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Department of Physiology, Wayne State University, School of Medicine, Detroit, Michigan 48201
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ABSTRACT |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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We tested the hypothesis that dynamic exercise resets the operating point and attenuates the gain of the arterial baroreflex regulation of heart rate (HR) in rats. Seven adult female spontaneously hypertensive rats (SHR) were chronically instrumented with left carotid arterial catheters. After the rats recovered, arterial baroreflex function was examined by recording reflex changes in HR in response to spontaneous changes in arterial pressure (AP) during a preexercise condition and during steady-state treadmill running at 6 and 18 m/min. Dynamic exercise at 6 and 18 m/min, respectively, reduced the spontaneous range (by 55 and 70%) and spontaneous gain (by 64 and 82%) of the arterial baroreflex control of HR. Dynamic exercise at 6 and 18 m/min, respectively, also increased the pressure at the midpoint of the spontaneous pressure range (by 7 and 12%), the spontaneous minimum HR response (by 35 and 59%), the HR at the midpoint of the spontaneous HR range (by 31 and 52%), and the spontaneous maximum HR response (by 27 and 46%). Sinoaortic denervation eliminated the relationship between AP and HR by reducing the spontaneous gain 95%. These results demonstrate that dynamic exercise shifted the operating point of the arterial baroreflex to a higher pressure and reduced the spontaneous gain in female SHR.
spontaneous arterial baroreflex; hypertension
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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THE ARTERIAL BAROREFLEX functions as a short-term, negative feedback regulator of arterial pressure (AP). An increased AP elicits an arterial baroreflex-mediated bradycardia and sympathoinhibition that compensates for the elevation in pressure. Conversely, a decreased AP elicits an arterial baroreflex-mediated tachycardia and sympathoexcitation that compensates for the decrease in pressure. It is apparent, however, that there are situations when both AP and heart rate (HR) increase simultaneously, i.e., dynamic exercise (19-21). This apparent paradox (simultaneous increase in HR and AP) may be explained by at least two possibilities. First, the arterial baroreflex may have a reduced gain or sensitivity during exercise. That is, the exercise-induced elevation in pressure is no longer a sufficient stimulus to elicit a reflex bradycardia (2, 17). A second possibility is that dynamic exercise resets the operating point (pressure sought by the reflex) of the arterial baroreflex to a higher pressure (5, 6, 10, 13, 15, 16, 18, 20). That is, the operating point of the baroreflex is shifted to a higher pressure so that the reflex now operates around (considers "normal") the new higher pressure. These possibilities have only been examined in normotensive canines (10, 15) and humans (2, 16-18). The generally accepted conclusion from these studies is that dynamic exercise is associated with a rapid resetting of the operating point, without a change in the gain of the arterial baroreflex, in normotensive humans and dogs (13, 20, 21).
However, this question has not been examined in rats. The response may be different in rats because the autonomic mechanisms mediating the arterial baroreflex changes in HR depend, in part, on the baseline level of sympathetic and parasympathetic tone (13, 15). Rats differ in their baseline level of sympathetic and parasympathetic tone from normotensive humans and dogs. At rest, the hearts of normotensive humans and dogs are predominantly under parasympathetic control with little to no sympathetic tone. However, during exercise, tonic parasympathetic and sympathetic tone exists (14). Thus, whereas the gain of the arterial baroreflex regulation of HR is not altered during exercise in dogs (10, 15) and humans (16, 18), the autonomic mechanisms mediating the reflex changes in HR are altered (15). In contrast, the hearts of rats are predominantly under sympathetic control at rest, and dynamic exercise further increases the level of sympathetic tone. Because the baseline level of autonomic tone can affect the magnitude of the arterial baroreflex changes in HR (15), it is reasonable to postulate that the spontaneous gain of the arterial baroreflex regulation of HR will be reduced during exercise in a species wherein the autonomic balance is different from those previously investigated.
We tested the hypothesis that dynamic exercise resets the operating point and attenuates the spontaneous gain of the arterial baroreflex regulation of HR in rats. We studied female hypertensive rats because the resting level of sympathetic tone and the sympathetic response to exercise are exaggerated in female vs. male and hypertensive vs. normotensive rats (4). Arterial baroreflex function was determined by recording reflex changes in HR during spontaneous changes in AP. This method eliminated many of the compounding influences of pharmacological changes in AP (8).
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Surgical Procedures
Intact condition. All procedures involving animals were in accordance with the guidelines established by the Institutional Animal Care and Use Committee. Seven adult female spontaneously hypertensive rats (SHR) were instrumented using aseptic surgical procedures. The rats were anesthetized with an intramuscular injection of xylazine (8 mg/kg), chlorpromazine hydrochloride (4 mg/kg), and ketamine hydrochloride (40 mg/kg). All rats were instrumented with a Teflon catheter inserted into the descending aorta via the left common carotid artery for measurements of AP and HR. The arterial catheter was flushed daily with heparinized saline, filled with heparin (1,000 U/ml), and plugged with a paraffin-filled obturator. The animals were allowed at least 3 days to recover. Rats were carefully monitored for signs of infection and changes in body weight during the recovery period. During this time, the rats were familiarized with running on the treadmill and experimental procedures. At the time of the experimental protocols, all rats were healthy and gaining weight.
Sinoaortic denervation condition. After completion of the experimental protocol in the intact condition, five rats underwent complete sinoaortic denervation (SAD). The rats were anesthetized as described above. An anterior cervical incision was made and the carotid arteries were isolated at the region of the carotid sinus. All nerves and tissues were stripped from the sinus, the carotid artery, and all branches above and below the area of the sinus. The aortic depressor nerves were isolated bilaterally and sectioned. The mean recovery time for the SAD rats was 8 ± 3 days.
Experimental Measurements
AP and HR were determined by connecting the arterial catheter to a Gould P23XL pressure transducer that was coupled to a MacLab BRIDGE amplifier. AP and HR analog signals were digitized at 200 samples/s by a MacLab 8 analog-to-digital converter and laboratory computer (Macintosh LCII).Experimental Protocol
Rats in the intact condition were oriented to the laboratory and investigators for at least 3 days before the experimental protocol began. On the day of the experiment, the rats were placed on the treadmill to obtain baseline hemodynamic data and spontaneous baroreflex responses. During the 2-h baseline period, control values for AP and HR were recorded. At the end of the 2-h baseline period, the rats ran on the treadmill at 6 m/min, 10% grade, while the data were continuously recorded. After hemodynamic variables reached a steady state (~5 min), the speed of the treadmill was gradually increased to 18 m/min. Animals ran at 18 m/min until AP and HR reached a steady state.The five rats in the SAD condition were studied only during the preexercise condition. On the day of the experiment, the rats were placed in a large Plexiglas box, and spontaneous arterial baroreflex responses were recorded.
Evaluation of Spontaneous Arterial Baroreflex Regulation of HR
Absolute values for HR (in beats/min) were used to evaluate the capability of the arterial baroreflex to increase or decrease HR during spontaneous changes in AP. Raw data points were collected on a beat-to-beat basis. For the analysis of the relationship between systolic blood pressure (SBP) and the reflex responses in HR, the computer recorded SBP for each heartbeat. This pressure was then plotted against the HR recorded during the subsequent heartbeat at the point of the diastolic pressure (8). The number of beats sampled ranged from 400 to 600 beats. To illustrate the results of this analysis and goodness of fit, Fig. 1 presents the actual data points during a preexercise condition and following SAD in one animal. Because spontaneous increases and decreases in pressure produced a linear curve for the arterial baroreflex regulation of HR, the data from each animal were fit by a linear regression with HR being regressed on SBP. The slope of the regression line was used as an index of the overall spontaneous arterial baroreflex sensitivity or spontaneous gain for each animal under each condition. Figure 2 presents the method for determining arterial baroreflex function parameters for the arterial baroreflex regulation of HR. P1 represents the spontaneous range of HR, P4 is the spontaneous minimum HR response, and the spontaneous maximum HR response is the sum of P1 and P4. P3 represents the pressure at the midpoint of the spontaneous pressure range, whereas H3 represents the HR at the midpoint of the spontaneous HR range. Figure 3 presents actual data points illustrating the relationship between SBP and HR for one rat in the preexercise condition and during exercise at 6 and 18 m/min.
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The absolute data were then plotted as group means to determine the relationship between SBP and HR. The data points for SBP were divided into 5-mmHg bins for each curve under the three conditions. Each of these pressure points and the corresponding HR were then averaged and plotted for each of the three conditions (Fig. 4).
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Data Analysis
All data are expressed as means ± SE. A one-way ANOVA with repeated measures was used to compare P1, P3, H3, P4, spontaneous maximum HR, and spontaneous gain at preexercise vs. exercise. Significant interactions indicated by the one-way ANOVA were evaluated by a test of simple effects post hoc analysis. To evaluate the effect of SAD, we used an unpaired t-test to evaluate the difference between spontaneous gain of the intact and SAD animals during the preexercise condition. An
-level of 0.05 was used to
determine statistical significance.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Figure 1 presents actual data points that illustrate the relationship
between spontaneous changes in SBP and reflex responses in HR for a
preexercise period in the intact and SAD conditions. Resting MAP and HR
for the intact and SAD rats were 158 ± 3 vs. 173 ± 11 mmHg and 343 ± 9 vs. 325 ± 10 beats/min, respectively. SAD completely eliminated
the relationship between HR and AP. The intact and SAD animals had a
mean gain of 1.31 ± 0.14 and 0.063 ± 0.05 beats · min
1 · mmHg1,
respectively. These data show that the gain decreased 95% after SAD.
Figure 3 presents actual data points that illustrate the relationship between reflex changes in HR during spontaneous changes in SBP during a preexercise condition and during dynamic exercise at 6 and 18 m/min in one rat. As the exercise intensity increased, the spontaneous gain and correlation coefficient of the spontaneous arterial baroreflex regulation of HR decreased.
Figure 4 presents the group means for the spontaneous arterial baroreflex regulation of HR during a preexercise condition and during dynamic exercise. These data illustrate that dynamic exercise altered the spontaneous arterial baroreflex regulation of HR. The spontaneous arterial baroreflex was operating at a higher pressure and HR with a reduced gain.
Table 1 presents the spontaneous arterial baroreflex function parameters for the intact rats during the preexercise condition and during dynamic exercise. Dynamic exercise reduced both the spontaneous range of HR (by 55 and 70%) and the spontaneous gain (by 64 and 82%) at 6 and 18 m/min, respectively. Dynamic exercise also increased P3 (by 7 and 12%), H3 (by 31 and 52%), P4 (by 35 and 59%), and the spontaneous maximum HR (by 27 and 46%) at 6 and 18 m/min, respectively. These results demonstrate that each grade of dynamic exercise progressively reset the operating point of the arterial baroreflex upwards and to the right, and this shift was accompanied by a reduction in the spontaneous range and gain in female SHR.
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The arterial baroreflex has two important functions. First, the arterial baroreflex is a negative feedback reflex that regulates AP around a preset value called a set or operating point. Second, the arterial baroreflex also establishes the prevailing systemic AP by setting the operating point (22). That is, modulating the response of barosensitive neurons in the central nervous system establishes the operating point or prevailing systemic AP (3, 5, 19). Therefore, the operating point of the arterial baroreflex is not fixed but is variable over a wide range of pressures and is determined by a variety of inputs from the peripheral and central nervous systems (22).
Results from this study demonstrate that a single bout of dynamic exercise reset the operating point to a higher pressure and reduced the spontaneous gain of the arterial baroreflex control of HR. Specifically, during exercise, both AP and HR were elevated above preexercise levels. Furthermore, the spontaneous range and gain of the arterial baroreflex control of HR were reduced. In addition, the pressure at the midpoint of the pressure range, the HR at the midpoint of the HR range, and the spontaneous minimum and maximum HR of the arterial baroreflex control of HR were elevated during exercise. These data suggest that the exercise-induced elevation in AP and HR are mediated by both a reduction in spontaneous gain and a resetting of the operating point of the arterial baroreflex to higher pressures.
Influence of SAD on the Arterial Baroreflex Regulation of HR
To verify that the arterial baroreflex was responsible for the reflex responses in HR following spontaneous changes in AP, we compared arterial baroreflex function between intact and SAD rats. SAD significantly attenuated the relationship between AP and HR by reducing the spontaneous gain and the correlation coefficient of the linear regression analysis. Thus the arterial baroreflex is required for the reflex responses in HR following spontaneous changes in AP.Potential Mechanisms for Arterial Baroreflex Resetting
The mechanisms responsible for the exercise-induced shift of the operating point of the arterial baroreflex to a higher pressure and the reduction in spontaneous gain in hypertensive rats are unknown. Arterial baroreflex resetting and a reduction in gain may occur centrally at the nucleus of the solitary tract (NTS) by modulating the response of barosensitive neurons (3, 5). However, speculation as to the site of alteration in baroreflex control during exercise should not be limited to NTS neurons or input to NTS neurons by central command. Several additional sites may be involved. For example, it is possible that baroreceptor afferents become desensitized because of the exercise-induced increase in AP, thereby reducing afferent input to the NTS. Additionally, modulation of afferent input could be influenced by humoral changes that occur as a result of exercise. Alterations during exercise could also occur at the efferent side of the reflex. For example, neurons in the caudal ventral lateral medulla or rostral ventral lateral medulla could be altered. Finally, input to brainstem sites from hypothalamus or limbic regions may be responsible for the exercise effect.Other factors contributing to the reduction in gain during dynamic exercise involve the relative balance of sympathetic and parasympathetic control of HR. The arterial baroreflex mediates reflex changes in HR by altering both cardiac parasympathetic and sympathetic activity. An increased AP elicits an arterial baroreflex-mediated cardiac parasympathetic activation and cardiac sympathetic inhibition. In contrast, a decreased AP elicits an arterial baroreflex-mediated cardiac parasympathetic inhibition and cardiac sympathetic excitation. Furthermore, the arterial baroreflex responses to changes in AP are dependent on the baseline level of cardiac parasympathetic and sympathetic tone. O'Leary and Seamans (15) reported that the sensitivity of the arterial baroreflex control of HR was not different between rest and exercise in normotensive dogs; however, the autonomic mechanisms mediating the reflex changes in HR were different. These investigators concluded that the exercise-induced shift of the autonomic balance of the heart at rest from parasympathetic dominance to sympathetic dominance during exercise maintained arterial baroreflex sensitivity [dogs maintain substantial parasympathetic tone even during dynamic exercise (14)] but shifted the autonomic components mediating the reflex changes in heart rate.
In contrast, we examined arterial baroreflex responses during a preexercise condition and during dynamic exercise in female hypertensive rats. The experimental model is critical for understanding the potential mechanisms responsible for our results. Sympathetic activity is higher and parasympathetic activity is lower at rest in rats, females, and hypertensive states compared with canines or humans, males, or normotensive states. This difference in autonomic balance at rest is amplified during exercise (4). Thus, in contrast to canines or humans, female hypertensive rats are sympathetically dominated at rest (no significant parasympathetic control), and this dominance is amplified during exercise (4). This lack of cardiac autonomic balance may contribute to the reduced sensitivity of the arterial baroreflex control of HR in rats.
Assessment of Perturbational Methods for Determining Arterial Baroreflex Function
Frankel and colleagues (8) were the first investigators to assess the arterial baroreflex regulation of HR by recording continuous spontaneous fluctuations in AP and the corresponding reflex changes in HR over several hundred consecutive beats. These investigators adopted this methodology because of a number of theoretical and practical concerns regarding the more traditional methods for assessing cardiac baroreflex sensitivity.For example, baroreceptors respond to the average AP as well as the
rate of change of AP (dP/dt) (22). Nitric oxide (NO) donors and
-agonists alter pulse pressure (PP), average AP, and dP/dt.
However, alterations in PP and dP/dt differ in direction and
magnitude with the pharmacological agents (1). Furthermore, the
vasoactive properties of the drugs can differentially affect the
relationship between baroreceptor activity and pressure due to changes
in the coupling between the receptors and the vascular smooth muscle
(11).
Recent evidence also suggests that -agonists and NO donors have a
direct effect on the heart independently of the arterial baroreflex.
For example, NO increased the spontaneous beating rate in isolated
sinoatrial node preparations (12), whereas -agonists have a direct
chronotropic influence on the heart (23). Thus changes in HR in
response to vasoactive substances reflect an arterial
baroreflex-mediated response as well as a direct effect on the heart.
Similarly, NO can directly increase the spontaneous discharge rate of NTS neurons, independently of alterations in AP (9). Furthermore, microinjections of sodium nitroprusside (SNP) into the paraventricular nucleus (PVN, a site of central integration of autonomic cardiovascular responses) elicited a significant decrease in renal sympathetic nerve activity, AP, and HR (24). Thus, by directly altering the excitability of NTS and/or PVN neurons, NO has a direct effect on central autonomic regulation of the cardiovascular system. Taken together, these results document the need for a method to examine arterial baroreflex responses that are not subjected to the multiple effects of vasoactive agents.
Finally, there are no methods that selectively alter arterial baroreflex function. For example, the hemodynamic effects of vasoactive drugs (e.g., venous pooling, elevations in afterload) elicit cardiopulmonary responses. Similarly, vascular occluders also cause venous pooling or elevations in afterload. Furthermore, the responses obtained by altering carotid sinus pressure via the neck-collar method are opposed by intact aortic baroreceptors (7). However, the nonperturbational spontaneous arterial baroreflex method appears to selectively reflect arterial baroreflex function, inasmuch as SAD reduced the relationship between SBP and HR by 95%.
In summary, results from this study demonstrate that dynamic exercise resets the operating point of the arterial baroreflex to a higher pressure and reduces the gain of the arterial baroreflex control of HR in rats. The reduction in gain may result from the cardiac autonomic imbalance (sympathetic dominance at rest and during exercise) in rats. The results from this study suggest that exercise-induced elevations in AP and HR are mediated by both a reduction in gain and a resetting of the operating point of the arterial baroreflex to a higher pressure in rats.
Perspectives
The arterial baroreflex regulation of HR at rest and during exercise has previously only been investigated in humans and dogs, species with cardiac autonomic balance different from rats. The conclusion from these studies is that dynamic exercise is associated with a rapid resetting of the operating point without a change in gain of the arterial baroreflex. Species or conditions (hypertension) with low parasympathetic and high sympathetic tone may have responses different from humans or dogs because the baseline level of cardiac autonomic tone can affect the magnitude of the arterial baroreflex changes in HR. Because a large number of investigators study smaller species (rats, rabbits, and, increasingly, mice) to understand autonomic control mechanisms, it was important to examine this question in the rat.| |
ACKNOWLEDGEMENTS |
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This work was supported by National Heart, Lung, and Blood Institute Grant HL-OD58192 and by American Heart Association Ohio-West Virginia Affiliate Grant AK-95-02-S.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: S. E. DiCarlo, Dept. of Physiol., Wayne State University, School of Medicine, Scott Hall, 540 E. Canfield Ave., Detroit, MI 48201.
Received 8 May 1998; accepted in final form 2 September 1998.
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