Pregnancy increases baroreflex-independent GABAergic inhibition of the RVLM in rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 6, 2007, Pages

  Kvochina, Lyudmyla ^a   Hasser, Eileen M ^a   Heesch, Cheryl M ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Angiotensin II; Brain stem; Cardiovascular regulation; Sympathetic nerve activity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ANGIOTENSIN 1 RECEPTOR; BICUCULLINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENERVATION; FEMALE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HEART RATE; MEAN ARTERIAL PRESSURE; MEDULLA OBLONGATA; NERVE CONDUCTION; NONHUMAN; PREGNANCY; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; RAT; SYMPATHETIC NERVE;

ANIMALS; BAROREFLEX; BLOOD PRESSURE; FEMALE; GAMMA-AMINOBUTYRIC ACID; HEART RATE; MEDULLA OBLONGATA; NEURAL INHIBITION; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SYMPATHETIC NERVOUS SYSTEM;

EID: 36849064848     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00365.2007     Document Type: Article

References (72)

1. American Physiological Society. Guiding principles for research involving animals and human beings. Am J Physiol Regul Integr Comp Physiol 283: R281-R283, 2002.
2. 1a. Averill DB, Diz DI. Angiotensin peptides and baroflex control of sympathetic outflow: pathways and mechanisms of the medulla oblongata. Brain Res Bull 51: 119-128, 2000.
3. 1) receptor antagonist, attenuates pressor and sympathoexcitatory responses evoked by angiotensin II and L-glutamate in rostral ventrolateral medulla. Brain Res 665: 245-52, 1994.
4. Barron WM, Mujais SK, Zinaman M, Bravo EL, Lindheimer MD. Plasma catecholamine responses to physiologic stimuli in normal human pregnancy. Am J Obstet Gynecol 154: 80-84, 1986.
5. Belelli D, Herd MB, Mitchell EA, Peden DR, Vardy AW, Gentet L, Lambert JJ. Neuroactive steroids and inhibitory neurotransmission: mechanisms of action and physiological relevance. Neuroscience 138: 821-829, 2006.
6. Brooks VL, Kane CM, Van Winkle DM. Altered heart rate baroreflex during pregnancy: role of sympathetic and parasympathetic nervous systems. Am J Physiol Regul Integr Comp Physiol 273: R960-R966, 1997.
7. Brooks VL, Kane CM, Welch LS. Regional conductance changes during hemorrhage in pregnant and nonpregnant conscious rabbits. Am J Physiol Regul Integr Comp Physiol 277: R675-R681, 1999.
8. Brooks VL, Quesnell RR, Cumbee SR, Bishop VS. Pregnancy attenuates activity of the baroreceptor reflex. Clin Exp Pharmacol Physiol 22: 152-156, 1995.
9. Brooks VL, Quesnell RR, Kane CM, Keil LC. Hemodynamic and hormonal responses to hemorrhage in conscious rabbits at mid- and late gestation. Am J Physiol Regul Integr Comp Physiol 275: R1082-R1090, 1998.
10. Brooks VL, Welch LS, Kane CM. Role of angiotensin II in altered baroreflex function of conscious rabbits during late pregnancy. Am J Obstet Gynecol 184: 476-482, 2001.
11. Buck BJ, Kerman IA, Burghardt PR, Koch LG, Britton SL, Akil H, Watson SJ. Upregulation of GAD65 mRNA in the medulla of the rat model of metabolic syndrome. Neurosci Lett 419: 178-183, 2007.
12. Butcher RL, Collins WE, Fugo NW. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrous cycle of the rat. Endocrinology 94: 1704-1708, 1974.
13. Chan SHH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JYH. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Circ Res 97: 772-780, 2005.
14. Concas A, Mostallino MC, Porcu P, Follesa P, Barbaccia ML, Trabucchi M, Purdy RE, Grisenti P, Biggio G. Role of brain allopregnanolone in the plasticity of γ-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci USA 95: 13284-13289, 1998.
15. Crandall ME, Heesch CM. Baroreflex control of sympathetic outflow in pregnant rats: effects of captopril. Am J Physiol Regul Integr Comp Physiol 258: R1417-R1423, 1990.
16. Cravo SL, Morrison SF. The caudal ventrolateral medulla is a source of tonic sympathoinhibition. Brain Res 621: 133-136, 1993.
17. Cravo SL, Morrison SF, Reis DJ. Differentiation of two cardiovascular regions within caudal ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 261: R985-R994, 1991.
18. Curtis KS, Cunningham JT, Heesch CM. Fos expression in brain stem nuclei of pregnant rats after hydralazine-induced hypotension. Am J Physiol Regul Integr Comp Physiol 277: R532-R540, 1999.
19. Dampney RAL, Blessing WW, Tan E. Origin of tonic GABAergic inputs to vasopressor neurons in the subretrofacial nucleus of the rabbit. J Auton Nerv Syst 24: 227-239, 1988.
20. Dampney RAL, Horiuchi J, Tagawa T, Fontes MAP, Potts PD, Polson JW. Medullary and supramedullar mechanisms regulating sympathetic vasomotor tone. Acta Physiol Scand 177: 209-218, 2003.
21. Daubert DL, Chung MY, Brroks VL. Insulin resistance and impaired baroreflex gain during pregnancy. Am J Physiol Regul Integr Comp Physiol 292: R2188-R2195, 2007.
22. DeSwiet M. Hypertension in Pregnancy. New York: Elsevier Science, 1988.
23. Ferguson AV, Latchford KJ. Local circuitry regulates the excitability of rat neurohypophysial neurones. Exp Physiol 85: 153S-161, 2000.
24. Foley CM, Bruno SB, Kvochina L, Heesch CM. Alterations in baroreflex function by hindbrain microinjection of allopregnanolone in female rats (Abstract). FASEB J 19: A618, 2005.
25. Fontes MAP, Martins-Pinge MC, Naves V, Campagnole-Santos MJ, Lopes OU, Khosla MC, Santos RAS. Cardiovascular effects produced by microinjection of angiotensins and angiotensin antagonists into the ventrolateral medulla of freely moving rats. Brain Res 750: 305-310, 1997.
26. Frye CA, Bayon LE. Seizure activity is increased in endocrine states characterized by decline in endogenous levels of the neurosteroid 3α,5α-THP. Neuroendocrinology 68: 272-280, 1998.
27. Frye CA, Walf AA. Hippocampal 3α,5α-THP may alter depressive behavior of pregnant and lactating rats. Pharmacol Biochem Behav 78: 531-540, 2004.
28. Garland HO, Atherton JC, Baylis C, Morgan MRA, Milne CM. Hormone profiles for progesterone, oestradiol, prolactin, plasma renin activity, aldosterone and corticosterone during pregnancy and pseudopregnancy in two strains of rat: correlation with renal studies. J Endocrinol 113: 435-444, 1987.
29. Greenwood JP, Scott EM, Stoker JB, Walker JJ, Mary DASG. Sympathetic neural mechanisms in normal and hypertensive pregnancy in humans. Circulation 104: 2200-2204, 2001.
30. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 7: 335-346, 2006.
31. B independent sympathoinhibition from CVLM in rats. Brain Res 1125: 46-59, 2006.
32. Heesch CM, Laiprasert JD, Rogers RC, Ghosh S. Effects of 3α-hydroxy dihydroprogesterone (3α-OH-DHP) in the rostral ventrolateral medulla (RVLM) of female rats (Abstract). Soc Neurosci Abstr 23: 153, 1997.
33. Heesch CM, Rogers RC. Effects of pregnancy and progesterone metabolites on regulation of sympathetic outflow. Clin Exp Pharmacol Physiol 22: 136-142, 1995.
34. Hines T. Baroreceptor afferent discharge in the pregnant rat. Am J Physiol Regul Integr Comp Physiol 278: R1433-R1440, 2000.
35. Hines T, Mifflin SW. Gestational effects on volume-sensitive cardiopulmonary receptor reflexes in the rat. Am J Physiol Regul Integr Comp Physiol 268: R736-R743, 1995.
36. Hines T, Porter J. Role for central angiotensin II in control of blood pressure during pregnancy. Am J Physiol Regul Integr Comp Physiol 257: R1457-R1461, 1989.
37. 1) receptor in the rostral ventrolateral medulla in rats. J Appl Physiol 92: 2153-2161, 2002.
38. Ito S, Komatsu K, Tsukamoto K, Sved AF. Excitatory amino acids in the rostral ventrolateral medulla support blood pressure in spontaneously hypertensive rats. Hypertension 413-417, 2000.
39. Kaufman S, Deng Y. Renal response to atrial stretch during pregnancy in conscious rats. Am J Physiol Regul Integr Comp Physiol 265: R902-R906, 1993.
40. Kiely JM, Gordon FJ. Non-NMDA receptors in the rostral ventrolateral medulla mediate somatosympathetic pressor responses. J Auton Nerv Syst 43: 231-240, 1993.
41. Krieger EM. Neurogenic hypertension in the rat. Circ Res 15: 511-521, 1964.
42. Kvochina L, Heesch CM. Excitatory responses in rostral ventrolateral medulla (RVLM) of virgin and pregnant rats (abstract). FASEB J 16: A500, 2002.
43. Kvochina L, Heesch CM. Increased tonic inhibitory influences on rostral ventrolateral medulla in term pregnant compared with virgin rats (Abstract). FASEB Journal 17, A24. 2003.
44. Laiprasert JD, Hamlin R, Heesch CM. Afferent baroreceptor discharge in pregnant rats. Am J Physiol Heart Circ Physiol 281: H2456-H2462, 2001.
45. Laiprasert JD, Rogers RC, Heesch CM. Neurosteroid modulation of arterial baroreflex-sensitive neurons in rat rostral ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 274: R903-R911, 1998.
46. Latchford KJ, Ferguson AV. Angiotensin II activates a nitric-oxide-driven inhibitory feedback in the rat paraventricular nucleus. J Neurophysiol 89: 1238-1244, 2003.
47. Li DP, Chen SR, Pan HL. Angiotensin II stimulates spinally projecting paraventricular neurons through presynaptic disinhibition. J Neurosci 23: 5041-5049, 2003.
48. Lindheimer MD, Katz AI. Renal physiology and disease in pregnancy. In: The Kidney: Physiology and Pathophysiology, edited by Seldin DW and Giebisch G. New York: Raven, 1992, p. 3371-3432.
49. Lipski J, Kanjhan R, Kruszewska B, Rong W. Properties of presympathetic neurones in the rostral ventrolateral medulla in the rat: an intracellular study "in vivo." J Physiol 490: 729-744, 1996.
50. Lucini D, Strappazzon P, Vecchia LD, Maggioni C, Pagani M. Cardiac autonomic adjustments to normal human pregnancy: insight from spectral analysis of R-R interval and systolic arterial pressure variability. J Hypertens 17: 1899-1904, 1999.
51. Lumbers ER, Yu ZY. A method for determining baroreflex-mediated sympathetic and parasympathetic control of the heart in pregnant and non-pregnant sheep. J Physiol 515: 555-566, 1999.
52. Masilamani SME, Heesch CM. Effects of pregnancy and progesterone metabolites on baroreflex control of sympathetic outflow and heart rate in conscious rats. Am J Physiol Regul Integr Comp Physiol 272: R924-R934, 1997.
53. Mody I. Aspects of the homeostatic plasticity of GABAA receptormediated inhibition. J Physiol 562: 37-46, 2005.
54. Moreira TS, Sato MA, Takakura ACT, Menani JV, Colombari E. Role of pressor mechanisms from the NTS and CVLM in control of arterial pressure. Am J Physiol Regul Integr Comp Physiol 289: R1416-R1425, 2005.
55. O'Hagan KP, Casey SM. Arterial baroreflex during pregnancy and renal sympathetic nerve activity during parturition in rabbits. Am J Physiol Heart Circ Physiol 274: H1635-H1642, 1998.
56. 1 receptor block does not affect arterial baroreflex during pregnancy in rabbits. Am J Physiol Heart Circ Physiol 280: H1996-H2005, 2001.
57. Patel KP, Zhang PL. Role of renal nerves in renal responses to acute volume expansion during pregnancy in rats. Proc Soc Exp Biol Med 203: 1993.
58. Paxinos G, Watson C. The rat brain in stereotaxic coordinates (compact 3rd edition). New York: Academic 1997, p. 3.
59. Potas JR, Dampney RAL. Sympathoinhibitory pathway from caudal midline medulla to RVLM is independent of baroreceptor reflex pathway. Am J Physiol Regul Integr Comp Physiol 284: R1071-R1078, 2003.
60. Russell JA, Brunton PJ. Neuroactive steroids attenuate oxytocin stress responses in late pregnancy. Neuroscience 138: 879-889, 2006.
61. Schreihofer AM, Guyenet PG. The baroreflex and beyond: control of sympathetic vasomotor tone by GABAergic neurons in the ventrolateral medulla. Clin Exp Pharmacol Physiol 29: 514-521, 2002.
62. Schreihofer AM, Ito S, Sved AF. Brain stem control of arterial pressure in chronic arterial baroreceptor-denervated rats. Am J Physiol Regul Integr Comp Physiol 289: R1746-R1755, 2005.
63. Schreihofer AM, Sved AF. Use of sinoaortic denervation to study the role of baroreceptors in cardiovascular regulation. Am J Physiol Regul Integr Comp Physiol 266: R1705-R1710, 1994.
64. 1 receptors in the rostral ventrolateral medulla increases sympathetic activity under hypoxic conditions. Am J Physiol Regul Integr Comp Physiol 290: R733-R740, 2006.
65. Storey E, Kaufman S. Effect of pregnancy and 5α-pregnan- 3α-ol-20-one on atrial receptor afferent discharge in rats. Am J Physiol Regul Integr Comp Physiol 287: R1427-R1433, 2004.
66. Sun MK, Guyenet PG. GABA-mediated baroreceptor inhibition of reticulospinal neurons. Am J Physiol Regul Integr Comp Physiol 249: R672-R680, 1985.
67. Sved AF, Ito S, Madden CJ, Stocker SD, Yajima Y. Excitatory inputs to the RVLM in the context of the baroreceptor reflex. Ann NY Acad Sci 940: 247-258, 2002.
68. Sved AF, Ito S, Yajima Y. Role of excitatory amino acid inputs to the rostral ventrolateral medulla in cardiovascular regulation. Clin Exp Pharmacol Physiol 29: 503-506, 2002.
69. 1 receptors in the ventrolateral medulla. Braz J Med Biol Res 33: 643-652, 2000.
70. Wisloff U, Najjar SM, Oyvind E, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei KLSJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307: 418-420, 2005.
71. 1 receptor-like immunoreactivity in catecholaminergic neurons of the rat medulla oblongata. Neuroscience 81: 503-515, 1997.
72. Yang Z, Coote JH. Influence of the hypothalamic paraventricular nucleus on cardiovascular neurones in the rostral ventrolateral medulla of the rat. J Physiol 513: 521-530, 1998.