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Additive Role of the Vestibular End Organ and Baroreceptors on the Regulation of Blood Pressure in Rats

  • Lan, Yan (Department of Physiology and Pathophysiology, Yanbian University College of Medicine) ;
  • Yang, Yan-Zhao (Department of Physiology and Pathophysiology, Yanbian University College of Medicine) ;
  • Jiang, Xian (Department of Physiology and Pathophysiology, Yanbian University College of Medicine) ;
  • Li, Li-Wei (Department of Physiology and Pathophysiology, Yanbian University College of Medicine) ;
  • Jin, Guang-Shi (Department of Cerebral Surgery, Yanbian University College of Clinical Medicine) ;
  • Kim, Min Sun (Department of Physiology, Wonkwang University School of Medicine and Brain Science Institute at Wonkwang University) ;
  • Park, Byung Rim (Department of Physiology, Wonkwang University School of Medicine and Brain Science Institute at Wonkwang University) ;
  • Jin, Yuan-Zhe (Department of Physiology and Pathophysiology, Yanbian University College of Medicine)
  • Received : 2013.05.22
  • Accepted : 2013.07.12
  • Published : 2013.08.30

Abstract

Contribution of the vestibular end organ to regulation of arterial pressure was quantitatively compared with the role of baroreceptors in terms of baroreflex sensitivity and c-Fos protein expression in the rostral ventrolateral medulla (RVLM). Baroreflex sensitivity and c-Fos protein expression in the RVLM were measured in conscious rats that had undergone bilateral labyrinthectomy (BL) and/or baroreceptor unloading. BL attenuated baroreflex sensitivity during intravenous infusion of sodium nitroprusside (SNP), but did not significantly affect the sensitivity following infusion of phenylephrine (PE). Baroreflex sensitivity became positive following sinoaortic denervation (SAD) during infusion of PE and attenuated sensitivity during infusion of SNP. Baroreflex sensitivity also became positive following double ablation (BL+SAD) during infusion of PE, and attenuated sensitivity during infusion of SNP. c-Fos protein expression increased significantly in the RVLM in the sham group after SNP administration. However, the BL, SAD, and SAD+BL groups showed significant decreases in c-Fos protein expression compared with that in the sham group. The SAD group showed more reduced c-Fos protein expression than that in the BL group, and the SAD+BL group showed less expression than that in the SAD group. These results suggest that the vestibular system cooperates with baroreceptors to maintain arterial pressure during hypotension but that baroreceptors regulate arterial pressure during both hypotension and hypertension. Additionally, afferent signals for maintaining blood pressure from the vestibular end organs and the baroreceptors may be integrated in the RVLM.

Keywords

References

  1. Yates BJ, Siniaia MS, Miller AD. Descending pathways necessary for vestibular influences on sympathetic and inspiratory outflow. Am J Physiol. 1995;268:R1381-1385.
  2. Kerman IA, Yates BJ, McAllen RM. Anatomic patterning in the expression of vestibulosympathetic reflexes. Am J Physiol Regul Integr Comp Physiol. 2000;279:R109-117.
  3. Yates BJ, Holmes MJ, Jian BJ. Plastic changes in processing of graviceptive signals during spaceflight potentially contribute to postflight orthostatic intolerance. J Vestib Res. 2003;13: 395-404.
  4. Radtke A, Popov K, Bronstein AM, Gresty MA. Evidence for a vestibulo-cardiac reflex in man. Lancet. 2000;356:736-737. https://doi.org/10.1016/S0140-6736(00)02635-0
  5. Ray CA. Interaction of the vestibular system and baroreflexes on sympathetic nerve activity in humans. Am J Physiol Heart Circ Physiol. 2000;279:H2399-2404.
  6. Gotoh TM, Fujiki N, Matsuda T, Gao S, Morita H. Roles of baroreflex and vestibulosympathetic reflex in controlling arterial blood pressure during gravitational stress in conscious rats. Am J Physiol Regul Integr Comp Physiol. 2004;286: R25-30.
  7. Matsuda T, Gotoh TM, Tanaka K, Gao S, Morita H. Vestibulosympathetic reflex mediates the pressor response to hypergravity in conscious rats: contribution of the diencephalon. Brain Res. 2004;1028:140-147. https://doi.org/10.1016/j.brainres.2004.09.004
  8. Tanaka K, Gotoh TM, Awazu C, Morita H. Roles of the vestibular system in controlling arterial pressure in conscious rats during a short period of microgravity. Neurosci Lett. 2006;397: 40-43. https://doi.org/10.1016/j.neulet.2005.11.052
  9. Doba N, Reis DJ. Role of the cerebellum and the vestibular apparatus in regulation of orthostatic reflexes in the cat. Circ Res. 1974;40:9-18.
  10. Edis AJ. Aortic baroreflex function in the dog. Am J Physiol. 1971;221:1352-1357.
  11. Dampney RA, Stella A, Golin R, Zanchetti A. Vagal and sinoaortic reflexes in postural control of circulation and renin release. Am J Physiol. 1979;237:H146-152.
  12. Jian BJ, Cotter LA, Emanuel BA, Cass SP, Yates BJ. Effects of bilateral vestibular lesions on orthostatic tolerance in awake cats. J Appl Physiol. 1999;86:1552-1560. https://doi.org/10.1063/1.370928
  13. Mori RL, Cotter LA, Arendt HE, Olsheski CJ, Yates BJ. Effects of bilateral vestibular nucleus lesions on cardiovascular regulation in conscious cats. J Appl Physiol. 2005;98:526-533.
  14. Tanaka K, Abe C, Awazu C, Morita H. Vestibular system plays a significant role in arterial pressure control during head-up tilt in young subjects. Auton Neurosci. 2009;148:90-96. https://doi.org/10.1016/j.autneu.2009.03.007
  15. Gribbin B, Pickering TG, Sleight P, Peto R. Effect of age and high blood pressure on baroreflex sensitivity in man. Circ Res. 1971;29:424-431. https://doi.org/10.1161/01.RES.29.4.424
  16. Dampney RA, Polson JW, Potts PD, Hirooka Y, Horiuchi J. Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell Mol Neurobiol. 2003;23:597-616. https://doi.org/10.1023/A:1025080314925
  17. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci. 2006;7:335-346.
  18. Holstein GR, Friedrich VL Jr, Kang T, Kukielka E, Martinelli GP. Direct projections from the caudal vestibular nuclei to the ventrolateral medulla in the rat. Neuroscience. 2011;175:104-117. https://doi.org/10.1016/j.neuroscience.2010.12.011
  19. Yates BJ, Miller AD. Physiological evidence that the vestibular system participates in autonomic and respiratory control. J Vestib Res. 1998;8:17-25. https://doi.org/10.1016/S0957-4271(97)00035-9
  20. Yavorcik KJ, Reighard DA, Misra SP, Cotter LA, Cass SP, Wilson TD, Yates BJ. Effects of postural changes and removal of vestibular inputs on blood flow to and from the hindlimb of conscious felines. Am J Physiol Regul Integr Comp Physiol. 2009;297:R1777-1784. https://doi.org/10.1152/ajpregu.00551.2009
  21. Barman SM, Sugiyama Y, Suzuki T, Cotter LA, DeStefino VJ, Reighard DA, Cass SP, Yates BJ. Rhythmic activity of neurons in the rostral ventrolateral medulla of conscious cats: effect of removal of vestibular inputs. Am J Physiol Regul Integr Comp Physiol. 2011;301:R937-946. https://doi.org/10.1152/ajpregu.00265.2011
  22. Park BR, Kim MS, Kim JH, Jin YZ. Effects of acute hypotension on neuronal activity in the medial vestibular nuclei of rats. Neuroreport. 2001;12:3821-3824. https://doi.org/10.1097/00001756-200112040-00044
  23. Kim MS, Kim JH, Kry D, Choi MA, Choi DO, Cho BG, Jin YZ, Lee SH, Park BR. Effects of acute hypotension on expression of cFos-like protein in the vestibular nuclei of rats. Brain Res. 2003;962:111-121. https://doi.org/10.1016/S0006-8993(02)03977-X
  24. Li XL, An Y, Jin QH, Kim MS, Park BR, Jin YZ. Changes of some amino acid concentrations in the medial vestibular nucleus of conscious rats following acute hypotension. Neurosci Lett. 2010;477:11-14. https://doi.org/10.1016/j.neulet.2010.04.023
  25. Li XL, Nian B, Jin Y, Li LW, Jin GS, Kim MS, Park BR, Jin YZ. Mechanism of glutamate receptor for excitation of medial vestibular nucleus induced by acute hypotension. Brain Res. 2012;1443:27-33. https://doi.org/10.1016/j.brainres.2012.01.020
  26. Hunt MA, Miller SW, Nielson HC, Horn KM. Intratympanic injection of sodium arsanilate (atoxyl) solution results in postural changes consistent with changes described for labyrinthectomized rats. Behav Neurosci. 1987;101:427-428. https://doi.org/10.1037/0735-7044.101.3.427
  27. Wei S, Lei M, Tong M, Ding J, Han Q, Xiao M. Acute baroreceptor unloading evokes Fos expression in anesthetized rat brain. Brain Res Bull. 2008;76:63-69. https://doi.org/10.1016/j.brainresbull.2007.12.003
  28. Kim MS, Jin BK, Chun SW, Lee MY, Lee SH, Kim JH, Park BR. Effect of MK801 on cFos-like protein expression in the medial vestibular nucleus at early stage of vestibular compensation in uvulonodullectomized rats. Neurosci Lett. 1997;231:147-150. https://doi.org/10.1016/S0304-3940(97)00550-8
  29. Yates BJ. Vestibular influences on the sympathetic nervous system. Brain Res Brain Res Rev. 1992;17:51-59. https://doi.org/10.1016/0165-0173(92)90006-8
  30. Aoki M, Sakaida Y, Tanaka K, Mizuta K, Ito Y. Evidence for vestibular dysfunction in orthostatic hypotension. Exp Brain Res. 2012;217:251-259. https://doi.org/10.1007/s00221-011-2989-0
  31. Kim MS, Choi DO, Choi MA, Kim JH, Kim KY, Lee MY, Rhee JK, Chun SW, Park BR. Immunohistochemical detection of phosphorylated form of extracellular signal-regulated kinase 1/2 in rat vestibular nuclei following hemorrhagic hypotension. Neurosci Lett. 2004;360:49-52. https://doi.org/10.1016/j.neulet.2004.02.023
  32. Junqeira FL Jr, Krieger EM. Blood pressure and sleep in the rat in normotension and in neurogenic hypertension. J Physiol. 1976;259:725-735.
  33. Ito CS, Scher AM. Hypertension following arterial baroreceptor denervation in the unanesthetized dog. Circ Res. 1981;48:576-591. https://doi.org/10.1161/01.RES.48.4.576
  34. Cowley AW Jr. The concept of autoregulation of total blood flow and its role in hypertension. Am J Med. 1980;68:906-916. https://doi.org/10.1016/0002-9343(80)90225-9
  35. Cornish KG, Gilmore JP. Sino-aortic denervation in the monkey. J Physiol. 1985;360:423-432.
  36. Julien C, Zhang ZQ, Barrès C. Role of vasoconstrictor tone in arterial pressure lability after chronic sympathectomy and sinoaortic denervation in rats. J Auton Nerv Syst. 1993;42:1-10. https://doi.org/10.1016/0165-1838(93)90336-S
  37. Woodring SF, Rossiter CD, Yates BJ. Pressor response elicited by nose-up vestibular stimulation in cats. Exp Brain Res. 1997; 113:165-168. https://doi.org/10.1007/BF02454153
  38. Ray CA. Interaction between vestibulosympathetic and skeletal muscle reflexes on sympathetic activity in humans. J Appl Physiol. 2001;90:242-247.
  39. Sharp FR, Sagar SM, Swanson RA. Metabolic mapping with cellular resolution: c-fos vs. 2-deoxyglucose. Crit Rev Neurobiol. 1993;7:205-228.
  40. Holstein GR, Friedrich VL Jr, Martinelli GP, Ogorodnikov D, Yakushin SB, Cohen B. Fos expression in neurons of the rat vestibulo-autonomic pathway activated by sinusoidal galvanic vestibular stimulation. Front Neurol. 2012;3:4.
  41. Potts PD, Polson JW, Hirooka Y, Dampney RA. Effects of sinoaortic denervation on Fos expression in the brain evoked by hypertension and hypotension in conscious rabbits. Neuroscience. 1997;77:503-520. https://doi.org/10.1016/S0306-4522(96)00459-9
  42. Choi DO, Yon CI, Choi MA, Park BR, Kim MS. Activation of vestibular neurons projecting to autonomic brain stem nuclei following acute hypotension in rats. Korean J Physiol Pharmacol. 2004;8:181-185.
  43. Murad F. Cyclic guanosine monophosphate as a mediator of vasodilation. J Clin Invest. 1986;78:1-5. https://doi.org/10.1172/JCI112536
  44. Li YW, Dampney RA. Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience. 1994;61:613-634. https://doi.org/10.1016/0306-4522(94)90439-1
  45. Okere CO, Kaba H, Seto K, Higuchi T. Intracerebroventricular injection of a nitric oxide donor attenuates fos expression in the paraventricular and supraoptic nuclei of lactating rats. Brain Res. 1999;828:104-114. https://doi.org/10.1016/S0006-8993(99)01334-7
  46. Barman SM, Gebber GL. Axonal projection patterns of ventrolateral medullospinal sympathoexcitatory neurons. J Neurophysiol. 1985;53:1551-1566.
  47. Kumada M, Terui N, Kuwaki T. Arterial baroreceptor reflex: its central and peripheral neural mechanisms. Prog Neurobiol. 1990;35:331-361. https://doi.org/10.1016/0301-0082(90)90036-G
  48. Sugiyama Y, Suzuki T, Yates BJ. Role of the rostral ventrolateral medulla (RVLM) in the patterning of vestibular system influences on sympathetic nervous system outflow to the upper and lower body. Exp Brain Res. 2011;210:515-527. https://doi.org/10.1007/s00221-011-2550-1
  49. Yates BJ, Yamagata Y, Bolton PS. The ventrolateral medulla of the cat mediates vestibulosympathetic reflexes. Brain Res. 1991;552:265-272. https://doi.org/10.1016/0006-8993(91)90091-9
  50. Destefino VJ, Reighard DA, Sugiyama Y, Suzuki T, Cotter LA, Larson MG, Gandhi NJ, Barman SM, Yates BJ. Responses of neurons in the rostral ventrolateral medulla to whole body rotations: comparisons in decerebrate and conscious cats. J Appl Physiol. 2011;110:1699-1707. https://doi.org/10.1152/japplphysiol.00180.2011

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