John B. Buckwalter

The Paradox of Sympathetic Vasoconstriction in Exercising Skeletal Muscle

BUCKWALTER, J.B., and P.S. CLIFFORD. The paradox of sympathetic vasoconstriction in exercising skeletal muscle. Exerc. Sport Sci. Rev., Vol. 29, No. 4, pp. 159–163, 2001. Is there sympathetic vasoconstriction in exercising skeletal muscle? Although convincing evidence exists that demonstrates vasoconstriction in active muscle, the proposition that the sympathetic nervous system constricts skeletal muscle during exercise poses a paradox, given the robust vasodilation that occurs in muscle during exercise. Ultimately, muscle perfusion is a balance between metabolic vasodilation and sympathetic vasoconstriction.

Mechanical compression elicits vasodilatation in rat skeletal muscle feed arteries

To date, no satisfactory explanation has been provided for the immediate increase in blood flow to skeletal muscles at the onset of exercise. We hypothesized that rapid vasodilatation is a consequence of release of a vasoactive substance from the endothelium owing to mechanical deformation of the vasculature during contraction. Rat soleus feed arteries were isolated, removed and mounted on micropipettes in a sealed chamber. Arteries were pressurized to 68 mmHg, and luminal diameter was measured using an inverted microscope. Pressure pulses of 600 mmHg were delivered for 1 s, 5 s, and as a series of five repeated 1 s pulses with 1 s between pulses. During application of external pressure the lumen of the artery was completely closed, but immediately following release of pressure the diameter was significantly increased. In intact arteries (series 1, n= 6) for the 1 s pulse, 5 s pulse and series of five 1 s pulses, the peak increases in diameter were, respectively, (mean ±s.e.m.) 16 ± 2, 14 ± 2 and 27 ± 3%, with respective times from release of pressure to peak diameter of 4.1 ± 0.3, 4.6 ± 0.7 and 2.8 ± 0.4 s. In series 2 (n= 9) the arteries increased diameter by 15 ± 2, 15 ± 2 and 30 ± 3% before and by 8 ± 1, 8 ± 1 and 21 ± 2% after removal of the endothelium with air. The important new finding in these experiments is that mechanical compression caused dilatation of skeletal muscle feed arteries with a time course similar to the change in blood flow after a brief muscle contraction. The magnitude of dilatation was not affected by increasing the duration of compression but was enhanced by increasing the number of compressions. Since removal of the endothelium reduced but did not abolish the dilatation in response to mechanical compression, it appears that the dilatation is mediated by both endothelium‐dependent and ‐independent signalling pathways.

Sympathetic vasoconstriction in active skeletal muscles during dynamic exercise

Studies utilizing systemic administration of alpha-adrenergic antagonists have failed to demonstrate sympathetic vasoconstriction in working muscles during dynamic exercise. The purpose of this study was to examine the existence of active sympathetic vasoconstriction in working skeletal muscles by using selective intra-arterial blockade. Six mongrel dogs were instrumented chronically with flow probes on the external iliac arteries of both hindlimbs and with a catheter in one femoral artery. All dogs ran on a motorized treadmill at three intensities on separate days. After 2 min, the selective alpha 1-adrenergic antagonist prazosin (0.1 mg) was infused as a bolus into the femoral artery catheter. At mild, moderate, and heavy workloads, there were immediate increases in iliac conductance of 76 +/- 7, 54 +/- 11, and 22 +/- 6% (mean +/- SE), respectively. Systemic blood pressure and blood flow in the contralateral iliac artery were unaffected. These results demonstrate that there is sympathetic vasoconstriction in active skeletal muscles even at high exercise intensities.

Vasodilatation is obligatory for contraction-induced hyperaemia in canine skeletal muscle

There is a rapid increase in blood flow to active skeletal muscle with the onset of exercise, but the mechanism(s) eliciting this increase remains elusive. We hypothesized that the rapid increase in blood flow to active skeletal muscle with the onset of exercise is attributable to vasodilatation as a consequence of smooth muscle hyperpolarization. To test this hypothesis we examined the blood flow response to a brief tetanic contraction in which potassium (K+) was infused intra‐arterially to elevate the [K+]o and clamp the smooth muscle membrane potential within the skeletal muscle vascular bed. In six anaesthetized beagle dogs control contractions increased hindlimb blood flow by 97 ± 14 ml min−1. During K+ infusion the hyperaemic response to contraction was 8 ± 3 ml min−1. Since the hindlimb blood flow was reduced during K+ infusion, a similar reduction in baseline blood flow was produced with phenylephrine infusion. During phenylephrine infusion the hyperaemic response to contraction was preserved (89 ± 23 ml min−1). Recovery contractions performed after the discontinuation of the K+ infusion elicited blood flow responses similar to control (100 ± 11 ml min−1). In a separate experimental protocol using the isolated gastrocnemius muscle of mongrel dogs (n= 6) K+ infusion did not alter force production by the skeletal muscle. Our data indicate that in the absence of vasodilatation, there is virtually no change in blood flow. One implication of this finding is that the muscle pump cannot be responsible for the initial contraction‐induced hyperaemia. We conclude that the increase in blood flow immediately following a single muscle contraction is due to vasodilatation, presumably as a consequence of smooth muscle hyperpolarization.

α-Adrenergic vasoconstriction in active skeletal muscles during dynamic exercise

Sympathetic vasoconstriction in working muscles during dynamic exercise has been demonstrated by intra-arterial administration of α1-adrenergic antagonists. The purpose of this study was to examine the existence of α1- and α2-adrenergic receptor-mediated vasoconstriction in active skeletal muscles during exercise. Six mongrel dogs were instrumented chronically with flow probes on the external iliac arteries of both hindlimbs, and a catheter was inserted in one femoral artery. All dogs ran on a motorized treadmill at three exercise intensities (3 miles/h, 6 miles/h, and 6 miles/h at 10% grade) on separate days. After 5 min of exercise, a selective α1- (prazosin) or a selective α2-adrenergic antagonist (rauwolscine) was infused as a bolus into the femoral arterial catheter (only one drug per day). The doses of the antagonists were adjusted to maintain the same effective concentration at each exercise intensity. At the mild, moderate, and heavy workloads prazosin infusion produced immediate increases in iliac conductance of 65 ± 9, 35 ± 6, and 18 ± 4% (means ± SE), respectively, and increases in blood flow of 290 ± 24, 216 ± 23, and 172 ± 18 ml/min, respectively. Rauwolscine infusion produced increases in conductance of 52 ± 5%, 36 ± 5%, and 26 ± 3%, respectively, and blood flow increases of 250 ± 34, 244 ± 39, and 259 ± 35 ml/min at the three workloads. Systemic blood pressure and blood flow in the contralateral iliac artery were unaffected by any of the antagonist infusions. These results demonstrate that there is ongoing α1- and α2-adrenergic receptor-mediated vasoconstriction in exercising skeletal muscles even at heavy workloads and that the magnitude of vasoconstriction decreases as exercise intensity increases.

Autonomic control of skeletal muscle blood flow at the onset of exercise

The purpose of this study was to determine whether the autonomic nervous system is involved in skeletal muscle vasodilation at the onset of exercise. Mongrel dogs ( n = 7) were instrumented with flow probes on both external iliac arteries. Before treadmill exercise at 3 miles/h, 0% grade, hexamethonium (10 mg/kg) and atropine (0.2 mg/kg) or saline was infused intravenously. Ganglionic blockade increased resting heart rate from 87 ± 5 to 145 ± 8 beats/min ( P < 0.01) and reduced mean arterial pressure from 100 ± 4 to 88 ± 5 mmHg ( P < 0.01). During steady-state exercise, heart rate was unaffected by ganglionic blockade (from 145 ± 8 to 152 ± 5 beats/min), whereas mean arterial pressure was reduced (from 115 ± 4 to 72 ± 4 mmHg; P < 0.01). Immediate and rapid increases in iliac blood flow and conductance occurred with initiation of exercise with or without ganglionic blockade. Statistical analyses of hindlimb conductance at 5-s intervals over the first 30 s of exercise revealed a statistically significant difference between the control and ganglionic blockade conditions at 20, 25, and 30 s ( P < 0.01) but not at 5, 10, and 15 s of exercise. Hindlimb conductance at 1 min of exercise was 9.21 ± 0.68 and 11.82 ± 1.32 ml ⋅ min-1 ⋅ mmHg-1for the control and ganglionic blockade conditions, respectively. Because ganglionic blockade did not affect the initial rise in iliac conductance, we concluded that the autonomic nervous system is not essential for the rapid vasodilation in active skeletal muscle at the onset of exercise in dogs. Autonomic control of skeletal muscle blood flow during exercise is manifested through vasoconstriction and not vasodilation.

Effect of rolling resistance on poling forces and metabolic demands of roller skiing

OBJECTIVE To examine the effect of an increase in roller ski rolling resistance on the physiological and upper body demands of roller skiing with the V2-alternate technique. METHODS Nine highly skilled cross-country skiers roller skied at three paced speeds on a flat oval loop using roller skis with high (HiR) and low (LowR) rolling resistance. Oxygen uptake (VO2), heart rate, and poling forces were measured during the last 30 s and rating of perceived exertion (RPE) was requested immediately after each 4-min bout of roller skiing. RESULTS VO2 and all force-related variables increased significantly with speed and were higher (P < 0.01) for HiR at given speeds. Poling time was similar between HiR and LowR, whereas poling recovery time was shorter (P = 0.0002) and cycle rate was higher (P = 0.002) for HiR. For given VO2 levels, peak and average forces, heart rates, and RPE values were similar between HiR and LowR, whereas average poling force across the cycle was greater (P = 0.006) and duty cycle (i.e., percentage of cycle when poling forces were applied) was higher (P = 0.0001) with HiR. CONCLUSIONS 1) The decrease in poling recovery time and increase in cycle rate associated with an increase in roller ski rolling resistance is comparable to the effect previously observed from increasing grade and probably occurs as a means of limiting deceleration. 2) Since changes in rolling resistance do not alter the relationships of RPE and heart rate with VO2, the central cardiovascular adaptations from roller ski training should not be affected by the rolling resistance of the roller skis. 3) Higher resistance roller skis are likely to induce greater upper body aerobic adaptations than lower resistance roller skis.

The effect of aging on adrenergic and nonadrenergic receptor expression and responsiveness in canine skeletal muscle

We tested the hypothesis that adrenergic and nonadrenergic receptor responsiveness and protein expression would be altered with advancing age. Young (n = 6; 22 ± 1 mo; mean ± SE) and old (n = 6; 118 ± 9 mo) beagles were instrumented with flow probes and an indwelling catheter for continuous measurement of external iliac blood flow and arterial blood pressure. Vascular conductance (VC) was calculated as hindlimb blood flow/mean arterial pressure. Selective agonists for α-1, α-2, neuropeptide-Y (NPY), and purinergic (P2X) receptors were infused at rest and during treadmill running at moderate (2.5 mph) and heavy (4 mph with 2.5% grade) exercise intensities. Feed arteries were dissected from gracilis muscles, and α-1D, α-1B, α-2A, P2X-4, P2X-1, and NPY-Y1 receptor protein expression was determined. Phenylephrine produced similar decreases (P > 0.05) in VC in young and old beagles at rest (young: -62 ± 5%; old: -59 ± 5%) and during moderate (young: -67 ± 5%; old: -62 ± 4%) and heavy (young: -54 ± 4%; old: -49 ± 3%) exercise. Clonidine caused similar (P > 0.05) decreases in VC in old compared with young dogs at rest (young: -59 ± 8%; old: -70 ± 6%) and during moderate (young: -52 ± 6%; old: -47 ± 5%)- and heavy (young: -42 ± 5%; old: -43 ± 5%)-intensity exercise. NPY infusion resulted in a similar decline in VC in young and old beagles at rest (young: -40 ± 7%; old: -39 ± 9%) and during moderate (young: -47 ± 6%; old: -40 ± 6%)- and heavy (young: -40 ± 3%; old: -38 ± 4%)-intensity exercise. α-β-Methylene-ATP also produced similar decreases in VC in young and old beagles at rest (young: -36 ± 6%; old: -40 ± 8%) and during exercise at moderate (young: -42 ± 5%; old: -40 ± 9%) and heavy (young: -47 ± 5%; old: -42 ± 8%) intensities. α-1B receptor protein expression was elevated (P < 0.05) in old compared with young dogs, whereas there were no age-related differences in α-1D or α-2A receptor expression and nonadrenergic P2X-4, P2X-1, and NPY-Y1 receptor expression. The present findings indicate that postsynaptic adrenergic and nonadrenergic receptor responsiveness was not altered by advancing age. Moreover, the expression of adrenergic and nonadrenergic receptors in skeletal-muscle feed arteries was largely unaffected by aging.

Frequency and pattern dependence of adrenergic and purinergic vasoconstriction in rat skeletal muscle arteries

Sympathetic nerves fire in bursts followed by brief periods of quiescence. Periods of quiescence may be a valuable part of coding for different neurotransmitters. We compared adrenergic‐ and non‐adrenergic‐mediated vasoconstriction with repeating burst patterns versus constant frequency stimulation. Seventeen rats were killed, and the femoral arteries dissected out and mounted in organ tissue baths at 37°C and pH 7.4. Field stimulation was applied to artery rings from five rats at constant frequencies of 2–6 Hz for 144 impulses. In 12 rats, artery rings were stimulated with two burst pattern protocols consisting of repeating pairs, triplets, quadruplets or sextuplets performed using either 8 or 30 Hz as the instantaneous frequency for a total of 144 impulses. All protocols were repeated with the P2 purinergic antagonist pyridoxal‐phosphate‐6‐azophenyl‐2′4′‐disulphonic acid (PPADs; 0.42 m) or the α1‐antagonist prazosin (1.59 μm). Tension was decreased by the addition of the P2 antagonist PPADs (P < 0.05). Prazosin abolished tension at all constant frequencies (P < 0.05). P2 and α1‐antagonism decreased tension with 8 and 30 Hz burst pattern field stimulation. However, the magnitude of decrease in tension with prazosin was less with burst patterns compared to the same average constant frequencies (P < 0.05). It appears that P2X receptors and α1‐receptors in the femoral artery are sensitive to frequency and patterns of electrical stimulation.

Heart rates of elementary physical education students during the dancing classrooms program.

Abstract We examined how different types of dance activities, along with their duration, influenced heart rate responses among fifth-grade physical education students (N = 96) who participated in the Dancing Classrooms program. Results indicated that the overall Dancing Classrooms program elicits a moderate cardiovascular heart rate response (M = 124.4 bpm), in which 47% of class time was spent above a 60% maximal heart rate threshold. The swing dance in particular (M = 143.4 bpm) stimulated a much higher heart rate level than all other dances in the program, with a mean heart rate change of 52.6 bpm. Girls (127.3 bpm) achieved marginally higher heart rates (p = .059) than boys (121.1 bpm).