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(Hypertension. 1995;26:1111-1116.)
© 1995 American Heart Association, Inc.

Articles

Changes of Renal Sympathetic Activity in Acute and Chronic Conscious Sinoaortic Denervated Rats

Maria Claudia Irigoyen; Edson Dias Moreira; Fumio Ida; Mara Pires; Idágene Aparecida Cestari; Eduardo Moacyr Krieger

From the Laboratory of Cardiovascular Physiology, Department of Physiology, Biosciences Institute, University of Rio Grande do Sul (M.C.I.) and the Hypertension Unit (E.D.M., F.I., M.P., E.M.K.) and Bioengineering Division (I.A.C.), Heart Institute, School of Medicine, University of São Paulo, Brazil.

Correspondence to Eduardo M. Krieger, MD, PhD, Hypertension Unit, Heart Institute, Faculty of Medicine, University of São Paulo, Brazil, Av Dr Enéas de Carvalho Aguiar 44, São Paulo, SP 05403 000, Brazil.

	Abstract

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Abstract The arterial pressure level attained in sinoaortic denervated rats depends on the net effect of eliminating excitatory and inhibitory influences (chemoreceptor and baroreceptor elimination, respectively). After sinoaortic denervation is completed, the hypertension usually observed within the first few days is followed by normotension at the chronic stages. In this work renal sympathetic nerve activity was measured in conscious, unrestrained rats 6 hours (acute) and 20 days (chronic) after sinoaortic denervation. Increased arterial pressure (154±10 versus 114±3 mm Hg in controls) and renal sympathetic nerve activity (32±5 versus 13±2 bars per cycle in controls) with no changes in heart rate (404±17 vs 380±26 beats per minute) were observed in rats with acute sinoaortic denervation. In rats with chronic sinoaortic denervation, arterial pressure (119±8 mm Hg) and renal sympathetic nerve activity (13±6 bars per cycle) returned to control levels. Bradycardiac and tachycardiac responses to changes in blood pressure were reduced to 88% and 89%, respectively, in rats with acute sinoaortic denervation and 76% and 74%, respectively, in rats with chronic sinoaortic denervation. The reflex control of renal sympathetic nerve activity after acute and chronic sinoaortic denervation showed an impairment of sympathoinhibition (0.13±0.02 and 0.25±0.1 bars per cycle, respectively, versus 0.9±0.17 bars per cycle in controls). Sympathoexcitatory responses also were impaired in rats with acute and chronic sinoaortic denervation (0.08±0.03 and 0.37±0.1 bars per cycle, respectively, compared with 0.98±0.2 bars per cycle in controls). The variability of mean arterial pressure expressed by standard deviation was higher in rats with acute and chronic sinoaortic denervation (13±2 and 15±2 mm Hg, respectively) than in controls (6±3 mm Hg). The variability coefficient of renal sympathetic nerve activity was lower 6 hours (0.22±0.07) but normal 20 days after sinoaortic denervation (0.88±0.24 versus 0.77±0.06 in controls). We conclude that (1) acute sinoaortic denervation increases arterial pressure and renal sympathetic nerve activity and reduces renal sympathetic variability, (2) blood pressure and renal sympathetic activity return to normal levels in rats after chronic sinoaortic denervation, and (3) increased variability and impairment of the baroreflexes persisted in the chronic phase of sinoaortic denervation.

Key Words: sympathetic nervous system • blood pressure • baroreflex

	Introduction

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The arterial baroreceptor reflex system is one of the most powerful and rapidly acting mechanisms for controlling AP. However, SAD produces variable changes in the AP level of conscious, undisturbed animals^{1 2 3 4 5 6} but a persistent and marked increase in the variability of AP. Factors that possibly account for the disparity in these results include the techniques used for AP measurement, which cause different degrees of excitement; the extent of the denervation; the time after baroreceptor deafferentation; the duration of the AP recording; and, finally, the effects of behaviors that act either to increase or decrease AP in SAD animals.⁷ Sympathetic hyperactivity has been implicated as the major determinant of increased AP after SAD. Catecholamine measurements, acute and chronic sympathetic blockade, and localized lesioning of the central nervous system have been used to indirectly estimate increased peripheral neurogenic tone.^{7 8 9} Moreover, hemodynamic evaluation of SAD rats indicates that increased peripheral resistance is responsible for hypertension 1 and 6 hours after denervation.¹⁰ Indeed, preliminary data from our laboratory showed increased RSNA in unanesthetized rats subjected to acute deafferentation of baroreceptors.¹¹ However, we have no systematic information on the temporal changes in peripheral sympathetic activity after SAD, even considering that in the chronic phase quiet and undisturbed SAD rats show only slight hypertension or none.⁷ Therefore, the present investigation was undertaken to study the acute (at 6 hours) and chronic (after 20 days) effects of SAD on AP, HR, and baroreflex control of HR and RSNA in conscious, unrestrained rats.

	Methods

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Male Wistar rats weighing 250 to 300 g were used. The rats were housed individually with ad libitum access to food and water. The experimental groups consisted of normal rats (n=6), SADa rats (measured 6 hours after SAD, n=6) and SADc rats (measured 20 days after SAD, n=6). All rats were maintained on a 12-hour light/dark cycle. AP and RSNA were recorded simultaneously in healthy rats 6 hours and 20 days after denervation.

SAD
SAD was performed as described previously by our laboratory.⁴ Briefly, under ether anesthesia a 3-cm midline incision was made, and sternocleidomastoid muscles were reflected laterally, exposing the neurovascular sheath. The common carotid arteries and the vagal trunk were isolated, and the aortic depressor fibers either traveling with the sympathetic nerve or as an isolated aortic nerve were cut. The communicating branch of the aortic fibers was also resected. The third contingent of aortic baroreceptor fibers traveling with the inferior laryngeal nerve was interrupted by resection of the superior laryngeal nerve after the carotid bifurcation was exposed extensively for carotid stripping. To complete SAD, the sinus nerve as well as all carotid branches and the carotid body were resected.

Instrumentation
Arterial and venous cannulas were implanted in normal control rats and SADa and SADc rats 1 day before cardiovascular and nerve monitoring, and all animals were treated with a single injection of penicillin G benzatine (benzethacil 60 000 U). While the rat was under ether anesthesia, polyethylene-tipped Tygon cannulas filled with heparin in normal saline were inserted into the abdominal aorta and inferior vena cava through the left femoral artery and vein, respectively. The free ends of the cannulas were tunneled subcutaneously and exteriorized at the top of the skull. On the day of the experiment a thin bipolar platinum electrode was placed around a branch of the left renal nerve and insulated with silicone rubber (Wacker Sil-Gel 604) while the rat was under ether anesthesia. Electrode implantation was performed during the same experimental period in the SADa group and 20 days after denervation in SADc group. Measurements were performed 4 to 6 hours after completion of surgery to allow the rat to recover from anesthesia. For completion of the experiments, each rat was placed in the cage in which it had been housed since the previous day (25x15x10-cm Plexiglas cage with a grid floor). The electrode cable and the arterial cannula were attached to special extensions during the recording period, allowing the rat complete freedom of movement within the cage.

Cardiovascular and Nerve Monitoring
AP was recorded in conscious rats by connecting the arterial cannula to a pressure transducer (Statham P23 Db) and a pressure amplifier (model 8805C, Hewlett Packard). The signal from the nerve electrode was recorded after being amplified (Tektronix 5A22N differential amplifier) and filtered (bandpass filter, 100 Hz to 2 kHz). Both AP and the original neurogram were monitored with a storage oscilloscope (Tektronix 5111) and stored on a tape recorder (model 7754A, Hewlett Packard) during a control period of 3 minutes. RSNA and HR responses to changes in AP induced to test baroreflex sensitivity were recorded after control recordings. Further processing was performed using a data acquisition system assembled on a microcomputer (PC AT 386) equipped with an analog-to-digital converter board (10 bits, CAD 10/26, Lynx). An electronic circuit was built for preprocessing the neurogram before digital conversion. This circuit allows subtraction of a desired voltage from the input signal, amplification, full-wave rectification and integration with an analog output provided for oscilloscope monitoring after each stage. At the end of the experiment a dose of phenylephrine was administered to produce a sudden and marked increase in MAP, which inhibited and decreased neural activity to a minimum considered to be the baseline bioelectrical or near-noise signal for subtraction from the original neurogram before integration. Noise subtraction is performed manually with the use of a high-resolution potentiometer followed by amplification with a variable gain to produce a maximum spike amplitude of 10 V. The neurogram is full-wave rectified to preserve all information contained in the negative and positive components of the electrical signal. For this application integration was performed in two modes: the neurogram was integrated over the pressure pulse interval (as shown in the tracings of Fig 2) and voltage reset mode. In the latter integration is determined by the voltage across the capacitor of the integrator rather than by time or event periodicity. In this application every time this voltage level equals 10 V the capacitor is allowed to discharge and produces a barlike signal of constant amplitude with a frequency of occurrence proportional to the density of the input signal. AP and integrated sympathetic activity were filtered and digitized (120 Hz). Systolic and diastolic AP and MAP, HR, and RSNA were determined on a beat-to-beat basis using a specially written software with additional processing performed with a commercial software (EXCEL 5.0, Microsoft). HR was determined to be one over the interval between two successive peaks of the pressure wave. RSNA was expressed by the number of bars per cardiac cycle.^{11 12 13} To compare different groups of rats, RSNA values were expressed in bars per cycle or as a percentage of the maximal (100%) and minimal (0%) nerve activity during 1000 cardiac cycles as described by Lundin et al.¹² Briefly, to normalize for the varying quality of the multifiber recording, values of maximal and minimal nerve activity (100% and 0%) were determined from the 3% of the recorded cardiac cycles that showed the highest and the lowest activity levels. The average "zero nerve activity" was arbitrarily calculated from these 3% out of 1000 cycles recorded because at least 3% of all cardiac cycles in these rats appeared to lack nerve spikes. The 3% of all cardiac cycles with the highest activity was used as the maximal activity.

View larger version (9K): [in this window] [in a new window]   Figure 2. Tracings showing changes in RSNA, integrated nerve activity (IA), and blood pressure (BP) in control (A) and SADa (B) and SADc (C) rats.

Spontaneous and Reflex Baroreceptor Testing
The resting spontaneous relation between AP and RSNA was quantified by averaging RSNA in each pressure class (2 mm Hg) from higher to lower values of systolic pressure obtained during the recording period as described elsewhere.¹³ Briefly, with the use of the recorded 1000 cardiac cycles, we sorted systolic AP values from highest to lowest in classes of 2 mm Hg. The corresponding RSNAs obtained at each pressure class were averaged and are presented in Fig 3. The correlation between AP and RSNA was expressed by fitting a regression line through the points relating averaged RSNA and increasing systolic pressure values of each class. The reflex control of RSNA and HR were evaluated by at least three pressure responses (from 3 to 40 mm Hg) to phenylephrine (0.25 to 4 µg/mL) and sodium nitroprusside (6 to 25 µg/mL) injections. Peak increase or decrease of MAP after every dose of phenylephrine or nitroprusside injection was correlated with peak reflex change of RSNA or HR. The baroreflex sensitivity was analyzed by the regression line obtained by best-fit points relating changes in RSNA (in bars per cycle) or HR (in bpm) and MAP (in millimeters of mercury). The basal nerve activity was obtained by averaging the RSNA in the first 40 cycles immediately before drug injection.

View larger version (20K): [in this window] [in a new window]   Figure 3. Top, line graph showing relation between systolic blood pressure and RSNA expressed by regression lines (mean±SEM) in control and SADa and SADc rats. Bottom, scatterplot showing spontaneous relation between systolic AP (SAP) and averaged RSNA for each systolic pressure class (2 mm Hg) in one SADc rat.

Statistical Analysis
Data are reported as mean±SEM. The results were compared by use of repeated-measures ANOVA. The post hoc test used was the Newman-Keuls test. P.05 was considered significant.

	Results

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Recordings were performed in conscious, unrestrained rats that were usually kept quiet and moved very little. MAP, HR, and RSNA were increased in SADa group rats and returned to control levels 20 days after SAD (Table). Fig 1 shows the histogram of distribution of RSNA activity. In SADa rats there is a lesser proportion (9% versus 67% in controls) of cycles with no synchronized activity (integrated activity >40% of the maximal RSNA),¹⁴ and this explains the greater averaged cycle activity found in these rats. In the SADc group we found a pattern of distribution similar to that of the controls, which explains the normalization of the averaged values of the discharges.

View this table: [in this window] [in a new window]   Table 1. Changes in AP, HR, and RSNA in Control, SADa, and SADc Rat Groups

View larger version (27K): [in this window] [in a new window]   Figure 1. Bar graphs showing the occurrence of cardiac cycles in each level of normalized RSNA in control (top) and SADa (middle) and SADc (bottom) rats. Note the different proportions of cardiac cycles within 0% and 40%.

Original AP tracings, the renal neurogram, and RSNA integrated over the AP pulse interval are shown in Fig 2 to illustrate the differences between control, SADa, and SADc rats. SADc rats showed normalization of RSNA with a higher proportion of silent cycles and consequently with a lower 1:1 synchronization between RSNA and cardiac cycles.

Hypertension and increased AP variability (analyzed by standard deviation of MAP) was detected in SADa rats, whereas in SADc rats the MAP normalized but the increased AP variability persisted (from 6±3 in controls to 13±2 and 15±2, respectively, in SADa and SADc rats). The variability of RSNA expressed by a coefficient relating standard deviation and the average RSNA in 1000 cardiac cycles showed decreased variability in SADa rats (0.22±0.07) and normal variability in SADc rats compared with controls (0.88±0.24 versus 0.77±0.66 in controls).

Spontaneous and Reflex Changes in RSNA
The spontaneous relation between systolic pressure and RSNA is illustrated in Fig 3. The great variability observed in the values of RSNA in different systolic pressure classes in normal rats decreases significantly after SAD. The inverse correlation between systolic pressure and average RSNA in each class of systolic pressure (every 2-mm Hg variation) observed in intact rats disappeared in SADa rats (-0.02±0.01% per mm Hg versus -1.90±0.3% per mm Hg in controls) and SADc rats (-0.32±0.05% per mm Hg).

In response to nitroprusside and phenylephrine SAD rats had an impaired sensitivity for baroreflex control of HR. When the blood pressure increased, the baroreflex bradycardia in SAD rats decreased (from -2.51±0.16 bpm per mm Hg in controls to -0.15±0.01 and -0.60±0.2 bpm per mm Hg in SADa and SADc rats, respectively). The tachycardiac responses to blood pressure reduction were attenuated (from -2.86±0.4 bpm per mm Hg in controls to -0.18±0.02 and -0.7±0.2 bpm per mm Hg in SADa and SADc rats, respectively).

The RSNA responses to blood pressure increases were similarly reduced from -0.9±0.17 bars per cycle in controls to -0.13±0.02 and -0.25±0.1 bars per cycle in SADa and SADc rats, respectively. The RSNA reflex responses to blood pressure decreases decreased from -0.98±0.2 bars per cycle in controls to -0.08±0.03 and -0.37±0.1 bars per cycle in SADa and SADc rats, respectively.

	Discussion

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Anesthesia usually produces marked alterations in the baroreflex mechanisms.¹⁵ Therefore, we analyzed acute and chronic effects of SAD on AP, HR baroreflexes, and RSNA in the conscious rats with the method described by Lundin et al¹² and that we used in previous studies.¹³ The use of multifiber recordings for estimating sympathetic discharges has been criticized^{16 17 18} because of the critical dependence of absolute measured activity on the electrode position. Although the multifiber recording represents a direct approach to quantifying the neurogenic activity in different physiological or pathological conditions, the attachment of the electrode to the nerve is crucial. Therefore, different experimental approaches and different procedures for data normalization¹⁹ have been suggested since the first recordings were performed.^{20 21} Care was taken in the present study (see "Methods") to validate comparisons of RSNA between groups. First, the baseline noise of the postfiltered signal was eliminated, and only activity that exceeded the noise level was considered. Second, the method used to quantify RSNA eliminated the errors of summation existing in other methods.¹⁹ Third, the recording conditions were similar in control and SAD rats. With these approaches a significant increase in RSNA was observed acutely 6 hours after SAD but not after 20 days of SAD. The difference was demonstrated not only when the absolute values of bars per cycle were measured but also by a normalization procedure¹² in which the cycle activity was expressed in percent (0% to 100%) during 1000 cardiac cycles.

Indirect hemodynamic,^{10 21 22} neural,¹¹ and biochemical^{8 9} evidence has indicated that hypertension in the early phase of SAD in rats is produced by sympathetic hyperactivity. In the present study direct recording of RSNA showed a 100% increase in activity within the first 6 hours after SAD, which is higher than the 30% increase detected after 24 hours.²³ These data indicate that the increased sympathetic activity after SAD progressively diminishes or that the different results obtained by Barres et al²³ may be attributed to methodological differences. It is well known that the evaluation of nervous activity by spike counting as used by Barres et al may be inadequate when summation phenomena are present.¹⁹ Indeed, after 20 days of SAD RSNA was normal. Normalization of the sympathetic activity in SADc has been indicated by normalization of HR²⁴ and biochemical measurements⁹ as well as by the reversal of hypertension.⁷ Our hypothesis is that AP and RSNA in SAD are determined by simultaneous elimination of chemoreceptors (hypotensive influence) and baroreceptors (hypertensive influence). In early SAD the effect of baroreceptor denervation with a consequent increase in sympathetic activity and AP is predominant.^{7 11} Later in the chronic stage normalization of RSNA and AP reflect a balance between opposite effects of baroreceptor and chemoreceptor denervation. Also, the interplay of other reflexes (cardiopulmonary, for instance) probably works to reverse the hypertension.^{7 25}

In distinction to the normalization of hyperactivity of RSNA in SADc impairment of baroreflexes is still demonstrable as shown in the present experiments as well as by others.^{23 24} The tendency of the depressed baroreflex to improve in SADc rats was observed Barres et al,²³ who showed improvement of bradycardiac and sympathoinhibition 14 days after SAD in rats. These data suggest that reflex mechanisms other than the arterial baroreflex could be active. One possibility is that cardiopulmonary reflexes could play a role in these responses because they are relatively insensitive to the moment-to-moment changes in AP seen after SAD.²⁶ Another possibility is that the intake of sodium was reduced in SADc rats, since it was demonstrated that blood pressure is salt sensitive in SAD rats²⁷ and that the increase of dietary sodium may increase the gain of baroreflex control of RSNA in Wistar-Kyoto rats.²⁸

The most consistent cardiovascular alteration produced by SADa or SADc is the great increase in AP lability. Previous studies have described similar high variability in dogs,²⁹ cats,³⁰ and rats.^{23 25} Usually, the lability of AP in SAD animals is characterized by an increased standard deviation of AP obtained from computerized recordings.^{24 25} The main determinant of the increased AP lability in SAD rats was attributed to sympathetic hyperactivity because variability decreases after the attenuation of the hyperactivity in SADc rats.²⁵ On the other hand the blockade of sympathetic neural transmission reduced AP lability by 75% in SAD rats.³¹ In the present experiments the higher lability of AP in SADa and SADc rats was accompanied by decreased RSNA variability in SADa rats and normal RSNA variability in SADc rats.

The normalization of RSNA variability with the maintenance of AP fluctuations in SADc rats and of impairment of baroreflex control suggests that the RSNA variability in SADc rats represents fluctuations in sympathetic outflow of central origin. Indeed, the spontaneous relation between systolic pressure and averaged RSNA showed an inverse correlation in control rats that was lost in SADa and SADc rats, indicating that after SAD the AP values are not directly correlated with RSNA. We observed in healthy control rats a cardiac-related discharge pattern or a good synchronization between pulse pressure and bursts of RSNA in distinction to SAD rats in which greater time intervals separated sequential bursts of synchronized activity. It may be an indication that the impairment of baroreflex control of sympathetic outflow may not be the only factor responsible for the increased AP lability in SAD rats. The absence of the beat-to-beat synchronization of the sympathetic activity seems to be important to the generation of increased AP lability in SAD rats.³² Indeed, after ganglion blockade in intact rats³¹ and after the increase in sympathetic activity in SAD rats,¹¹ an increase in AP lability is observed. The common factor under both circumstances is that the baroreflex control of synchronization of sympathetic activity is lost. In this regard studies of Gebber and Barman³³ showed that sympathetic discharges generated by brain stem neurons in a 2 to 6 cycles per second rhythm are still observed after baroreceptor denervation. In animals with intact baroreceptor nerves, however, the 2 to 6 cycles per second rhythm is entrained in a 1:1 relation to the cardiac cycle.

In summary our findings demonstrate that in SADc rats hypertension and the hyperactivity of RSNA observed in SADa rats are diminished whereas the baroreflex control of HR and RSNA is still impaired. Carotid sinus denervation resulting in a diminution of sympathetic drive by the chemoreceptors may play a role not only in decreasing RSNA³⁴ but also in reducing AP.²⁵ Finally, increased lability of AP may be due to the absence of a straight beat-to-beat synchronization between AP and sympathetic nerve activity normally provided by the baroreceptors.

	Selected Abbreviations and Acronyms

 

AP = arterial pressure bpm = beats per minute HR = heart rate MAP = mean arterial pressure RSNA = renal sympathetic nerve activity SAD = sinoaortic denervated, sinoaortic denervation SADa = (rats with) acute SAD SADc = (rats with) chronic SAD

	Acknowledgments

 
This work was supported by Financiadora de Estudos e Projetos (FINEP), Fundação de Amparo a Pesquisado Estado de São Paulo (FAPESP) and Conselho Nacionalde Desenvolvimento Cientifico e Tecnológico (CNPq).

Received June 20, 1995; first decision September 16, 1995; accepted October 12, 1995.

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