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Vol. 83, Issue 6, 2091-2097, December 1997
Department of Physiology, The University of Texas Health Science Center, San Antonio, Texas 78284-7764
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Ryan, Kathy L., W. Fred Taylor, and Vernon S. Bishop.
Arterial baroreflex modulation of heat-induced vasodilation in the
rabbit ear. J. Appl. Physiol. 83(6):
2091-2097, 1997.
The purpose of this study was to determine
whether nonthermal baroreflexes arising from cardiopulmonary
and/or arterial baroreceptors modulate rabbit ear blood flow
(EBF) during hyperthermia. Intact and sinoaortic-denervated (SAD)
rabbits were chronically instrumented with a Doppler ultrasonic flow
probe for measurement of EBF velocity (kHz). During whole body heating
in conscious rabbits, EBF and ear vascular conductance (EVC) increased
as core temperature increased until maximal plateau levels of EBF and
EVC were reached. The maximal plateau level of EVC attained during heat
stress was lower in SAD than in intact rabbits. Subsequent
intrapericardial administration of procaine at maximal EBF blocked
cardiac afferents but did not alter EVC in either animal group. In a
second experiment, ramp decreases in mean arterial pressure were
produced by vena caval occlusion at maximal EBF. In intact rabbits, EBF
and EVC decreased linearly as mean arterial pressure fell, but EBF and
EVC did not decrease during vena caval occlusion in SAD rabbits. Thus
neither pharmacological nor mechanical unloading of cardiac
baroreceptors results in reflex vasoconstriction in the heat-stressed
rabbit ear. However, baroreflexes arising from arterial baroreceptors
may modulate EBF in heat-stressed rabbits.
temperature regulation; blood pressure regulation; baroreflexes; skin blood flow; conscious rabbits
INTRODUCTION ALTHOUGH SOME DOUBTS linger (20, 31), the preponderance
of evidence indicates that baroreflexes participate in the regulation of the cutaneous circulation in humans (13, 28). In normothermic humans, baroreceptor unloading produces cutaneous vasoconstriction (2,
9, 29, 34). The ability of the baroreflex to modulate skin blood flow
(SkBF) persists during hyperthermia (7, 14, 16), thereby facilitating
the maintenance of blood pressure in the face of simultaneous
challenges to thermoregulation and blood pressure regulation. Thus the
baroreflex competes with thermoregulatory reflexes to produce an
integrated cutaneous vascular response to combined challenges in
humans.
In animal models, however, evidence concerning baroreflex control of
the cutaneous circulation is not as clear. In cats, cutaneous sympathetic nerve activity is not clearly synchronous with the cardiac
cycle (11, 12, 17, 23), leading some to conclude that the cutaneous
circulation is not under baroreflex control. However, hemorrhage is
clearly associated with cutaneous vasoconstriction in mice (36), rats
(25, 27, 30, 32), rabbits (21), and dogs (3, 4). Early reports
suggested that this cutaneous vasoconstriction is the result of
elevated levels of catecholamines (3) or vasopressin (27) rather than
direct baroreceptor-mediated alterations in sympathetic outflow. In a
more recent study, however, O'Leary and Johnson (25) clearly
demonstrated that vasoconstriction of the tail occurs during hemorrhage
in normothermic and hyperthermic rats and that this vasoconstriction is
of neural origin and not solely dependent on circulating
vasoconstrictor agents. These investigators thus concluded that
baroreflexes directly control sympathetic outflow to the tail
vasculature.
In a separate but related issue, it is also unclear whether
baroreceptor input acts to modulate peripheral vascular responses to
heat stress. In anesthetized dogs, abolition of arterial and cardiopulmonary baroreceptor reflexes failed to alter increases in
hindpaw blood flow during heating of the spinal cord (5). Furthermore,
acute removal of arterial baroreceptor input did not modify decreases
in sympathetic nerve activity to the skin produced by thermal challenge
in anesthetized cats (22). Thermoregulatory cutaneous vasodilation in
the absence of baroreceptor input has not been examined further.
Recently, it has been demonstrated that arterial blood pressure, heart
rate (HR), and visceral vascular resistance responses to nonexertional
heat stress are altered in conscious rats lacking intact arterial
baroreflexes and that sinoaortic deafferentation reduces thermal
tolerance (18).
Investigation of the interaction between thermoregulatory and
baroreceptor control of SkBF has been hindered by the lack of an animal
that closely models the human in terms of the nervous control of SkBF.
As previously noted, the tail of the rat responds to baroreflexes
during normothermia and hyperthermia (25), but the rat tail does not
possess an active neurogenic vasodilator system (28). In contrast, an
active vasodilator system mediates at least 90% of the total human
cutaneous vascular response to hyperthermia (28). Recently, we reported
that ~80% of the increase in rabbit ear blood flow (EBF) during
hyperthermia is the result of activation of sympathetic vasodilator
nerves (33). For this reason, the rabbit ear may be a useful model to
study interactions between thermoregulatory and nonthermoregulatory
reflexes. Therefore, this study was designed to determine whether the
rabbit ear vasculature is on the efferent arm of the baroreflex.
Specifically, we sought to determine whether
1) arterial baroreceptor input
modulates cardiovascular and thermoregulatory responses to heat stress
and 2) cardiopulmonary and arterial
baroreceptors modulate EBF in heat-stressed rabbits.
METHODS Seventeen New Zealand White rabbits (1.8-3.0 kg) of either sex
were housed in individual cages and maintained on a 12:12-h light-dark
cycle. Animals were given free access to water and standard rabbit
chow, supplemented by fresh cabbage and carrots. All animal care and
use were in accordance with National Institutes of Health guidelines
(20a).
Surgical Procedures
After a recovery period of at least 2 wk, the rabbits were again anesthetized, and a silicone rubber-tipped catheter was placed into the ascending aorta via a femoral artery for the measurement of arterial blood pressure. At the same time, a closed-tip catheter was placed alongside a common carotid artery for the later insertion of a copper-constantan thermocouple (model IT-18, Physitemp Instruments) to measure core temperature (Tc). A Doppler ultrasonic flow probe was also placed around a central ear artery for the measurement of EBF. All catheters and flow probe wires were exteriorized at the back of the neck. The arterial catheter was heparinized every other day. An antibiotic (amoxicillin, 75 mg/kg) was administered for up to 5 days after each surgical procedure. Rabbits were allowed 3-4 days to recover from surgery and were trained daily to sit quietly in a standard rabbit restrainer.
Six rabbits underwent sinoaortic denervation (SAD) before thoracotomy. In these rabbits the aortic depressor and carotid sinus nerves were exposed through a midcervical incision. Aortic depressor nerves were cut at the level of the nodose ganglia. The bifurcations of the external and internal carotid arteries were isolated and stripped of all nerve fibers. The region of the carotid sinus was then painted with 10% phenol. All animals were allowed to recover for at least 2 wk before undergoing further surgery.
After the animals recovered from catheter implantation, the efficacy of
the SAD procedure was assessed by acutely increasing arterial blood
pressure via a bolus intravenous infusion (through a marginal ear vein)
of phenylephrine. Denervation was considered complete if HR decreased
20 beats/min in response to a 40-mmHg increase in mean arterial
pressure (MAP). All the SAD rabbits used in this study completed this
test successfully.
Recordings
EBF, blood pressure, and HR were continuously recorded during all experiments on a polygraph (model 611, Beckman). Arterial blood pressure was measured with a transducer (model CDX2, Cobe). Instantaneous HR was determined by a cardiotachometer (model 9857b, Beckman) triggered from the arterial pressure pulse. EBF was measured by a Doppler ultrasonic flowmeter (C. Hartley, Baylor College of Medicine). Mean EBF and MAP were recorded by passing the pulsatile signals through low-pass filters. Ear vascular conductance (EVC) was calculated by dividing EBF by MAP. Tc was measured by connecting the thermocouple to a 37.0°C electronic reference junction, which provided a digital readout; Tc was noted every 5 min throughout the experiment. Outputs from the Beckman recorder were connected to an analog-to-digital converter (MacLab, WPI), and digitized values were displayed and recorded using a Macintosh microcomputer.Experimental Protocols
On the day of the experiment, the conscious rabbit was placed in a restrainer and wrapped in a rubber pad through which warmed water could be circulated. The rabbit was then allowed to stabilize for 20-30 min. After this control period, whole body heating (WBH) was begun by circulating warm (41°C) water through the rubber pad. The time required for EBF to reach a maximum plateau level ranged from 40 to 120 min. This plateau level was taken to be the maximal response to WBH, because further minor increases in Tc failed to produce further increments in EBF. At this point, Tc was maintained at a relatively constant level by adjusting the temperature of the water circulating through the pad. On completion of experimental manipulations, WBH was ended, and the rabbit was exposed to ambient temperature during a recovery period of ~30 min. Protocol 1. This protocol was designed to determine whether pharmacological blockade of cardiac afferents produces reflex vasoconstriction in the rabbit ear during thermal stress. It was performed on rabbits with intact arterial baroreflexes (n = 6) and on those without arterial baroreflexes (SAD, n = 4). On the morning of the experiment, the rabbit was placed in the restrainer and allowed to stabilize while MAP and HR were recorded. Veratridine (20 µg/kg) was then administered intrapericardially; this dose of veratridine typically decreased MAP by 15-35 mmHg. The rabbit was then removed from the restrainer and returned to its cage. At least 2 h later, the rabbit was again placed in the restrainer, and after a control period, WBH was begun. Once maximal EBF levels were reached and maintained, the local anesthetic procainamide HCl (2%, 1 ml) was administered intrapericardially. Cardiac autonomic blockade was maintained for at least 30 min by further administration of 0.1-ml increments of procainamide at 15-min intervals. At the end of this period, veratridine (20 µg/kg) was once again infused into the pericardial sac to test the efficacy of the blockade. Blockade was considered complete if MAP was unaltered by this second dose of veratridine. Administration of procainamide in such a fashion anesthetizes afferent and efferent innervation to the heart (8). Protocol 2. This protocol sought to determine whether mechanical unloading of arterial and cardiopulmonary baroreceptors during WBH results in reflex vasoconstriction in the ear. Again, this protocol was performed in rabbits with intact arterial baroreceptors (n = 6) and in SAD rabbits (n = 6). One of the intact rabbits was subjected to protocols 1 and 2; four of the SAD rabbits performed both protocols. Rabbits were placed in the restrainer, and after a control period, WBH was performed. When maximal EBF values were attained, ramp decreases in MAP were produced by progressive inflation of the vena caval occluder over a 5-min period. At least three vena caval occlusions were performed during WBH, with a stabilization period of at least 10 min between each occlusion. Data derived from these three periods of occlusion were averaged to yield mean values of each measured parameter for each animal.Necropsy
After the completion of experiments, rabbits were euthanized by an overdose of pentobarbital sodium. In all rabbits, visual inspection verified that the tip of the catheter was properly positioned within the pericardium.Statistical Analysis
To determine the effects of WBH per se on intact and SAD rabbits, data derived from both protocols were pooled for each group. Student's t-test was used to compare times required for maximal vasodilation, rates of heating, and thresholds for vasodilation between groups (37). A two-way analysis of variance (ANOVA) with repeated measures was applied to determine differences in preheat and peak heat values within and between each group (37). This was followed by the Student-Newman-Keuls multiple-comparison test where appropriate (37). To determine differences between groups over time during the initial phases of WBH (Fig. 1), a two-way ANOVA followed by the Student-Newman-Keuls test was also applied.
To determine the effects of procaine administration during WBH (protocol 1), a randomized block ANOVA with repeated measures was followed by the Student-Newman-Keuls multiple comparison test.
For the experiments of protocol 2, EBF, EVC, and HR values during vena caval occlusion were first plotted vs. MAP. Linear regression analysis was then applied, yielding regression coefficients (slopes) and y-intercept values for each relationship in each rabbit. These raw values describing the individual lines for each rabbit were then averaged, yielding mean regression coefficients and y-intercept values for each group (i.e., intact and SAD rabbits). Student's t-test was then used to determine statistical differences between the line descriptor values from intact and SAD rabbits (37). In all statistical tests, P < 0.05 was considered significant. Values are means ± SE.
RESULTS
Responses to WBH
Normothermic (pre-WBH) levels of Tc, HR, EBF, and EVC were similar in intact and SAD rabbits (Table 1, Fig. 1). However, MAP was higher in SAD than in intact rabbits. Figure 1 illustrates the increases in EBF and EVC in response to increasing Tc during the initial phase of heating. During the early period of WBH shown in Fig. 1, there were no significant differences in Tc, EBF, and EVC at any of the time points between the two groups of animals. Figure 1 includes only time points during which each member of the group was exposed to WBH in the absence of procainamide infusion or vena caval occlusion; because of the range of WBH exposure times required to attain maximal ear vasodilation, the final time point graphed in intact and SAD rabbits thus differs and reflects the animal with the lowest WBH exposure time to reach this point in each group. The Tc threshold for ear vasodilation was 40.30 ± 0.16°C in intact rabbits and 40.28 ± 0.28°C in SAD rabbits; again, these values did not differ statistically. Subsequently, EBF increased to a similar plateau level in both groups (Table 1). Very importantly, however, the maximal level of EVC achieved was significantly lower in SAD rabbits (Table 1). The time of WBH exposure required to reach maximal ear vasodilation in intact and SAD rabbits was 66 ± 7 and 61 ± 8 min, respectively; these values were not statistically different. Furthermore, the absence of arterial baroreceptor input did not alter the Tc at which maximal vasodilation occurred (Table 1) or the rate of Tc increase: 0.024 ± 0.004 and 0.026 ± 0.003°C/min for intact and SAD rabbits, respectively. The pre-WBH difference in MAP between SAD and intact rabbits was maintained during WBH, inasmuch as WBH did not alter the control value of this variable in either group (Table 1, Fig. 1). HR did not significantly increase during WBH within either group, although HR values in SAD rabbits during WBH were slightly but significantly greater than those in intact rabbits (Table 1, Fig. 1).
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Protocol 1
Intrapericardial administration of local anesthetic at maximal ear vasodilation during WBH failed to alter EBF, MAP, or EVC in intact rabbits (Fig. 2). In SAD rabbits, intrapericardial procainamide produced a significant decrease in EBF but only after a delay of 30 min (Fig. 3). This slight decrease in EBF was the result of a reduction in MAP, because EVC did not change after procainamide treatment. In all animals, veratridine challenge 30 min after procainamide treatment failed to alter MAP (data not shown), indicating complete blockade of cardiac afferents.
Protocol 2
The linear regression coefficients of the EBF-MAP, EVC-MAP, and HR-MAP relationships produced by vena caval occlusion during WBH were significantly lower in SAD than in intact rabbits (Table 2, Fig. 4). Indeed, the slope of the EVC-MAP relationship in SAD rabbits was not statistically different from 0. EBF and EVC decreased as MAP fell in rabbits with intact arterial baroreflexes. Simultaneously, HR reflexly increased during vena caval occlusion in intact rabbits. In contrast, neither EBF nor EVC fell during MAP decreases in rabbits without arterial baroreflexes. Furthermore, the reflex increase in HR that normally accompanies a depression in MAP was dramatically reduced in SAD rabbits.
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DISCUSSION
There are two major findings derived from this study. First, sinoaortic deafferentation limits the maximal cutaneous vasodilatory response to WBH in rabbits. Second, decreases in arterial blood pressure result in baroreflex-induced vasoconstriction in the hyperthermic rabbit ear. Therefore, the ear vasculature of the rabbit is on the efferent arm of the baroreflex. However, baroreflex modulation of EBF occurs via unloading of arterial baroreceptors, without major contribution from cardiopulmonary baroreceptors.
Previous reports have indicated that the degree of cutaneous vasodilation (5) and the decrease in sympathetic nerve activity to the skin (22) produced by application of thermal stimuli are similar in acute anesthetized animal preparations with and without intact baroreceptor reflexes. In contrast, results from this study demonstrate that in the chronic absence of input from arterial baroreflexes the cutaneous vasodilatory response in conscious rabbits is significantly altered. Although the threshold for vasodilation and maximal EBF attained during WBH did not differ between intact and SAD rabbits, the maximal level of EVC reached by SAD animals was significantly attenuated. Thus SAD acts to limit the cutaneous vasodilatory response during hyperthermia. To our knowledge, this is the first report of an alteration in a specific physiological response subserving thermoregulation in SAD animals. Although Kregel et al. (18) demonstrated that thermal tolerance in rats is dependent on intact arterial baroreceptor reflexes, they did not measure a specific heat loss mechanism such as cutaneous vasodilation. Despite their attenuated maximal cutaneous vasodilatory response, however, SAD rabbits did not demonstrate an increased heating rate and decreased thermal tolerance.
How does SAD limit the ability of the rabbit ear to vasodilate during heat stress? The mechanism producing this response has yet to be investigated. On the basis of the available data, however, we offer the following suggestions. First, it is unlikely that this attenuated response could be due to unloading of the remaining baroreceptor input (i.e., from cardiopulmonary baroreceptors) during heat stress, because the data contained here effectively eliminate any major contribution from cardiopulmonary baroreceptors. Additionally, there does not appear to be a possible stimulus for such a mechanism, because neither cardiac output nor HR is altered by hyperthermia in the rabbit (19), suggesting that stroke volume and venous return are also unaltered. More probably, the elimination of baroreceptor input from arterial baroreceptors acts at a central location to limit the maximal cutaneous vasodilatory response to WBH. That is, this study demonstrates that decreases in arterial baroreceptor input by SAD or by unloading of intact baroreceptors (vena caval occlusion in intact animals) result in decreases in EVC. This observation suggests that baroreceptor input somehow acts at a central integratory site to allow maximal thermoregulatory responses. When baroreceptor input decreases, cutaneous vasodilation may be limited by increasing sympathetic vasoconstrictor tone or decreasing sympathetic vasodilatory tone to ear cutaneous vascular beds (see below). Determination of the precise mechanism subserving this response remains to be investigated.
Previously, we demonstrated that the rabbit ear possesses an active neurogenic vasodilator system, as does human nonapical skin (33). We now report that the rabbit ear is also on the efferent arm of the baroreceptor reflex during hyperthermia, inasmuch as unloading of baroreceptors produces dramatic decreases in EBF and EVC in intact rabbits. This finding is similar to previous observations that indicate that the cutaneous circulation of humans subserves not only thermoregulatory but also nonthermoregulatory functions (13). Hence, the integrated response to combined thermoregulatory and nonthermoregulatory challenges in rabbits and humans is one that favors the maintenance of cardiovascular homeostasis while compromising temperature regulation. Similarly, blood flow in the rat tail is also modulated by baroreflexes during hyperthermia (25); however, the rat tail does not possess an active vasodilator system (26). Therefore, of the animal models extensively studied, the efferent control of blood flow in the rabbit ear most closely models that of the cutaneous circulation in humans, inasmuch as the rabbit ear possesses an active vasodilator system and is modulated by nonthermoregulatory reflexes originating from baroreceptors.
Alterations of EBF in response to hypotensive episodes during hyperthermia are dependent primarily on input from arterial baroreceptors. Two lines of evidence support this contention. First, pharmacological blockade of cardiopulmonary baroreceptor input via intrapericardial administration of procainamide did not decrease EVC during heat stress in intact or SAD rabbits. Theoretically, if cardiopulmonary baroreceptors were on the afferent arm of a baroreflex affecting EVC, pharmacological unloading of cardiac afferents should result in reflex vasoconstriction in the ear, especially in SAD rabbits without arterial baroreceptor input. Second, decreases in arterial blood pressure produced by vena caval occlusion failed to alter EVC in SAD rabbits. If cardiopulmonary baroreceptors were involved in triggering reflex increases in vasoconstriction, EVC would have declined to some degree as blood pressure decreased, inasmuch as input from cardiopulmonary baroreceptors is still intact in these animals. Because neither of these events occurred, one must conclude that cardiopulmonary baroreceptors do not make a major contribution to the observed modulation of EBF during heat stress.
Alternatively, it is possible that WBH per se may unload the cardiopulmonary baroreceptors to such an extent that subsequent pharmacological or mechanical unloading produces no further limitation on EVC. Although we cannot totally discount this possibility, no data are available in animals or humans to support this contention.
The finding that cardiopulmonary baroreceptor unloading fails to produce sympathetic vasoconstriction in the rabbit ear during hyperthermia contrasts markedly with the traditional view of the level of control exerted by cardiopulmonary baroreceptors on the cutaneous circulation in humans (13). In normothermic humans, small reductions in right atrial pressure (in the absence of decreases in MAP or arterial pulse pressure) result in large reductions in forearm blood flow and comparatively small reductions in splanchnic blood flow (1, 13, 15). Although forearm blood flow consists of muscle and skin components, forearm SkBF has been demonstrated to be decreased by application of mild, nonhypotensive levels of lower body negative pressure in mildly hyperthermic humans (24, 34). Hence, baroreflex control of forearm SkBF in humans has been thought to be mediated largely by cardiopulmonary baroreceptors, whereas visceral blood flow appears to be more sensitive to control by arterial baroreceptors (13). However, this view of the differential organization of vascular control in humans has recently been challenged, inasmuch as others have failed to observe cutaneous vasoconstriction in response to low levels of lower body negative pressure during hyperthermia (6, 10, 35). Which baroreceptor population acts to mediate cutaneous vasodilation in humans therefore remains controversial.
Baroreflex modulation of SkBF during heat stress could conceivably occur via 1) increases in sympathetic vasoconstrictor activity, 2) decreases in sympathetic vasodilator activity, or 3) some combination of these two effects. Recently, Kellogg and colleagues (16) attempted to determine which of these possibilities occurs in heat-stressed humans exposed to hypotensive episodes produced by lower body negative pressure. In this elegant study, these investigators iontophoresed bretylium into human skin, thereby abolishing vasoconstrictor control while leaving the active vasodilator system intact. Bretylium treatment failed to alter cutaneous vasoconstrictor responses to lower body negative pressure in hyperthermic humans, clearly demonstrating that the baroreceptor reflex exerts control over the active neurogenic vasodilator system in human skin. Presumably, such integration of the baroreflex and thermoregulatory reflexes must therefore occur within the nervous system (16). The present study does not address how baroreflex modulation of thermoregulatory SkBF occurs in the rabbit ear. Whether the mechanism involves increases in sympathetic vasoconstrictor activity or withdrawal of active vasodilator activity awaits further investigation. If it is subsequently determined that modulation of rabbit EBF by the baroreflex occurs by withdrawal of active sympathetic vasodilator activity, as it does in humans, it would be of considerable interest to investigate where this integration occurs and how it might be altered by other nonthermoregulatory reflexes. The use of the rabbit model offers the possibility of investigating such questions using more invasive methods than those available to human studies.
In conclusion, the arterial baroreceptors modulate cutaneous vasodilatory responses to heat stress in the conscious rabbit. Therefore, the vasculature of the rabbit ear is clearly on the efferent arm of the baroreflex and acts to maintain cardiovascular homeostasis during combined thermoregulatory and nonthermoregulatory challenges. Furthermore, baroreflex modulation of EVC during heat stress is mediated predominantly by the arterial baroreceptors without significant input from the cardiopulmonary baroreceptors. Further study is necessary to elucidate the efferent mechanism(s) by which the arterial baroreflex modulates heat-induced increases in EVC.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the superb technical support of Linda K. Stahl, E. Anne Josey, and Brenda Friesenhahn. They also thank Sue Garner for expert secretarial support.
FOOTNOTES
Address for reprint requests: V. S. Bishop, Dept. of Physiology, The University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78284-7764.
Received 13 May 1996; accepted in final form 20 August 1997.
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