular variability is/is not an index of autonomic control of circulation J. Appl. Physiol. 101 2006 684 688
33. M.C. Martins-Pinge, I. Baraldi-Passy, and O.U. Lopes Excitatory effects of nitric oxide within the rostral ventrolateral medulla of freely moving rats Hypertension 30 1997 704 707 (Pubitemid 27444259)
34. M.C. Martins-Pinge, P.J. Mueller, C.M. Foley, S. Friskey, C. Heesch, and E.M. Hasser Cardiovascular effects of nitric oxide and GABA in the paraventricular nucleus of the hypothalamus in conscious rats Faseb J. 18 1 2004 A668
35. M.C. Martins-Pinge, L.K. Becker, M.R.L. Garcia, D.B. Zoccal, R.V. Neto, L.S. Basso, H.C. Souza, and O.U. Lopes Attenuated pressor responses to amino acids in the rostral ventrolateral medulla after swimming training in conscious rats Auton. Neurosci. 122 2005 21 28 (Pubitemid 41476371)
36. M.C. Martins-Pinge, P.J. Mueller, C.M. Foley, C.M. Heesch, and E.M. Hasser Tonic cardiovascular effects in the PVN of conscious rats: GABA, Glutamate and nitric oxide interactions Faseb J. 19 4 2005 A598
37. A. Medeiros, E.M. Oliveira, R. Gianolla, D.E. Casarini, C.E. Negrão, and P.C. Brum Swimming training increases cardiac vagal activity and induces cardiac hypertrophy in rats Braz. J. Med. Biol. Res. 37 2004 1909 1917 (Pubitemid 40089945)
38. L.C. Michelini, and J.E. Stern Exercise-induced neuronal plasticity in central autonomic networks: role in cardiovascular control Exp. Physiol. 94 9 2009 947 960
39. A. Miyagawa, H. Okamura, and Y. Ibata Coexistence of oxytocin and NADPH-diaphorase in magnocellular neurons of the paraventricular and the supraoptic nuclei of the rat hypothalamus Neurosci. Lett. 171 1994 13 16 (Pubitemid 24142077)
40. P.J. Mueller, and E.M. Hasser Putative role of the NTS in alterations in neural control of the circulation exercise training in rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 2 2006 R383 R392
41. P.J. Mueller Exercise training attenuates increases in lumbar sympathetic nerve activity produced by stimulation of the rostral ventrolateral medulla J. Appl. Physiol. 102 2007 803 813 (Pubitemid 46220914)
42. B. Nafz, C.D. Wagner, and P.B. Persson Endogenous nitric oxide buffers blood pressure variability between 0.2 and 0.6 Hz in the conscious rat Am. J. Physiol. 272 1997 H632 H637
43. C.E. Negrão, M.C. Irigoyen, E.D. Moreira, P.C. Brum, P.M. Freire, and E.M. Krieger Effect of exercise training on RSNA, baroreflex control, and blood pressure responsiveness Am. J. Physiol. 265 2 Pt 2 1993 R365 R370
44. M. Pagani, F. Lombardi, S. Guzzetti, O. Rimoldi, R. Furlan, P. Pizzinelli, G. Sandrone, G. Malfatto, S. Dell'Orto, and E. Piccaluga Power spectral anlysis of heart rate and arterial pressure variability as a marker of sympatho-vagal interaction in man and conscious dog Circulation Research 59 1986 178 193 (Pubitemid 16017873)
45. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 4a ed. 1998 Academic Press New York
46. R. Rubini, A. Porta, G. Baselli, S. Cerutti, and M. Paro Power spectrum analysis of cardiovascular variability monitored by telemetry in conscious unrestrained rats J. Auton. Nerv. Syst. 45 1993 181 190 (Pubitemid 24010158)
47. I.C. Sanches, M. Sartori, L. Jorge, M.C. Irigoyen, and K. De Angelis Tonic and reflex cardiovascular autonomic control in trained-female rats Braz. J. Med. Biol. Res. 42 10 2009 942 948
48. B.M. Sayers Analysis of heart rate variability Ergonomics 16 1973 17 32
49. H.C. Souza, G. Ballejo, M.C. Salgado, V.J. Da Silva, and H.C. Salgado Cardiac sympathetic overactivity and decreased baroreflex sensitivity in l-NAME hypertensive rats Am. J. Physiol. Heart Circ. Physiol. 280 2 2001 H844 H850
50. H.C. Souza, D.M. Penteado, M.C. Martin-Pinge, O. Barbosa Neto, V.P. Teixeira, J.H. Blanco, and V.J. Silva Nitric oxide synthesis blockade increases hypertrophy and cardiac fibrosis in rats submitted to aerobic training Arq. Bras. Cardiol. 89 2 2007 88 93
51. H.C. Souza, J.E. De Araújo, M.C. Martins-Pinge, I.C. Cozza, and D.P. Martins-Dias Nitric oxide synthesis blockade reduced the baroreflex sensitivity in trained rats Auton. Neurosci. 150 1-2 2009 38 44
52. S.B. Souza, K. Flues, J. Paulini, C. Mostarda, B. Rodrigues, L.E. Souza, M.C. Irigoyen, and K. De Angelis Role of exercise training in cardiovascular autonomic dysfunction and mortality in diabetic ovariectomized rats Hypertension 50 2007 786 791 (Pubitemid 47442746)
53. J.E. Stern, Y. Li, and W. Zhang Nitric oxide: a local signalling molecule controlling the activity of pre-autonomic neurones in the paraventricular nucleus of the hypothalamus Acta Physiol. Scand. 177 1 2003 37 42 (Pubitemid 36062553)
54. J.E. Stern Nitric oxide and homeostatic control: an intracellular signalling molecule contributing to autonomic and neuroendocrine integration? Prog. Biophys. Mol. Biol. 84 2004 197 215 (Pubitemid 38215212)
55. L.W. Swanson, and P.E. Sawchenko Hypothalamic integration: organization of the paraventricular and supraoptic nuclei Annu. Rev. Neurosci. 6 1983 269 324 (Pubitemid 13101466)
56. L.W. Swanson, P.E. Sawchenko, S.J. Wiegand, and J.L. Price Separate neurons in the paraventricular nucleus project to the median eminence and to the medulla or spinal cord Brain Res. 198 1980 190 195 (Pubitemid 10002684)
57. Task Force Of The European Society Of Cardiology And The North American Society Of Pacing And Electrophysiology Heart rate variability: standards of measurement, physiological interpretation and clinical use Circulation 93 1996 1043 1065
58. G.C. Tezini, L.C. Silveira, K.D. Maida, J.H. Blanco, and H.C. Souza The effect of ovariectomy on cardiac autonomic control in rats submitted to aerobic physical training Auton. Neurosci. 143 1-2 2008 5 11
59. A. Zanesco, and E. Antunes Effects of exercise training on the cardiovascular system: pharmacological approaches Pharmacol. Ther. 114 3 2007 307 317 (Pubitemid 46850766)
60. K. Zhang, W.G. Mayhan, and K.P. Patel Nitric oxide within the paraventricular nucleus mediates changes in renal sympathetic nerve activity Am. J. Physiol. 273 1997 864 872
61. K. Zhang, and K.P. Patel Effect of nitric oxide within the paraventricular nucleus on renal sympathetic nerve discharge: role of GABA Am. J. Physiol. Regul. Integr. Comp. Physiol. 275 1998 728 734
62. K. Zhang, Y.F. Li, and K.P. Patel Blunted nitric oxide-mediated inhibition of renal nerve discharge within PVN of rats with heart failure Am. J. Physiol. Heart Circ. Physiol. 281 2001 995 1004
63. H. Zheng, Y.F. Li, K.G. Cornish, I.H. Zucker, and K.P. Patel Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure Am. J. Physiol. Heart Circ. Physiol. 288 2005 2332 2341