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Role of the Median Preoptic Nucleus in Arterial Pressure Regulation and Sodium and Water Homeostasis During High Dietary Salt Intake

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Neurophysiology Aims and scope

Changes in the osmolality and level of angiotensin II (ANG II) are important peripheral signals modulating appropriate central sympathetic output and maintaining normal arterial pressure during high salt intake. The median preoptic nucleus (MnPO) receives reciprocal inputs from the subfornical organ (SFO) and organum vasculosum of the lamina terminalis (OVLT), the circumventricular organs that have been shown to be necessary in multiple central effects of changes in the osmolality and circulating ANG II directed toward the maintenance of sodium and water homeostasis. We, therefore, hypothesized that the MnPO is a crucial part of the central neuronal mechanisms mediating the blood pressure control by altered osmolality and/or ANG II signaling during chronic high dietary salt intake. Male Sprague–Dawley rats were randomly assigned to either sham (operation) or electrolytic lesion of the MnPO. After a 7-day recovery, rats were instrumented with radiotelemetric transducers and aortic flow probes for measurement of the mean arterial pressure (MAP) + heart rate (HR) and cardiac output (CO), respectively. Femoral venous catheters were also implanted to collect blood for the measurements of plasma osmolality and sodium concentration, as well as plasma renin activity. Rats were given another 10 days to recover and then were subjected to a 28-day-long study protocol that included a 7-day control period (1.0% NaCl diet) followed by 14 days of high salt (4.0% NaCl), and a 7-day recovery period (1.0% NaCl). The data showed, that despite a slight increase in the MAP observed in both MnPO-(n = 12) and sham-lesioned (n = 8) rats during the high-salt period, there were no significant differences between the MAP, HR, and CO in the two groups throughout the study protocol. These findings do not support the hypothesis that the MnPO is necessary to maintain the normal blood pressure during high dietary salt intake. However, MnPO-lesioned rats showed less sodium balance than sham-lesioned rats during the first 4 days of high salt intake. Although these results may be explained partly by the plasma hyperosmolarity and hypernatremia observed in MnPO-lesioned rats, they also shed light on the role of the MnPO in central neuronal control of renal sodium handling during chronic high dietary salt intake.

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References

  1. V. L. Brooks and J. W. Osborn, “Hormonal-sympathetic interactions in long-term regulation of arterial pressure: An hypothesis,” Am. J. Physiol., 268, R1343–R1358 (1995).

    CAS  PubMed  Google Scholar 

  2. V. L. Brooks, K. E. Scrogin, and D. F. McKeogh, “The interaction of angiotensin II and osmolality in the generation of sympathetic tone during changes in dietary salt intake. An hypothesis,” Ann. New York Acad. Sci., 940, 380–394 (2001).

    Article  CAS  Google Scholar 

  3. F. C. Luft, L. I. Rankin, D. P. Henry, et al., “Plasma and urinary norepinephrine values at extremes of sodium intake in normal man,” Hypertension, 1, 261–266 (1979).

    Article  CAS  PubMed  Google Scholar 

  4. M. Bouvier, L. Farley, and J. de Champlain, “Red blood cell catecholamine levels in normotensive and DOCA-salt hypertensive rats,” Am. J. Physiol., 253, H270–H275 (1987).

    CAS  PubMed  Google Scholar 

  5. V. M. Campese, M. S. Romoff, D. Levitan, et al., “Abnormal relationship between sodium intake and sympathetic nervous system activity in salt-sensitive patients with essential hypertension,” Kidney Int., 21, 371–378 (1982).

    Article  CAS  PubMed  Google Scholar 

  6. T. Fujita, K. Ando, and E. Ogata, “Systemic and regional hemodynamics in patients with salt-sensitive hypertension,” Hypertension, 16, 235–244 (1990).

    Article  CAS  PubMed  Google Scholar 

  7. Y. Huang and D. H. Wang, “Role of renin-angiotensinaldosterone system in salt-sensitive hypertension induced by sensory denervation,” Am. J. Physiol. (Heart Circ. Physiol.), 281, H2143–H2149 (2001).

    CAS  Google Scholar 

  8. H. K. Jin, R. H. Yang, J. M. Wyss, et al., “Intrahypothalamic clonidine infusion prevents NaCl-sensitive hypertension,” Hypertension, 18, 224–229 (1991).

    Article  CAS  PubMed  Google Scholar 

  9. J. W. Osborn, B. J. Provo, J. S. Montana 3rd, and K. A. Trostel, “Salt-sensitive hypertension caused by long-term alpha-adrenergic blockade in the rat,” Hypertension, 21, 995–999 (1993).

    Article  CAS  PubMed  Google Scholar 

  10. V. L. Brooks, J. R. Haywood, and A. K. Johnson, “Translation of salt retention to central activation of the sympathetic nervous system in hypertension,” Clin. Exp. Pharmacol. Physiol., 32, 426–432 (2005).

    Article  CAS  PubMed  Google Scholar 

  11. G. M. Toney, Q. H. Chen, M. J. Cato, and S. D. Stocker, “Central osmotic regulation of sympathetic nerve activity,” Acta Physiol. Scand., 177, 43–55 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. J. M. Adams, C. J. Madden, A. F. Sved, and S. D. Stocker, “Increased dietary salt enhances sympathoexcitatory and sympathoinhibitory responses from the rostral ventrolateral medulla,” Hypertension, 50, 354–359 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. Q. H. Chen and G. M. Toney, “AT(1)-receptor blockade in the hypothalamic PVN reduces central hyperosmolalityinduced renal sympathoexcitation,” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 281, R1844–R1853 (2001).

    CAS  Google Scholar 

  14. J. W. Osborn and B. J. Hornfeldt, “Arterial baroreceptor denervation impairs long-term regulation of arterial pressure during dietary salt loading,” Am. J. Physiol., 275, H1558–H1566 (1998).

    CAS  PubMed  Google Scholar 

  15. R. R. Miselis, “The efferent projections of the subfornical organ of the rat: A circumventricular organ within a neural network subserving water balance,” Brain Res., 230, 1–23 (1981).

    Article  CAS  PubMed  Google Scholar 

  16. C. B. Saper and D. Levisohn, “Afferent connections of the median preoptic nucleus in the rat: Anatomical evidence for a cardiovascular integrative mechanism in the anteroventral third ventricular (AV3V) region,” Brain Res., 288, 21–31 (1983).

    Article  CAS  PubMed  Google Scholar 

  17. J. Ciriello, M. M. Caverson, and F. R. Calaresu, “Lateral hypothalamic and peripheral cardiovascular afferent inputs to ventrolateral medullary neurons,” Brain Res., 347, 173–176 (1985).

    Article  CAS  PubMed  Google Scholar 

  18. Z. J. Gieroba and W. W. Blessing, “Abdominal vagal afferents excite A1 area neurons antidromically activated from the region of the supraoptic nucleus in the rabbit,” Brain Res., 616, 181–187 (1993).

    Article  CAS  PubMed  Google Scholar 

  19. Y. W. Li, Z. J. Gieroba, and W. W. Blessing, “Chemoreceptor and baroreceptor responses of A1 area neurons projecting to supraoptic nucleus,” Am. J. Physiol., 263, R310–R317 (1992).

    CAS  PubMed  Google Scholar 

  20. J. Tanaka, J. Nishimura, F. Kimura, and M. Nomura, “Noradrenergic excitatory inputs to median preoptic neurons in rats,” NeuroReport, 3, 946–948 (1992).

    Article  CAS  PubMed  Google Scholar 

  21. M. J. Westerhaus and A. D. Loewy, “Sympathetic-related neurons in the preoptic region of the rat identified by viral transneuronal labeling,” J. Comp. Neurol., 414, 361–378 (1999).

    Article  CAS  PubMed  Google Scholar 

  22. P. E. Sawchenko and L. W. Swanson, “The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat,” J. Comp. Neurol., 218, 121–144 (1983).

    Article  CAS  PubMed  Google Scholar 

  23. A. M. Zardetto-Smith, R. L. Thunhorst, M. Z. Cicha, and A. K. Johnson, “Afferent signaling and forebrain mechanisms in the behavioral control of extracellular fluid volume,” Ann. New York Acad. Sci., 689, 161–176 (1993).

    Article  CAS  Google Scholar 

  24. S. D. Stocker and G. M. Toney, “Median preoptic neurons projecting to the hypothalamic paraventricular nucleus respond to osmotic, circulating ANG II and baroreceptor input in the rat,” J. Physiol., 568, 599–615 (2005).

    Article  CAS  PubMed  Google Scholar 

  25. M. J. McKinley, E. Badoer, and B. J. Oldfield, “Intravenous angiotensin II induces fosimmunoreactivity in circumventricular organs of the lamina terminalis,” Brain Res., 594, 295–300 (1992).

    Article  CAS  PubMed  Google Scholar 

  26. B. J. Oldfield, E. Badoer, D. K. Hards, and M. J. McKinley, “Fos production in retrogradely neurons of the lamina terminalis following intravenous infusion of either hypertonic saline or angiotensin II,” Neuroscience, 60, 255–262 (1994).

    Article  CAS  PubMed  Google Scholar 

  27. P. D. Potts, Y. Hirooka, and R. A. Dampney, “Activation of brain neurons by circulating angiotensin II: Direct effects and baroreceptor-mediated secondary effects,” Neuroscience, 90, 581–594 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. N. E. Rowland, B. H. Li, A. K. Rozelle, et al., “Localization of changes in immediate early genes in brain in relation to hydromineral balance: Intravenous angiotensin II,” Brain Res. Bull., 33, 427–436 (1994).

    Article  CAS  PubMed  Google Scholar 

  29. S. D. Stocker and G. M. Toney, “Vagal afferent input alters the discharge of osmotic and ANG II-responsive median preoptic neurons projecting to the hypothalamic paraventricular nucleus,” Brain Res., 1131, 118–128 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. J. Tanaka, M. Nomura, K. Kariya, et al., “Median preoptic neurons projecting to the hypothalamic paraventricular nucleus are sensitive to blood pressure changes,” Brain Res., 605, 338–341 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. J. Tanaka, S. Hatakenaka, H. Miyakubo, and M. Nomura, “Noradrenaline release in the median preoptic nucleus area caused by hemorrhage in the rat,” Brain Res. Bull., 60, 233–240 (2003).

    Article  CAS  PubMed  Google Scholar 

  32. J. T. Cunningham, T. Beltz, R. F. Johnson, and A. K. Johnson, “The effects of ibotenate lesions of the median preoptic nucleus on experimentally-induced and circadian drinking behavior in rats,” Brain Res., 580, 325–330 (1992).

    Article  CAS  PubMed  Google Scholar 

  33. T. W. Gardiner, J. G. Verbalis, and E. M. Stricker, “Impaired secretion of vasopressin and oxytocin in rats after lesions of nucleus medianus,” Am. J. Physiol., 249, R681–R688 (1985).

    CAS  PubMed  Google Scholar 

  34. R. W. Lind and A. K. Johnson, “Subfornical organmedian preoptic connections and drinking and pressor responses to angiotensin II,” J. Neurosci., 2, 1043–1051 (1982).

    CAS  PubMed  Google Scholar 

  35. M. L. Mangiapane, T. N. Thrasher, L. C. Keil, et al., “Deficits in drinking and vasopressin secretion after lesions of the nucleus medianus,” Neuroendocrinology, 37, 73–77 (1983).

    Article  CAS  PubMed  Google Scholar 

  36. T. Ployngam and J. P. Collister, “An intact median preoptic nucleus is necessary for chronic angiotensin II-induced hypertension,” Brain Res., 1162, 69–75 (2007).

    Article  CAS  PubMed  Google Scholar 

  37. T. Ployngam and J. P. Collister, “Role of the median preoptic nucleus in chronic angiotensin II-induced hypertension,” Brain Res., 1238, 75–84 (2008).

    Article  CAS  PubMed  Google Scholar 

  38. D. M. Fine, P. Ariza-Nieto, and J. W. Osborn, “Does whole body autoregulation mediate the hemodynamic responses to increased dietary salt in rats with clamped ANG II?” Am. J. Physiol. (Heart Circ. Physiol.), 285, H2670–H2678 (2003).

    CAS  Google Scholar 

  39. K. A. Trostel, S. A. Katz, and J. W. Osborn, “Functional evidence for sympathetic nerve activity in conscious cervical spinal rats,” Am. J. Physiol., 261, R434–R441 (1991).

    CAS  PubMed  Google Scholar 

  40. D. A. Fitts, “Misuse of ANOVA with cumulative intakes,” Appetite, 46, 100–102 (2006).

    Article  PubMed  Google Scholar 

  41. E. Miyajima and R. D. Bunag, “Dietary salt loading produces baroreflex impairment and mild hypertension in rats,” Am. J. Physiol., 249, H278–H284 (1985).

    CAS  PubMed  Google Scholar 

  42. M. L. Weiss, D. E. Claassen, T. Hirai, and M. J. Kenney, “Nonuniform sympathetic nerve responses to intravenous hypertonic saline infusion,” J. Auton. Nerv. Syst., 57, 109–115 (1996).

    Article  CAS  PubMed  Google Scholar 

  43. K. E. Scrogin, E. T. Grygielko, and V. L. Brooks, “Osmolality: A physiological long-term regulator of lumbar sympathetic nerve activity and arterial pressure,” Am. J. Physiol., 276, R1579–R1586 (1999).

    CAS  PubMed  Google Scholar 

  44. S. D. Stocker, K. J. Keith, and G. M. Toney, “Acute inhibition of the hypothalamic paraventricular nucleus decreases renal sympathetic nerve activity and arterial blood pressure in water-deprived rats,” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 286, R719–R725 (2004).

    Article  CAS  Google Scholar 

  45. K. L. Freeman and V. L. Brooks, “AT(1) and glutamatergic receptors in paraventricular nucleus support blood pressure during water deprivation,” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 292, R1675–R1682 (2007).

    Article  CAS  Google Scholar 

  46. P. Shi, S. D. Stocker, and G. M. Toney, “Organum vasculosum laminae terminalis contributes to increased sympathetic nerve activity induced by central hyperosmolality,” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 293, R2279–R2289 (2007).

    Article  CAS  Google Scholar 

  47. S. L. Hochstenbach and J. Ciriello, “Effect of lesions of forebrain circumventricular organs on c-fos expression in the central nervous system to plasma hypernatremia,” Brain Res., 713, 17–28 (1996).

    Article  CAS  PubMed  Google Scholar 

  48. D. J. Sly, M. J. McKinley, and B. J. Oldfield, “Activation of kidney-directed neurons in the lamina terminalis by alterations in body fluid balance,” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 281, R1637–R1646 (2001).

    CAS  Google Scholar 

  49. Z. Xu and J. Herbert, “Regional suppression by lesions in the anterior third ventricle of c-fos expression induced by either angiotensin II or hypertonic saline,” Neuroscience, 67, 135–147 (1995).

    Article  CAS  PubMed  Google Scholar 

  50. M. D. Hendel and J. P. Collister, “Sodium balance, arterial pressure, and the role of the subfornical organ during chronic changes in dietary salt,” Am. J. Physiol. (Heart. Circ. Physiol.), 289, H426–H431 (2005).

    Article  CAS  Google Scholar 

  51. A. K. Johnson, “The sensory psychobiology of thirst and salt appetite,” Med. Sci. Sports Exerc., 39, 1388–1400 (2007).

    Article  PubMed  Google Scholar 

  52. C. M. Ferrario, I. Abe, and D. B. Averill, “Sodium and vasopressin modulation of renal sympathetic nerve activity,” Clin. Exp. Hypertension, A. 9, Suppl. 1, 59–74 (1987).

    Article  Google Scholar 

  53. J. G. Verbalis, M. P. Mangione, and E. M. Stricker, “Oxytocin produces natriuresis in rats at physiological plasma concentrations,” Endocrinology, 128, 1317–1322 (1991).

    Article  CAS  PubMed  Google Scholar 

  54. K. E. Scrogin, D. F. McKeogh, and V. L. Brooks, “Is osmolality a long-term regulator of renal sympathetic nerve activity in conscious water-deprived rats?” Am. J. Physiol. (Regul. Integrat. Comp. Physiol.), 282, R560–R568 (2002).

    CAS  Google Scholar 

  55. G. F. DiBona, “Neurogenic regulation of renal tubular sodium reabsorption,” Am. J. Physiol., 233, F73–F81 (1977).

    CAS  PubMed  Google Scholar 

  56. H. Morita, K. Ishiki, and H. Hosomi, “Effects of hepatic NaCl receptor stimulation on renal nerve activity in conscious rabbits,” Neurosci. Lett., 123, 1–3 (1991).

    Article  CAS  PubMed  Google Scholar 

  57. H. Morita, T. Matsuda, F. Furuya, et al., “Hepatorenal reflex plays an important role in natriuresis after high-NaCl food intake in conscious dogs,” Circ. Res., 72, 552–559 (1993).

    Article  CAS  PubMed  Google Scholar 

  58. Y. Nishida, I. Sugimoto, H. Morita, et al., “Suppression of renal sympathetic nerve activity during portal vein infusion of hypertonic saline,” Am. J. Physiol., 274, R97–R103 (1998).

    CAS  PubMed  Google Scholar 

  59. Y. Yasuda, K. Honda, H. Negoro, et al., “The contribution of the median preoptic nucleus to renal sympathetic nerve activity increased by intracerebroventricular injection of hypertonic saline in the rat,” Brain Res., 867, 107–114 (2000).

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Veterinary Biosciences, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota, USA

    T. Ployngam, S. A. Katz & J. P. Collister

  2. Department of Integrative Biology and Physiology, Medical School, University of Minnesota, St. Paul, Minnesota, USA

    T. Ployngam, S. A. Katz & J. P. Collister

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  1. T. Ployngam
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Ployngam, T., Katz, S.A. & Collister, J.P. Role of the Median Preoptic Nucleus in Arterial Pressure Regulation and Sodium and Water Homeostasis During High Dietary Salt Intake. Neurophysiology 44, 363–375 (2012). https://doi.org/10.1007/s11062-012-9307-8

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