(Hypertension. 1995;25:1287-1293.)
© 1995 American Heart Association, Inc.
Articles |
Sympathectomy and Cardiovascular Spectral Components in Conscious Normotensive Rats
From Centro Fisiologia Clinica e Ipertensione, Ospedale Maggiore and CNR (A.D., C.F., A.R., G.M., A.U.F.), Milano; Cattedra di Fisiopatologia Applicata, Divisione di Cardioriabilitazione, Ospedale di Seregno, USSL 62 (A.U.F.); Cattedra di Medicina Interna, Ospedale S. Gerardo (G.M.), and Clinica Medica, Universitá di Milano (A.D., C.F., A.R., G.M., A.U.F.); and LaRC–Centro di Bioingegneria, Fondazione Don Gnocchi, Politecnico di Milano (P.C., M. Di R.) (Italy).
Correspondence to Prof Alberto Ferrari, Centro Fisiologia Clinica e Ipertensione, Ospedale Maggiore, Via F. Sforza, 35, 20122, Milano, Italy.
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Abstract |
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Abstract We examined the extent to which sympathetic influences are reflected by spectral powers of blood pressure and pulse interval in specific frequency bands in spontaneously behaving Wistar-Kyoto rats subjected to continuous intra-arterial blood pressure recording. The rats were pretreated with 6-hydroxydopamine (150 mg/kg twice in 1 week, n=19) to produce chemical sympathectomy or received vehicle (n=15). In the sympathectomized group, additional monitoring sessions were performed with rats under
-adrenergic receptor blockade with phenoxybenzamine
(n=8), ß-receptor blockade with propranolol (n=7), or
cholinergic receptor blockade with atropine (n=8). Blood pressure
signals were analyzed by a computer to calculate spectral powers (fast
Fourier transform) in the low-frequency (0.025 to 0.1 Hz),
mid-frequency (0.1 to 0.6 Hz), and high-frequency (0.8 to 3.0 Hz)
bands. In sympathectomized rats, low-frequency power of blood pressure
was 70% greater than in intact rats, whereas mid-frequency power was
60% smaller (P<.05 for both) and high-frequency power was
unchanged. High-frequency power of pulse interval was also unchanged in
sympathectomized rats, whereas low- and mid-frequency powers were
reduced by approximately 50% (P<.05). No further
alterations in spectral powers were observed by adding - or
ß-adrenergic blockade to sympathectomy, whereas adding
cholinergic blockade caused a striking reduction in all pulse interval
powers. Thus, mid-frequency blood pressure power depends on
sympathetic but also to a substantial extent on nonsympathetic
influences. Sympathetic influences do not contribute to low-frequency
blood pressure power, having instead a restraining effect. The
low- and mid-frequency pulse interval powers depend on both sympathetic
and vagal influences. Thus, no blood pressure or pulse interval power
in the mid- and low-frequency ranges can be regarded as a specific
marker of sympathetic activity.
Key Words: spectrum analysis • sympathetic nervous system • blood pressure • pulse interval • sympathectomy
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Introduction |
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Spectral analysis has shown in animals and humans that blood pressure and heart rate fluctuate over a wide range of frequencies. Most studies, however, have focused on discrete frequency bands, defined as high-frequency (HF), mid-frequency (MF), and low-frequency (LF), that have been thought to carry important information on cardiovascular control mechanisms.1 2 3 4 5 6 In particular, the LF and MF fluctuations have been deemed to reflect sympathetic influences because these fluctuations increase and decrease under conditions in which sympathetic cardiovascular drive rises and falls, respectively.6 7 8 9 However, the ability of LF and MF blood pressure and heart rate powers to represent precise markers of sympathetic cardiovascular influences is not consistent with several other observations. First, LF and MF heart rate powers were shown to depend also on vagal cardiac influences, and LF and MF blood pressure powers were not consistently attenuated or abolished by sympatholytic drugs.3 10 11 12 Second, in humans, MF heart rate power was not found to increase during a sympathoexcitatory maneuver such as mental arithmetic,13 and under resting conditions, a limited correlation was reported to exist between heart rate and blood pressure fluctuations in the LF and MF bands and directly recorded sympathetic nerve activity in both humans and rats.14 15 Finally, preliminary experiments performed in our laboratory in rats subjected to sympathectomy by 6-hydroxydopamine suggested that this intervention reduces but does not abolish the MF power of systolic blood pressure (SBP), the concomitant LF SBP power paradoxically being increased.16
These experiments, however, were difficult to interpret because
6-hydroxydopamine spares the adrenal medulla and may
not destroy all peripheral sympathetic nerves. In addition, data
analysis was limited to SBP. In the present study, we attempted
to overcome these limitations and thus provide conclusive evidence on
whether the use of MF and/or LF blood pressure powers as specific
indexes of sympathetic activity is justified. We pursued this by
performing spectral analysis of SBP and diastolic blood pressure
(DBP) in a large number of intact and sympathectomized rats; the latter
were examined before and after superimposition of - or
ß-adrenergic blockade to completely remove cardiovascular adrenergic
influences. A further goal of the study was to perform spectral
analysis of pulse interval in rats studied before and after
sympathectomy and additional cholinergic blockade and determine to what
degree the MF and LF heart rate powers are specific sympathetic markers
and whether vagal influences may also contribute.
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Methods |
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Thirty-four normotensive Wistar-Kyoto male rats (Charles River Calco) were housed in groups of two to four and received standard chow and water ad libitum. At the time of the study, rats were 10 to 12 weeks old. Intact rats weighed 218±9 g, and sympathectomized rats weighed 221±8 g (mean±SEM).
Chemical Sympathectomy
Destruction of efferent sympathetic nerve endings was
accomplished in 19 rats by administration of
6-hydroxydopamine (Sigma Chemical Co) injected twice at
150 mg/kg body wt over a period of 5 to 7 days.17 18 The
first dose was injected intraperitoneally, and the
second dose was injected intravenously after chronic instrumentation of
the rats (see below). Fifteen intact rats injected with vehicle alone
were used as controls. Before the blood pressure monitoring session
(see below) was started, the effectiveness of sympathectomy was tested
by comparing the pressor and tachycardic responses to tyramine (ie, a
drug that releases norepinephrine from sympathetic endings) at
150 µg/kg IV in treated versus untreated rats. The example of
Fig 1 and the average responses summarized in Table 1 indicate that 6-hydroxydopamine
administration produced a subtotal (85% to 90%) sympathectomy.
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Surgical Procedure
After anesthesia with ketamine HCl at 80 mg/kg IP, each rat was
instrumented with polyethylene catheters inserted into a femoral artery
and femoral vein. The catheters were tunneled subcutaneously and
exteriorized at the interscapular region, their patency being
maintained by periodic flushing with minute amounts of heparinized
saline solution. After instrumentation, rats were individually housed
in a wide cage for 24 hours to allow them to recover from surgery and
become acclimated to the environment.
Experimental Protocol
In both sympathectomized and control rats, the arterial
catheter was connected to a P23Dc pressure transducer (Gould-Statham);
this catheter-transducer system had a flat frequency response up to 30
Hz. This avoided distortions of the harmonic components of the pressure
wave smaller than 6; ie, it allowed accurate recordings of components
accounting for virtually all signal variance. The blood pressure signal
was displayed on a chart recorder (7D polygraph, Grass Instrument Co),
and heart rate was also displayed by tachographic beat-to-beat
conversion of the pulsatile arterial blood pressure signal. Initially,
tyramine was injected via the venous catheter (see above). The rat was
then allowed to recover from the effects of tyramine for no less than
30 minutes. Finally, arterial blood pressure was monitored for 90
minutes, the signal being stored on a high-fidelity FM magnetic tape
recorder (Racal Store 4), while the rats could freely move, explore,
eat, and sleep within their cages. During the recording period,
acoustic disturbances were avoided, and the cage was kept at constant
temperature and moderate degree of illumination. The rats were kept
under constant visual surveillance; no appreciable behavioral
differences were perceived in the rat groups subjected to the various
interventions. In 8 sympathectomized rats, an additional 90-minute
recording period was carried out after administration of
phenoxybenzamine at 1 mg/kg. This was done to remove possible
influences on -adrenergic receptors exerted by (1) residual
norepinephrine release from the sympathetic endings that may not have
been destroyed by 6-hydroxydopamine and (2)
catecholamines released by the adrenal medulla, which is spared by this
model of sympathectomy.19 Similarly, since residual
catecholamine release may also affect variability by stimulating
vascular and cardiac ß-adrenoceptors, 7 sympathectomized rats were
subjected to a further 90-minute blood pressure recording after
administration of 1 mg/kg propranolol. Finally, in 8
sympathectomized rats, an additional 90-minute recording period was
carried out after 0.8 mg/kg IV atropine. This was done to establish the
contribution of vagal modulation of the cardiovascular system to pulse
interval and blood pressure powers after sympathectomy. Four of the
sympathectomized rats were used for two drug interventions, the
atropine session being carried out immediately after baseline recording
and the phenoxybenzamine session being carried out 24 hours later.
The effectiveness of -adrenergic blockade was tested by the
disappearance of the pressor effect of phenylephrine: at 2
µg/kg IV, this drug induced an increase in mean arterial pressure
always greater than 20 mm Hg before and never greater than 2 mm Hg
after phenoxybenzamine. The effectiveness of ß-adrenergic blockade
was tested by the disappearance of the tachycardic effect of
isoproterenol: at 4 µg/kg IV, the drug induced an increase of heart
rate always greater than 40 beats per minute before and never greater
than 5 beats per minute after propranolol. The cholinergic
blockade was regarded as effective if the reflex bradycardic response
to a phenylephrine-induced (2 µg/kg IV bolus)
increase in blood pressure was reduced by at least 90%.
The experimental procedures were performed in accordance with Italian government directions concerning the protection of animals used for scientific purposes.
Data Analysis
A detailed description of the spectral analysis
technique we used has been reported elsewhere.20 In brief,
the 90-minute tape-recorded arterial pressure signal was fed into a
computer (Olivetti XP5), sampled at 250 Hz, digitized at 12 bits, and
edited for artifacts as well as for nonstationarities caused by the
occurrence of arrhythmias. Systolic and diastolic values were
identified for each cardiac cycle and computed on a beat-to-beat basis;
pulse interval was computed by measuring the interval between two
consecutive systolic peaks. To improve the time resolution of the pulse
interval estimate, the systolic portion of each sampled pulse wave was
interpolated by a parabolic curve, the apex of which was taken as the
true time of occurrence of the systolic peak. We have previously shown
that in normotensive and hypertensive humans under concomitant 24-hour
blood pressure and electrocardiographic recordings, the use of pulse
interval (the time interval between two consecutive systolic peaks) and
of RR interval (electrocardiographic) provided similar spectral
powers.6 Pulse interval and corresponding RR interval were
similar also in our conscious rats. This is exemplified in Fig 2, which shows a 30-minute recording of heart interval
by the two methods. The average heart interval values of the 30-minute
period were both 167.3 milliseconds when estimated by pulse interval
and RR interval, the corresponding standard deviations being 4.45 and
4.36 milliseconds, respectively. The absolute difference (regardless of
the sign) was 0.92 millisecond.
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For each 90-minute recording period, average SBP, DBP, and pulse interval along with the respective variances were computed. In addition, each SBP, DBP, and pulse interval beat-to-beat series was divided into consecutive 100-second periods, and for each of the three variables, the spectra were calculated by the fast Fourier transform technique. This approach provided spectra including the power related to both rhythmic and nonrhythmic variations in line with what is usually done in spectral studies on rats.3 8 10 11 12 Since SBP, DBP, and pulse interval are defined on a beat-to-beat basis, they were irregularly sampled in time (because of the variability in heart rate) but regularly spaced as a function of the beat number. Thus, the obtained spectra, which should be estimated from evenly sampled data, had frequencies expressed as cycles per beat. To transform the results into hertz (cycles per second), the original frequencies were divided by the average pulse interval computed over the respective 100-second period. This approach could be used without risk of distortion in the spectra, instead of procedures based on the interpolation and resampling of the data, because the pulse interval variations in a single period were largely lower than the average pulse interval value.21 From each spectrum thus obtained, power spectral densities were integrated in the HF band (3.0 to 0.8 Hz), MF band (0.6 to 0.1 Hz), and LF band (0.1 to 0.025 Hz) based on (1) preferential clustering of power in these frequency regions, in agreement with observations made in earlier spectral studies in rats,3 8 10 11 12 22 and (2) correspondence of these bands to the HF, MF, and LF bands identified within a lower frequency range (between 1 and 0.07 Hz) in spectral studies on humans and large laboratory animals.8
Individual data were averaged separately for intact and
sympathectomized rats. Statistical comparisons of the differences
between the two groups were performed by the t test for
unpaired observations. The t test for paired observations
was used to statistically evaluate the effects of -adrenergic
blockade and cholinergic blockade. The level of statistical
significance was set at a value of P<.05.
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Results |
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Sympathectomy and Spectral Powers
Table 2 shows that sympathectomized rats had lower SBP and DBP than control rats, whereas pulse interval was not significantly different in the two groups. SBP and DBP variances were significantly larger in sympathectomized rats, whereas pulse interval variance was not different in sympathectomized and control rats.
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Fig 3 shows a typical spectral profile of SBP in one control and one sympathectomized rat, with the average spectral data reported in Fig 4. For both SBP and DBP, the power of the HF band was similar in control and sympathectomized rats. In sympathectomized rats, however, the MF power for both SBP and DBP was significantly lower than in control rats, and the LF power was significantly higher. The decrease in the MF power and the increase in the LF power displayed by the sympathectomized rats amounted to approximately -60% and +70%, respectively.
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The HF power of pulse interval was similar in control and sympathectomized rats, and the MF and LF powers were significantly lower in the latter compared with the former group.
-Adrenergic Receptor Blockade and Spectral Powers
In sympathectomized rats, additional -adrenergic blockade was
accompanied by no significant change in SBP and DBP and by a slight but
significant reduction in pulse interval (Table 3). On
the other hand, the variance of all three variables was unchanged. This
was the case also for the LF, MF, and HF powers, which for SBP, DBP,
and pulse interval were not significantly different before and after
-adrenergic blockade (Fig 5).
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ß-Adrenergic Receptor Blockade and Spectral Powers
In sympathectomized rats, additional ß-adrenergic blockade was
accompanied by a slight but significant increase in SBP and by the
expected increase in pulse interval (Table 3). On the other hand, the
variance of all three variables was unchanged. This was the case also
for LF, MF, and HF powers of SBP and DBP, which were not significantly
different before and after ß-adrenergic blockade. LF and MF powers of
pulse interval showed a trend toward a further reduction after
propranolol although the difference was not statistically
significant in either case with the prepropranolol data
(Fig 6).
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Cholinergic Receptor Blockade and Spectral Powers
In sympathectomized rats, additional cholinergic blockade
was accompanied by no significant changes in SBP and DBP and by the
expected reduction in pulse interval (Table 3). Both SBP and DBP
variances were increased, whereas pulse interval variance was
strikingly reduced. SBP and DBP powers were unaffected in the HF and MF
bands, and they were significantly increased in the LF band; pulse
interval power was drastically reduced in all three frequency bands
(Fig 7).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Our study shows that in spontaneously behaving unanesthetized Wistar-Kyoto rats, sympathectomy by 6-hydroxydopamine is associated with an increase in LF and a decrease in MF powers of SBP and DBP. Both the increased LF and decreased MF blood pressure powers were unaffected by additional
- or ß-adrenergic blockade, ie, by
removal of possible residual vascular adrenergic influences. It can
thus be concluded that the LF blood pressure power is not produced by
sympathetic influences, which instead exert a net counteracting effect
on its amplitude. In contrast, the MF blood pressure power does depend
on sympathetic mechanisms, as suggested by previous
studies.11 22 It should be emphasized, however, that about
a third of the MF blood pressure power survived sympathectomy without
or with additional - or ß-adrenergic blockade, which means that a
substantial proportion of this power is generated by nonsympathetic
factors. Thus in spontaneously behaving rats, the specificity of MF
blood pressure power as a marker of sympathetic activity is
limited.
Another new finding of our study is that sympathectomy caused a marked
reduction in the MF but also in the LF powers of pulse interval. Thus,
sympathetic influences are more extensively involved in the production
of heart rate powers than they are in the production of blood pressure
powers. Also for heart rate, however, the specificity of these powers
as sympathetic markers is limited because a noticeable proportion of
the LF (50%) and MF (30%) powers seen in control rats was still
present in sympathectomized rats. Our study did not allow us to
establish the extent to which the observed sympathetic influences on
spectral powers originate from central neural rather than from
baroreflex mechanisms. However, the spectral effects of sympathectomy
seen in the present study were similar to those caused by
sinoaortic denervation in a previous study on conscious
cats,23 suggesting that reflex influences may be
significantly involved. We also have no information on the nature of
the nonsympathetic influences accounting for the residual MF and
enhanced LF blood pressure powers seen after sympathectomy and - or
ß-adrenergic blockade. It is clear from our atropine data, however,
that these influences are not parasympathetic. We can speculate that
fluctuations in (1) circulating vasoactive substances such as
angiotensin II or vasopressin, (2) receptor responsiveness, and/or (3)
myogenic activity in the vessel wall cause changes in systemic vascular
resistance and blood pressure within the MF and LF bands; indeed,
several previous studies have implicated the renin-angiotensin system
in the genesis of LF blood pressure
fluctuations.3 5 12 24
Several other aspects of our study deserve to be discussed. First, one can speculate that part of the increase in LF power and the reduction in MF blood pressure power produced by sympathectomy were related to each other, ie, that this pattern reflected a redistribution of power from the MF to lower-frequency regions and thus an entraining effect of sympathetic influences toward the MF band. This entraining effect may not be limited to the LF and MF powers but may extend over a lower frequency range. Namely, sympathectomy may enhance spectral powers to a progressively greater extent at frequencies progressively lower than LF, sympathetic influences thereby reducing the degree to which blood pressure power normally increases as frequency diminishes (the so-called 1/f slope).25 Second, the unchanged HF power and reduced LF and MF powers of pulse interval seen after sympathectomy were markedly blunted by additional cholinergic blockade by atropine, in line with previous reports that the spectral expression of vagal cardiac control extends well below the HF range.3 4 22 It is thus clear that pulse interval fluctuations in the MF and LF regions of the spectrum are generated by concurrent vagal and sympathetic influences and that none of these fluctuations represent specific sympathetic or vagal markers.
The third and final point concerns the methodology of power spectral analysis, ie, the fact that cardiovascular spectral data are often analyzed and presented as HF and LF bands only, the LF band including the MF range as well. However, previous data in dogs, cats, and rats indicate that interfering with autonomic cardiovascular influences may affect LF and MF blood pressure powers in a quantitatively and qualitatively different fashion.3 10 11 22 23 This is fully confirmed in the present study in which LF and MF blood pressure powers were affected in an opposite direction by chemical sympathectomy. Thus, lumping MF and LF blood pressure powers together may conceal information on their determinants that can instead be obtained by analyzing each of the two frequency components separately.
In conclusion, our study provides evidence that in rats MF blood pressure power originates from sympathetic but to a sizable extent also from nonautonomic influences. Therefore, its specificity as a sympathetic marker is limited. In contrast, LF blood pressure power is not produced by sympathetic influences, which are likely to oppose LF blood pressure oscillations. Both MF and LF powers of pulse interval are markers of cardiac sympathetic control, but their specificity is also limited because of concurrent vagal influences impinging on the same frequency range.
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Footnotes |
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Revision accepted January 30, 1995.
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References |
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1. Sayers B McA. Analysis of heart rate variability. Ergonomics. 1973;16:17-32. [Medline] [Order article via Infotrieve]
2. Kitney RI, Rompelman O. In: The Study of Heart Rate Variability. Oxford, UK: Claredon; 1980:59-107.
3.
Akselrod S, Gordon D, Ubel FA, Shannon DC, Barger AC,
Cohen RJ. Power spectrum analysis of heart rate fluctuation:
a quantitative probe of beat to beat cardiovascular control.
Science. 1981;213:220-223.
4.
Pomeranz B, Macaulay RJB, Candill MA, Kutz I, Adam D,
Gordon D, Kilborn KM, Barger AC, Shannon DC, Cohen RJ, Benson H.
Assessment of autonomic function in humans by heart rate
spectral analysis. Am J Physiol. 1985;248:H151-H153.
5. Koepchen HP. History of studies and concepts of blood pressure waves. In: Miyakawa K, Koepchen HP, Polosa C, eds. Mechanisms of Blood Pressure Waves. Tokyo, Japan: Japan Sci Soc Press; Berlin, Germany: Springer Verlag; 1984:3-23.
6.
Parati G, Castiglioni P, Di Rienzo M, Omboni S,
Pedotti A, Mancia G. Sequential spectral analysis of 24-hour
blood pressure and pulse interval in humans.
Hypertension. 1990;16:414-421.
7.
Pagani M, Lombardi F, Guzzetti S, Rimoldi O,
Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell'Orto S, Piccaluga
E, Turiel M, Baselli G, Cerutti S, Malliani A. Power spectral
analysis of heart rate and arterial pressure variabilities as a
marker of sympatho-vagal interaction in man and conscious dog.
Circ Res. 1986;59:178-193.
8.
Akselrod S, Eliash S, Oz O, Cohen S.
Hemodynamic regulation in SHR: investigation by spectral
analysis. Am J Physiol. 1987;253:H176-H183.
9.
Malliani A, Pagani M, Lombardi F, Cerutti S.
Cardiovascular neural regulation explored in the frequency
domain. Circulation. 1991;84:482-492.
10.
Akselrod S, Gordon D, Madwed JB, Snidam NC, Shannon DC,
Cohen RJ. Hemodynamic regulation: investigation by spectral
analysis. Am J Physiol. 1985;249:H867-H875.
11.
Cerutti C, Gustin MP, Paultre CZ, Lo M, Julien C,
Vincent M, Sassard J. Autonomic nervous system and
cardiovascular variability in rats: a spectral analysis
approach. Am J Physiol. 1991;261:H1292-H1299.
12. Eliash S, Oz O, Cohen S, Akselrod S. The role of the renin-angiotensin and alpha control in the regulation of blood pressure in a normotensive versus in a hypertensive system. Proc Computers in Cardiology, Chicago, 1990. Los Alamitos, Calif: IEEE Comput Society Press. 1991:155-158.
13. Langewitz W, Ruddel H. Spectral analysis of heart rate variability under mental stress. J Hypertens. 1989;7:S32-S33.
14.
Saul JP, Rea RF, Eckberg DL, Berger RD, Cohen RJ.
Heart rate and muscle sympathetic nerve variability during
reflex changes of autonomic activity. Am J Physiol. 1990;258:H713-H721.
15.
Persson PB, Stauss H, Chung O, Wittmann U, Unger T.
Spectrum analysis of sympathetic nerve activity and blood
pressure in conscious rats. Am J Physiol. 1992;263:H1348-H1355.
16. Daffonchio A, Franzelli C, Di Rienzo M, Castiglioni P, Ramirez AJ, Parati G, Mancia G, Ferrari AU. Effect of sympathectomy on blood pressure variability in conscious rat. J Hypertens. 1991;9(suppl 6):S70-S71.
17. Provoost AP. Sympathectomy and the development of hypertension in rats. In: De Jøng W, ed. Handbook of Hypertension, Volume 4: Experimental and Genetic Models of Hypertension. Amsterdam, Netherlands: Elsevier Science Publishers; 1984:495-517.
18.
Ferrari AU, Daffonchio A, Franzelli C, Mancia G.
Potentiation of the baroreceptor–heart rate reflex by
sympathectomy in conscious rats.
Hypertension. 1991;18:230-235.
19.
Kostrezewa RM, Jacobowitz DM. Pharmacological
actions of 6-hydroxydopamine. Pharmacol
Rev. 1974;26:199-275.
20. Di Rienzo M, Castiglioni P, Mancia G, Parati G, Pedotti A. 24-Hour sequential spectral analysis of arterial blood pressure and pulse interval in free-moving subjects. IEEE Trans Biomed Eng. 1989;36:1066-1075. [Medline] [Order article via Infotrieve]
21. Rompelman O, Coenen AJRM, Kitney RI. Measurement of heart rate variability, part 1: comparative study of heart rate variability analysis methods. Med Biol Eng Comput. 1977;15:233-239. [Medline] [Order article via Infotrieve]
22. Japundzic N, Grichois ML, Zitoun P, Laude D, Elghozi JL. Spectral analysis of blood pressure and heart rate in conscious rat: effects of autonomic blockers. J Auton Nerv Syst. 1990;30:91-100. [Medline] [Order article via Infotrieve]
23.
Di Rienzo M, Parati G, Castiglioni P, Omboni S, Ferrari
AU, Ramirez AJ, Pedotti A, Mancia G. Role of sinoaortic
afferents in modulating BP and pulse-interval spectral characteristics
in unanesthetized cats. Am J Physiol. 1991;261:H1811-H1818.
24. Akselrod S, Oz O, Eliash S. Neural and humoral factors in regulation of blood pressure in the investigation of essential hypertension. In: Di Rienzo M, Mancia G, Parati G, Pedotti A, Zanchetti A, eds. Blood Pressure and Heart Rate Variability. Amsterdam, Netherlands: IOS Press; 1993:192-206.
25.
Marsh DJ, Osborn JL, Cowley AW. 1/f fluctuations
in arterial pressure and regulation of renal blood flow in
dogs. Am J Physiol. 1990;258:F1394-F1400.
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