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J Appl Physiol 83: 2037-2042, 1997;
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Vol. 83, Issue 6, 2037-2042, December 1997

Autonomic control of skeletal muscle vasodilation during exercise

John B. Buckwalter, Patrick J. Mueller, and Philip S. Clifford

Departments of Anesthesiology and Physiology, Veterans Affairs Medical Center and Medical College of Wisconsin, Milwaukee, Wisconsin 53295

ABSTRACT
INTRODUCTION
METHODS AND PROCEDURES
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES

ABSTRACT

Buckwalter, John B., Patrick J. Mueller, and Philip S. Clifford. Autonomic control of skeletal muscle vasodilation during exercise. J. Appl. Physiol. 83(6): 2037-2042, 1997.---Despite extensive investigation, the control of blood flow during dynamic exercise is not fully understood. The purpose of this study was to determine whether beta -adrenergic or muscarinic receptors are involved in the vasodilation in exercising skeletal muscle. Six mongrel dogs were instrumented with ultrasonic flow probes on both external iliac arteries and with a catheter in a branch of one femoral artery. The dogs exercised on a treadmill at 6 miles/h while drugs were injected intra-arterially into one hindlimb. Isoproterenol (0.2 µg) or acetylcholine (1 µg) elicited increases in iliac blood flow of 89.8 ± 14.4 and 95.6 ± 17.4%, respectively, without affecting systemic blood pressure or blood flow in the contralateral iliac artery. Intra-arterial propranolol (1 mg) or atropine (500 µg) had no effect on iliac blood flow, although they abolished the isoproterenol and acetylcholine-induced increases in iliac blood flow. These data indicate that exogenous activation of beta -adrenergic or muscarinic receptors in the hindlimb vasculature increases blood flow to dynamically exercising muscle. More importantly, because neither propranolol nor atropine affected iliac blood flow, we conclude that beta -adrenergic and muscarinic receptors are not involved in the control of blood flow to skeletal muscle during moderate steady-state dynamic exercise in dogs.

blood flow; acetylcholine; muscarinic; beta -adrenergic; dogs

INTRODUCTION

VASODILATION in active skeletal muscles during steady-state exercise reflects the high oxygen demands associated with exercise. The mechanism by which vasodilation to active skeletal muscles is maintained is poorly understood. It is well known that beta -adrenergic receptors and muscarinic receptors are present in the arterial vasculature of skeletal muscle (4, 11, 13, 25). There is some evidence suggesting that sympathetic beta -adrenergic (11, 14, 15, 20) and sympathetic cholinergic (22) receptors may play a role in the increase in blood flow to exercising skeletal muscle. In addition, it has been postulated that acetylcholine spillover from the neuromuscular junctions of exercising skeletal muscles may provide a source of acetylcholine for muscarinic-receptor-mediated vasodilation during exercise (23).

The purpose of this study was to examine the role of beta -adrenergic-receptor-mediated and muscarinic-receptor-mediated vasodilation in active skeletal muscles during steady-state exercise. We used a unique experimental approach that allowed examination of blood flow to one hindlimb without affecting systemic hemodynamics in conscious exercising dogs. We hypothesized that there is ongoing beta -adrenergic-receptor and muscarinic-receptor-mediated vasodilation during steady-state exercise.

METHODS AND PROCEDURES

All experimental procedures were approved by the Institutional Animal Care and Use Committee and conducted in accordance with the American Physiological Society's "Guiding Principles in the Care and Use of Animals." Six mongrel dogs, weighing between 20 and 24 kg, were selected for their willingness to run on a motorized treadmill and were instrumented in a series of sterile surgical procedures. Anesthesia was induced with thiopental sodium (15-30 mg/kg; Gensia Pharmaceuticals, Irvine, CA). After intubation of the dogs with a cuffed endotracheal tube, a surgical level of anesthesia was maintained through mechanical ventilation with 1.5% halothane (Halocarbon Laboratories, River Edge, NJ) and 98.5% oxygen. Antibiotics (cefazolin sodium, Apothecon, Princeton, NJ) and analgesic drugs (buprenorphine hydrochloride, 0.3 mg; Reckitt and Colman, Kingson-upon-Hull, UK) were given postoperatively. During the first surgical procedure, the carotid arteries were placed in skin tubes in the neck so that they could be cannulated percutaneously to measure arterial blood pressure (17, 18). In the second surgery, all dogs were instrumented with flow probes (4- or 6-mm ultrasonic transit-time flow probes, Transonic Systems, Ithaca, NY) around the external iliac arteries to measure hindlimb blood flow. The cables were tunneled under the skin to the back, and the dogs were given 2 wk to recover from flow-probe implantation. In the final surgery, a heparinized catheter (0.045 in. OD, 0.015 in. ID, Data Science International, St. Paul, MN) was implanted chronically through a side branch of the femoral artery for drug infusion. The catheter was tunneled to the back of the dog. The catheter was flushed daily with saline and filled with a heparin lock (100 IU heparin/ml in 50% dextrose solution) to maintain patency. The dogs were given at least 2 days to recover from the final surgery before any experiments were performed.

All experiments were performed in a laboratory in which the temperature was maintained below 20°C. A 20-gauge Teflon catheter (Angiocath, Deseret, Sandy, UT) was inserted retrogradely into the lumen of the carotid artery and attached to a solid-state pressure transducer (Viggo-Spectramed, Oxnard, CA). The flow probes were connected to a transit-time flowmeter (Transonic Systems). The dogs ran on a motorized treadmill at 6 miles/h (mph; 9.7 km/h) 0% grade, which represents a moderate workload. Six minutes into exercise, either a nonselective beta -receptor agonist (0.2 µg isoproterenol, Abbott Laboratories, Chicago, IL) or a muscarinic-receptor agonist (1 µg acetylcholine, Sigma Chemical, St. Louis, MO) was infused intra-arterially. Blood flow returned to baseline, and the relevant antagonist (1 mg propranonol, nonselective beta -receptor antagonist, or 500 µg atropine, muscarinic-receptor antagonist) was infused at 10 min of exercise. The above doses were determined in pilot studies that showed that the agonist doses nearly doubled iliac blood flow and that the antagonist doses were sufficient to abolish the response to subsequent agonist infusion. At least 24 h separated each beta -adrenergic-receptor or muscarinic-receptor blockade experiment.

Arterial blood pressure and right and left external iliac blood flow were simultaneously written to paper on a polygraph recorder (model 7, Grass Instruments, Warwick, RI) and stored on both a videocassette data recorder (model D, Vetter, Rebersburg, PA), and computer (Apple 8500 Power PC) by using a MacLab system at 100 Hz (AD Instruments, Castle Hill, Australia). Data were analyzed off-line by using the MacLab software to calculate mean arterial pressure (MAP), heart rate (HR), iliac blood flow, and iliac vascular conductance (blood flow/MAP). Control measurements were averaged over 30 s before drug infusion. For each drug infusion, all variables were averaged over 1-s intervals, and the peak response was recorded. Where no response was obvious, the peak response was chosen over the same interval where it occurred with the initial agonist infusion.

Statistical analyses of the data were performed with a one-way repeated-measures analysis of variance for isoproterenol and acetylcholine infusions. An alpha  level of 0.05 was used to establish statistical significance. Where significant F-ratios were found, a Tukey's post hoc test was performed. A paired t-test was used to examine hemodynamic changes before and after antagonist infusions. All descriptive statistics are presented as means ± SE.

RESULTS

Figure 1 is an original raw tracing from an individual dog exercising on the treadmill at 6 mph, 0% grade. The initial intra-arterial infusion of 0.2 µg isoproterenol caused a marked increase in blood flow and conductance in the experimental limb, with no corresponding changes in blood flow or conductance in the contralateral control limb. It is also apparent that there were no changes in MAP or HR with this bolus infusion. Blood flow quickly returned to baseline levels. Subsequent infusion of 1 mg of propranolol elicited no change in blood flow in the experimental or control limbs. It also produced no systemic cardiovascular effects (Table 1). After administration of propranolol, intra-arterial infusion of isoproterenol no longer produced blood flow changes in the experimental limb. Figure 2 summarizes the changes in iliac conductance with intra-arterial infusions of isoproterenol and propranolol in six dogs. There were statistically significant (P < 0.001) increases in iliac blood flow (89.8 ± 14.4%) and conductance (93.8 ± 15.2%) with intra-arterial infusion of isoproterenol before propranolol. However, there were no statistically significant differences (P > 0.05) in iliac blood flow or iliac conductance with propranolol infusion (0.7 ± 3.6 and -1.7 ± 4.1%, respectively) or isoproterenol infusion after propranolol (-0.1 ± 2.3 and 0.8 ± 2.4%, respectively).

Fig. 1. Original tracing from 1 dog during steady-state exercise at 6 miles/h, 0% grade. There was an immediate increase in blood flow and conductance in experimental limb with intra-arterial bolus of 0.2 µg of isoproterenol. In contrast, bolus of 1 mg of propranolol did not alter blood flow or conductance. Subsequent infusion of 0.2 µg of isoproterenol demonstrated effectiveness of beta -receptor blockade. None of the intra-arterial bolus infusions altered systemic blood pressure or blood flow in control limb.
[View Larger Version of this Image (27K GIF file)]

Table  1.   Hemodynamic values before and after antagonist infusion during exercise at 6 miles/h, 0% grade
MAP, mmHg HR, beats/min Control Limb Blood Flow, ml/min Experimental Limb Blood Flow, ml/min
Atropine
  Pre 114 ± 2.8  165 ± 10  560 ± 70  494 ± 58 
  Post 113 ± 3.4  166 ± 11  553 ± 72  482 ± 58 
Propranolol
  Pre 114 ± 2.9  162 ± 15  609 ± 106  496 ± 51 
  Post 117 ± 3.5  159 ± 14  614 ± 109  500 ± 51
Values are means ± SE. MAP, mean arterial pressure; HR, heart rate. There were no statistically significant differences (P > 0.05) between any of the preantagonist (Pre) variables and the postantagonist (Post) variables.

Fig. 2. Response to intra-arterial infusion of isoproterenol (Iso; 0.2 µg) and propranolol (1 mg) in experimental limb during steady-state exercise. Values are means ± SE. * Isoproterenol elicited a significant increase (P < 0.001) in iliac conductance before (pre), but not after (post), propranolol. Propranolol had no significant effect on iliac conductance.
[View Larger Version of this Image (31K GIF file)]

Similar results were found when the effects of the muscarinic-receptor agonist and antagonist were examined. Figure 3 is an original tracing from an individual dog exercising on the treadmill at 6 mph, 0% grade. Notice that the initial infusion of 1 µg acetylcholine caused a marked increase in blood flow and conductance in the experimental limb with no corresponding changes in blood flow or conductance in the contralateral limb. After blood flow returned to baseline, an infusion of 500 µg of atropine produced no changes in iliac blood flow or conductance. A subsequent infusion of 1 µg of acetylcholine no longer produced any changes in iliac blood flow or conductance. As with isoproterenol and propranolol, none of these infusions affected MAP or HR (Table 1). Figure 4 summarizes the changes in iliac conductance with intra-arterial infusions of acetylcholine and atropine in six dogs. There were statistically significant increases (P < 0.001) in blood flow (95.6 ± 17.4%) and conductance (90.1 ± 17.5%) with intra-arterial infusion of acetylcholine before atropine. However, there were no statistically significant differences (P > 0.05) in iliac blood flow or iliac conductance with atropine infusion (-2.3 ± 2.7 and -1.4 ± 3.1%, respectively) or acetylcholine infusion after atropine (5.7 ± 4.0 and 5.1 ± 5.5%, respectively).

Fig. 3. Original tracing from 1 dog during steady-state exercise at 6 miles/h, 0% grade. There was an immediate increase in blood flow and conductance in experimental limb with intra-arterial bolus of 1 µg of acetylcholine. In contrast, bolus of 500 µg of atropine did not alter blood flow or conductance. Subsequent infusion of 1 µg of acetylcholine demonstrated effectiveness of muscarinic-receptor blockade. None of the intra-arterial bolus infusions altered systemic blood pressure or blood flow in control limb.
[View Larger Version of this Image (25K GIF file)]

Fig. 4. Response to intra-arterial infusion of acetylcholine (ACh; 1 µg) and atropine (500 µg) in experimental limb during steady-state exercise. Values are means ± SE. * Acetylcholine elicited a significant increase (P < 0.001) in iliac conductance before, but not after, atropine. Atropine had no significant effect on iliac conductance.
[View Larger Version of this Image (31K GIF file)]

DISCUSSION

We observed no changes in canine hindlimb blood flow during dynamic exercise after blockade of beta -adrenergic or muscarinic receptors. The lack of an effect indicates that neither beta -adrenergic nor muscarinic receptors are involved in skeletal muscle hyperemia during moderate steady-state dynamic exercise in the dog. The experimental design in this study provides several distinct advantages over previous attempts to examine the role of beta -adrenergic or muscarinic receptors during exercise. Intra-arterial infusion of small doses of receptor antagonists creates a functionally isolated hindlimb in which localized blockade is produced in the experimental limb without confounding systemic changes in HR or MAP. Administration of antagonists during, rather than before, exercise interrupts ongoing beta -adrenergic-receptor or muscarinic-receptor activation. Coupled with continuous recordings of blood flow, this allows both control and experimental measurements during the same bout of exercise. Furthermore, because redundant mechanisms may be involved in the control of skeletal muscle blood flow, continuous recordings should allow the detection of any transient changes in blood flow, which would precede activation of compensatory mechanisms. Finally, infusion of antagonists during exercise ensures accessibility of receptors on blood vessels recruited during exercise.

beta -Blockade. Previous studies examining the role of beta -adrenergic-receptor-mediated vasodilation during exercise have come to conflicting conclusions. Several studies reported a reduction in blood flow to working skeletal muscle with beta -adrenergic blockade (2, 11, 14, 15, 20), whereas others found no effect (12, 13). In the studies that found reductions in skeletal muscle blood flow during exercise with beta -receptor blockade, there were also markedly lower HRs reported (2, 12, 13, 17, 20). Most certainly this was the result of blockade of beta 1-receptors in the heart and could have produced corresponding decreases in cardiac output and MAP with reflex increases in sympathetic outflow. In fact, Lisander and Nilsson (16) showed that systemic propranolol administration increased total peripheral resistance via baroreceptor-mediated increases in sympathetic constriction rather than abolishment of ongoing beta 2-receptor-mediated vasodilation in the anesthetized cat. Furthermore, Smith and Warren (24) found greater reductions in skeletal muscle blood flow with a single oral dose of the selective beta 1-receptor antagonists, metoprolol and atenolol, than with a single oral dose of the nonselective antagonist, propranolol. Thus systemic cardiovascular changes observed in previous studies have made it difficult to draw firm conclusions regarding beta 2-receptor-mediated skeletal muscle vasodilatation during dynamic exercise.

In the present study the influence of beta -adrenergic receptors on skeletal muscle hyperemia during steady-state dynamic exercise was examined by using small doses of a non-beta -receptor antagonist to avoid confounding systemic cardiovascular changes. The nonselective beta -adrenergic-receptor antagonist, propranolol, was chosen because of previously reported beta 1- and beta 2-receptor-mediated vasodilation in the skeletal muscle vasculature of dogs (25). Because of the small dose of propranolol and its localized effect, no beta 1-receptor-mediated reductions in HR were apparent, and any changes in blood flow would reflect ongoing beta -adrenergic-receptor-mediated vasodilation alone. However, the results show no evidence of beta -receptor-mediated vasodilation in the hindlimb vasculature of dynamically exercising dogs. Two previous studies employing intra-arterial infusions of propranolol in humans came to similar conclusions (12, 13). Hartling et al. (12) and Juhlin-Dannfelt and Astrom (13) found no beta -receptor-mediated exercise hyperemia in skeletal muscle of the forearm or leg. Thus to date there is little support for a role of beta -adrenergic receptors in the blood-flow response to steady-state exercise.

We reasoned that activation of beta -adrenergic receptors during exercise would be mediated by increased epinephrine release from the adrenal medulla or increased norepinephrine release from sympathetic nerve terminals. It is likely that there is only mild adrenal activation in dogs at the workload employed in this study (21). However, two lines of evidence suggest that there is an increase in efferent sympathetic nerve traffic to skeletal muscle during dynamic exercise. First, DiCarlo et al. (8) made direct measurements of postganglionic sympathetic nerve activity to the hindlimb (lumbar sympathetic trunk) in rats. They showed that there was an immediate and sustained increase in lumbar sympathetic nerve activity in response to dynamic exercise in rats. Second, our group (6) and O'Leary et al. (19) have recently demonstrated that there is substantial alpha 1-adrenergic-receptor restraint of skeletal muscle blood flow at mild, moderate, and severe workloads in dogs. We interpret these results to indicate that there is release of norepinephrine from sympathetic nerve terminals in the canine skeletal muscle vasculature across a wide range of exercise intensities. The data from the present study indicate that vascular beta -receptors are not activated by the norepinephrine released from these nerve terminals.

Although beta -adrenergic receptors do not play a role in skeletal muscle hyperemia during steady-state exercise, this study does not rule out a potential role for them at the onset of exercise. Indeed, Laughlin and Armstrong (15) reported no difference in rat hindlimb blood flow with propranolol at 5 min of exercise but did find significantly lower blood flow during the first 30 s of exercise. beta -Adrenergic receptors also appear to play a role in postexercise hyperemia, as previously shown by several investigations (12, 24).

Muscarinic blockade. The existence of sympathetic cholinergic-mediated vasodilation in the vasculature of skeletal muscle has been demonstrated in a number of studies (4, 5, 7, 22). These sympathetic cholinergic dilator fibers have been shown to be activated by the defense reaction (7). Interestingly, the cardiovascular changes associated with exercise such as tachycardia, increases in MAP, vasoconstriction in the visceral organs, and vasodilation to skeletal muscle are also seen with electrical stimulation of regions of the brain eliciting the defense reaction (1, 7, 9, 10). However, the mechanisms for skeletal muscle vasodilation arising from the defense reaction and steady-state exercise appear to differ. In particular, skeletal muscle vasodilation evoked by the defense reaction can be blocked by atropine (4, 5, 7), whereas the results of the present study demonstrate that exercise hyperemia was unaffected by muscarinic-receptor blockade. Thus muscarinic receptors do not appear to be involved in the elevated blood flow to dynamically exercising skeletal muscle during steady-state exercise, although these results do not preclude involvement of muscarinic receptors at the onset of exercise.

Sanders and colleagues (22) were able to demonstrate sympathetic cholinergic-mediated vasodilation in conjunction with forearm exercise. However, this atropine-sensitive dilation was in the contralateral resting forearm. In contrast, several studies using systemic doses of atropine found little evidence to support the involvement of muscarinic receptors in exercise hyperemia. Bolme and Novotny (4) reported that elevations of canine iliac blood flow in anticipation of exercise, but not during exercise, were abolished with atropine. Similarly, systemic doses of atropine did not alter skeletal muscle blood flow during treadmill exercise in rats (3, 20). However, it must be noted that the existence of sympathetic cholinergic fibers in the rat is in doubt (5).

Recently it has been postulated that, besides sympathetic cholinergic fibers, another possible physiological source of acetylcholine release during exercise is the neuromuscular junction (23, 26). This is an attractive hypothesis, which would provide a link between muscular contraction and blood flow, because motor nerve activity and skeletal muscle blood flow both increase at the onset of exercise and are augmented in an intensity-dependent manner. However, our results are not consistent with the hypothesis that acetylcholine spillover from the neuromuscular junction mediates skeletal muscle hyperemia during steady-state dynamic exercise.

In conclusion, the results from the present study show that, although functionally present, neither sympathetic beta -adrenergic nor muscarinic receptors mediate skeletal muscle hyperemia during moderate steady-state dynamic exercise in dogs.

ACKNOWLEDGEMENTS

The authors acknowledge the valuable technical assistance of Paul Kovac.

FOOTNOTES

   This project was supported by the Medical Research Service of the Department of Veterans Affairs and the National Heart, Lung, and Blood Institute.

Address for reprint requests: P. S. Clifford, Anesthesia Research 151, Veterans Affairs Medical Center, 5000 W. National Ave., Milwaukee, WI 53295.

Received 27 May 1997; accepted in final form 18 August 1997.

REFERENCES

1. Abrahams, V. C., S. M. Hilton, and A. W. Zbrozyna. Active muscle vasodilatation produced by stimulation of the brainstem: its significance in the defence reaction. J. Physiol. (Lond.) 154: 491-513, 1960.
2. Ahlborg, G., and A. Juhlin-Dannfelt. Effect of beta -receptor blockade on splanchnic and muscle metabolism during prolonged exercise in men. J. Appl. Physiol. 76: 1037-1042, 1994[Abstract/Free Full Text].
3. Armstrong, R. B., and M. H. Laughlin. Atropine: no effect on exercise muscle hyperemia in conscious rats. J. Appl. Physiol. 61: 679-682, 1986[Abstract/Free Full Text].
4. Bolme, P., and J. Novotny. Conditional reflex activation of sympathetic cholinergic vasodilator nerves in the dog. Acta Physiol. Scand. 77: 58-67, 1969[Medline].
5. Bolme, P., J. Novotny, B. Uvnas, and P. G. Wright. Species distribution of sympathetic cholinergic vasodilator nerves in skeletal muscle. Acta Physiol. Scand. 78: 60-64, 1970[Medline].
6. Buckwalter, J. B., P. J. Mueller, and P. S. Clifford. Sympathetic vasoconstriction to active skeletal muscles during dynamic exercise. J. Appl. Physiol. 83: 1575-1580, 1997[Abstract/Free Full Text].
7. Dean, C., and J. H. Coote. Discharge patterns in postganglionic neurones to skeletal muscle and kidney during activation of the hypothalamic and midbrain defence areas in the cat. Brain Res. 377: 271-278, 1986[Medline].
8. DiCarlo, S. E., C.-Y. Chen, and H. L. Collins. Onset of exercise increases lumbar sympathetic nerve activity in rats. Med. Sci. Sports Exerc. 28: 677-684, 1996[Medline].
9. Djojosugito, A. M., B. Folkow, P. H. Kylstra, B. Lisander, and R. S. Tuttle. Differentiated interaction between the hypothalamic defence reaction and baroreceptor reflexes. 1. Effects on heart rate and regional flow resistance. Acta Physiol. Scand. 78: 376-385, 1970[Medline].
10. Eliasson, S., B. Folkow, P. Lindgren, and B. Uvnas. Activation of sympathetic vasodilator nerves to the skeletal muscles in the cat by hypothalamic stimulation. Acta Physiol. Scand. 23: 333-351, 1951[Medline].
11. Gullestad, L., J. Hallen, and O. M. Sejersted. Variable effects of beta -adrenoceptor blockade on muscle blood flow during exercise. Acta Physiol. Scand. 149: 257-271, 1993[Medline].
12. Hartling, O. J., I. Noer, T. L. Svendsen, J. P. Clausen, and J. Trap-Jensen. Selective and non-selective beta -adrenoceptor blockade in the human forearm. Clin. Sci. Lond. 58: 279-286, 1980[Medline].
13. Juhlin-Dannfelt, A., and H. Astrom. Influence of beta -adrenoceptor blockade on leg blood flow and lactate release in man. Scand. J. Clin. Lab. Invest. 39: 179-183, 1979[Medline].
14. Kowalchuk, J. M., C. S. Klein, and R. L. Hughson. The effect of beta-adrenergic blockade on leg blood flow with repeated maximal contractions of the triceps surae muscle group in man. Eur. J. Appl. Physiol. 60: 360-364, 1990.
15. Laughlin, M. H., and R. B. Armstrong. Adrenoreceptor effects on rat muscle blood flow during treadmill exercise. J. Appl. Physiol. 62: 1465-1472, 1987[Abstract/Free Full Text].
16. Lisander, B., and H. Nilsson. Baroreceptor-induced decrease in muscle blood flow upon propranolol administration. Eur. J. Pharmacol. 50: 275-278, 1978[Medline].
17. Meier, M. A., and D. M. Long. Carotid artery loop for repeated catheterization of the left ventricle in dogs. Surgery 70: 797-799, 1971[Medline].
18. O'Brien, D. J., W. H. Chapman, F. V. Rudd, and J. W. McRoberts. Carotid artery loop method of blood pressure measurement in the dog. Am. J. Physiol. 260 ((Heart Circ. Physiol. 29): H37-H41, 1971.
19. O'Leary, D. S., E. D. Robinson, and J. L. Butler. Is active skeletal muscle functionally vasoconstricted during dynamic exercise in conscious dogs? Am. J. Physiol. 272 ((Regulatory Integrative Comp. Physiol. 41): R386-R391, 1997[Abstract/Free Full Text].
20. Overton, J. M. Influence of autonomic blockade on cardiovascular responses to exercise in rats. J. Appl. Physiol. 75: 155-161, 1993[Abstract/Free Full Text].
21. Peronnet, F., R. A. Nadeau, J. deChamplain, P. Magrassi, and C. Chatrand. Exercise plasma catecholamines in dogs: role of adrenals and cardiac nerve endings. Am. J. Physiol. 241 ((Heart Circ. Physiol. 10): H243-H247, 1981.
22. Sanders, J. S., A. L. Mark, and D. W. Ferguson. Evidence for cholinergically mediated vasodilation at the beginning of isometric exercise in humans. Circulation 79: 815-824, 1989[Abstract/Free Full Text].
23. Segal, S. S., and D. T. Kurjiaka. Coordination of blood flow control in the resistance vasculature of skeletal muscle. Med. Sci. Sports Exerc. 27: 1158-1164, 1995[Medline].
24. Smith, R. S., and D. J. Warren. Effect of acute oral beta adrenergic blockade on muscle blood flow in man. Cardiovasc. Res. 16: 205-208, 1982[Medline].
25. Vatner, S. F., D. R. Knight, and T. H. Hintze. Norepinephrine-induced beta 1-adrenergic peripheral vasodilation in conscious dogs. Am. J. Physiol. 249 ((Heart Circ. Physiol. 18): H49-H56, 1985.
26. Welsh, D. G., and S. S. Segal. Acetylcholine release from motor nerves triggers vasodilation (Abstract). FASEB J. 10: A55, 1996.



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