Autonomic mechanisms underpinning the stress response in borderline hypertensive rats

This study investigates blood pressure (BP) and heart rate (HR) short‐term variability and spontaneous baroreflex functioning in adult borderline hypertensive rats and normotensive control animals kept on normal‐salt diet. Arterial pulse pressure was recorded by radio telemetry. Systolic BP, diastolic BP and HR variabilities and baroreflex were assessed by spectral analysis and the sequence method, respectively. In all experimental conditions (baseline and stress), borderline hypertensive rats exhibited higher BP, increased baroreflex sensitivity and resetting, relative to control animals. Acute shaker stress (single exposure to 200 cycles min‐1 shaking platform) increased BP in both strains, while chronic shaker stress (3‐day exposure to shaking platform) increased systolic BP in borderline hypertensive rats alone. Low‐ and high‐frequency HR variability increased only in control animals in response to acute and chronic shaker (single exposure to restrainer) stress. Acute restraint stress increased BP, HR, low‐ and high‐frequency variability of BP and HR in both strains to a greater extent than acute shaker stress. Only normotensive rats exhibited a reduced ratio of low‐ to high‐frequency HR variability, pointing to domination of vagal cardiac control. In borderline hypertensive rats, but not in control animals, chronic restraint stress (9‐day exposure to restrainer) increased low‐ and high‐frequency BP and HR variability and their ratio, indicating a shift towards sympathetic cardiovascular control. It is concluded that maintenance of BP in borderline hypertensive rats in basal conditions and during stress is associated with enhanced baroreflex sensitivity and resetting. Imbalance in sympathovagal control was evident only during exposure of borderline hypertensive rats to stressors.

[1]  G. Dibona,et al.  Central alpha 2-adrenoceptor responsiveness in borderline hypertensive rats. , 1991, Journal of hypertension.

[2]  E. J. Green,et al.  Modulation of the baroreceptor reflex by stimulation of the hypothalamic defense and vigilance areas , 1996, Physiology & Behavior.

[3]  P. Grossman,et al.  Noninvasive assessment of baroreflex control in borderline hypertension. Comparison with the phenylephrine method. , 1996, Hypertension.

[4]  C. Julien,et al.  Sympathetic modulation of blood pressure variability , 2001, Journal of hypertension.

[5]  R. F. Kirby,et al.  Cardiovascular and sympathetic nervous system responses to an acute stressor in borderline hypertensive rats (BHR) , 1989, Physiology & Behavior.

[6]  Hélène Pierre,et al.  EVAluation of the prognostic value of BARoreflex sensitivity in hypertensive patients: the EVABAR study , 2008, Journal of hypertension.

[7]  A. Takeshita,et al.  Reduced baroreceptor sensitivity in borderline hypertension. , 1975, Circulation.

[8]  C. Julien Mental stress, hypertension and the baroreflex: what's new? , 2009, Journal of hypertension.

[9]  D W Slaaf,et al.  Hemodynamic basis of oscillations in systemic arterial pressure in conscious rats. , 1995, The American journal of physiology.

[10]  D. Paterson,et al.  Should we still use nitrovasodilators to test baroreflex sensitivity? , 2000, Journal of hypertension.

[11]  J. Elghozi,et al.  Differential Effects of Enalapril and Hydralazine on Short‐Term Variability of Blood Pressure and Heart Rate in Rats , 1992, Journal of cardiovascular pharmacology.

[12]  B. Janssen,et al.  Validation of a continuous baroreceptor reflex sensitivity index calculated from spontaneous fluctuations of blood pressure and pulse interval in rats , 1997, Journal of hypertension.

[13]  J. Lawler,et al.  Sympathetic control of BP and BP variability in borderline hypertensive rats on high- vs. low-salt diet. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[14]  N. Japundzic-Zigon Physiological mechanisms in regulation of blood pressure fast frequency variations. , 1998, Clinical and experimental hypertension.

[15]  Krzysztof Narkiewicz,et al.  Impaired baroreflex sensitivity as a potential marker of cardiovascular risk in hypertension. , 2008, Journal of hypertension.

[16]  T. Saito Hemodynamics and the baroreflex function in borderline hypertension. , 1983, Japanese circulation journal.

[17]  G. Parati,et al.  The role of blood pressure variability in end-organ damage , 2003, Journal of hypertension. Supplement : official journal of the International Society of Hypertension.

[18]  K. Okamoto,et al.  Modified characteristics of the aortic baroreceptor activities in the spontaneously hypertensive rat. , 1970, Japanese circulation journal.

[19]  A. Hoque,et al.  Vascular and hemodynamic effects of behavioral stress in borderline hypertensive and Wistar-Kyoto rats. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[20]  R. Cohen,et al.  Hemodynamic regulation: investigation by spectral analysis. , 1985, The American journal of physiology.

[21]  V. Lemaire,et al.  Telemetered recording of blood pressure and heart rate in different strains of rats during chronic social stress , 1995, Physiology & Behavior.

[22]  B. Sanders,et al.  Vascular responsiveness in the unstressed borderline hypertensive rat. , 1994, Clinical and experimental hypertension.

[23]  W. Paré Stress ulcer susceptibility and depression in Wistar Kyoto (WKY) rats , 1989, Physiology & Behavior.

[24]  A. D. Giulumian,et al.  Effect of behavioral stress on coronary artery relaxation altered with aging in BHR. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[25]  Tatjana Loncar-Turukalo,et al.  Temporal analysis of the spontaneous baroreceptor reflex during mild emotional stress in the rat , 2010, Stress.

[26]  J. Herbert,et al.  Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: Correlations with cardiovascular, hypothermic and endocrine responses , 1995, Neuroscience.

[27]  G. Drolet,et al.  Chronic stress induces sensitization in sympathoadrenal responses to stress in borderline hypertensive rats. , 1997, The American journal of physiology.

[28]  D. Morilak,et al.  Effects of acute restraint stress on tyrosine hydroxylase mRNA expression in locus coeruleus of Wistar and Wistar-Kyoto rats. , 2000, Brain research. Molecular brain research.

[29]  J. Deuchars,et al.  Adenoviral vector demonstrates that angiotensin II‐induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii of the rat , 2001, The Journal of physiology.

[30]  S. McDougall,et al.  Restraint stress : differential cardiovascular responses in Wistar-Kyoto and spontaneously hypertensive rats. , 2000, Hypertension.

[31]  K. Okamoto,et al.  Development of a strain of spontaneously hypertensive rats. , 1963, Japanese circulation journal.

[32]  J. Lawler,et al.  Cardiovascular and renal responses to stress in borderline hypertensive rat. , 1988, The American journal of physiology.

[33]  I. Bernátová,et al.  Effect of chronic social stress on nitric oxide synthesis and vascular function in rats with family history of hypertension. , 2006, Life sciences.

[34]  Giuseppe Mancia,et al.  Reappraisal of European guidelines on hypertension management: a European Society of Hypertension Task Force document , 2009, Blood pressure.

[35]  C Cerutti,et al.  Baroreflex modulation of blood pressure and heart rate variabilities in rats: assessment by spectral analysis. , 1994, The American journal of physiology.

[36]  G. Dibona,et al.  Role of Anteroventral Third Ventricle and Vasopressin in Renal Response to Stress in Borderline Hypertensive Rats , 1991, Hypertension.

[37]  D. Laude,et al.  Blood pressure variability in established L-NAME hypertension in rats. , 1999, Journal of hypertension.

[38]  J. Lawler,et al.  The borderline hypertensive rat (BHR) as a model for environmentally-induced hypertension: A review and update , 1992, Neuroscience & Biobehavioral Reviews.

[39]  P. Schmid,et al.  Pressor response to vasopressin and impaired baroreflex function in DOC-salt hypertension. , 1982, The American journal of physiology.

[40]  J. Juchmes,et al.  The arterial baroreflex and the cardiopulmonary reflex in borderline hypertension. , 1983, European Heart Journal.

[41]  David Murphy,et al.  The role of central vasopressin receptors in the modulation of autonomic cardiovascular controls: a spectral analysis study. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[42]  T. Saruta,et al.  Comparison of early and late start of antihypertensive agents and baroreceptor reflexes. , 1996, Hypertension.

[43]  N. Japundzic-Zigon,et al.  EFFECTS OF NONPEPTIDE V1a AND V2 ANTAGONISTS ON BLOOD PRESSURE FAST OSCILLATIONS IN CONSCIOUS RATS , 2001, Clinical and experimental hypertension.

[44]  G. Dibona,et al.  Renal manifestations of NaCl sensitivity in borderline hypertensive rats. , 1991, Hypertension.

[45]  C. Barrès,et al.  Blood pressure and baroreflex sensitivity in conscious hypertensive rats of Lyon strain. , 1986, The American journal of physiology.

[46]  M. Ruzicka,et al.  Cardiovascular effects of social stress in borderline hypertensive rats , 1994, Journal of hypertension.

[47]  D. Laude,et al.  Spectral analysis of blood pressure and heart rate in conscious rats: effects of autonomic blockers. , 1990, Journal of the autonomic nervous system.

[48]  A Pedotti,et al.  Evaluation of baroreceptor reflex by blood pressure monitoring in unanesthetized cats. , 1988, The American journal of physiology.

[49]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

[50]  D. McCarron,et al.  Cardiovascular response to stress: baroreflex resetting and hemodynamics. , 1997, The American journal of physiology.

[51]  Tatjana Loncar-Turukalo,et al.  Temporal Sequence Parameters in Isodistributional Surrogate Data: Model and Exact Expressions , 2011, IEEE Transactions on Biomedical Engineering.

[52]  G. Parati,et al.  Spectral analysis of blood pressure and heart rate variability in evaluating cardiovascular regulation. A critical appraisal. , 1995, Hypertension.

[53]  Daniel J Brotman,et al.  The cardiovascular toll of stress , 2007, The Lancet.

[54]  R. Hughson,et al.  Spontaneous cardiac baroreflex in humans. Comparison with drug-induced responses. , 1995, Hypertension.

[55]  J. Lawler,et al.  Baroreflex function in chronically stressed borderline hypertensive rats , 1991, Physiology & Behavior.

[56]  J. Elghozi,et al.  Contribution of the renin-angiotensin and kallikrein-kinin systems to short-term variability of blood pressure in two-kidney, one-clip hypertensive rats. , 1996, European journal of pharmacology.

[57]  J. H. Green,et al.  Baroceptor Function in Chronic Renal Hypertension , 1956, Circulation research.