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1 Departments of Health and Kinesiology and Medical Physiology, Texas A&M University, College Station, Texas 77843; 2 Department of Surgery, Allegheny University of the Health Sciences, Pittsburgh Campus, Pittsburgh, Pennsylvania 15212; and 3 Departments of Medicine and Cellular and Molecular Physiology, The Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033
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ABSTRACT |
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 Top
 Abstract
 Introduction
Methods
Results
Discussion
References
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During
eccentrically biased exercise (e.g., downhill locomotion), whole body
oxygen consumption and blood lactate concentrations are lower than
during level locomotion. These general systemic measurements indicate
that muscle metabolism is lower during downhill exercise. This study
was designed to test the hypothesis that hindlimb muscle blood flow is
correspondingly lower during downhill vs. level exercise. Muscle blood
flow (determined by using radioactive microspheres) was measured in
rats after 15 min of treadmill exercise at 15 m/min on the level (L,
0°) or downhill (D, 
17°). Blood flow to ankle extensor
muscles was either lower (e.g., white gastrocnemius muscle: D, 9 ± 2; L, 15 ± 1 ml · min
1 · 100 g1) or not different
(e.g., soleus muscle: D, 250 ± 35; L, 230 ± 21 ml · min1 · 100 g1) in downhill vs. level
exercise. In contrast, blood flow to ankle flexor muscles was higher
(e.g., extensor digitorum longus muscle: D, 53 ± 5; L, 31 ± 6 ml · min1 · 100 g1) during downhill vs.
level exercise. When individual extensor and flexor muscle flows were
summed, total flow to the leg was lower during downhill exercise (D,
3.24 ± 0.08; L, 3.47 ± 0.05 ml/min). These data indicate that
muscle blood flow and metabolism are lower during eccentrically biased
exercise but are not uniformly reduced in all active muscles; i.e.,
flows are equivalent in several ankle extensor muscles and higher in
ankle flexor muscles.
concentric contraction; eccentric contraction; muscle temperature
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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DURING DOWNHILL LOCOMOTION IN RATS (1, 3), as in humans
(17, 18), whole body oxygen consumption
(
O2) and blood lactate
concentrations are lower than during level locomotion at the same
speed. These general systemic measurements indicate that muscle
metabolism is lower during eccentrically biased exercise. Indeed,
eccentric muscle contractions have been shown to be metabolically less
demanding (4, 5) and to require activation of fewer motor units than
did concentric contractions to perform equivalent levels of work (4).
The effect of a lower metabolism during downhill exercise on muscle perfusion would predictably be a lowering of blood flow as a result of diminished release of vasoactive metabolites (11, 15). However, there are other vascular control mechanisms involved in the regulation of skeletal muscle hyperemia that could be differentially affected by eccentrically biased exercise, such as sympathetic nerve activity and the mechanical effects of the muscle pump (9, 13, 15). For example, it is possible that the efficacy of the muscle pump to elevate blood flow during lengthening muscular contractions is dissimilar to that during concentrically biased exercise. Therefore, the purpose of the present study was to determine whether steady-state perfusion of individual muscles is different during eccentric and concentric contraction-biased exercise. We hypothesized that muscle blood flow would be lower during eccentrically biased locomotion.
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Animals and Animal Care
Male Sprague-Dawley rats (Charles River) weighing 399-564 g were used in these studies. They were housed in an environmentally controlled room maintained at 23 ± 2°C and were given food (commercial rat chow) and water ad libitum. In study I, muscle blood flows were measured during level or downhill treadmill exercise, and in study II, soleus and tibialis anterior muscle temperatures were measured during level and downhill walking.Surgical Procedures
Study I: Blood flow. Each rat had a catheter (Dow Corning, Silastic: ID 0.6 mm, OD 1.0 mm) filled with heparinized (200 U/ml) saline implanted in the ascending aorta via the right carotid artery while under methoxyflurane anesthesia (Metofane), as previously described (14). This catheter was subsequently used for radiolabeled microsphere infusions to measure tissue blood flow and to record arterial pressure. A second polyurethane catheter (Braintree Science, Micro-renathane: ID 0.36 mm, OD 0.84 mm) for withdrawal of reference blood samples was implanted in the caudal artery of the tail and filled with heparinized saline as previously described (7).Study II: Muscle temperature. Two groups of rats were used to study muscle temperature responses to level and downhill exercise. The rats in one group had a 1-cm vertical cutaneous incision made along the lower lateral aspect of one leg while they were under methoxyflurane anesthesia. The lateral head of gastrocnemius muscle was slightly retracted to expose soleus muscle. An 18-gauge needle was inserted ~0.7 cm into the belly and down the length of soleus muscle. A tissue-implantable thermocouple microprobe (Yellow Springs Instruments series 500, model 511) was inserted through the needle and into the muscle; the needle was withdrawn with the probe in place in the muscle. The rats in the second group had a 1-cm vertical cutaneous incision made along the proximal aspect of the leg, and an 18-gauge needle was inserted ~0.7 cm into the belly and down the length of tibialis anterior muscle. An implantable thermocouple microprobe (type IT-23, Physitemp Instruments) was inserted through the needle and into the muscle. The temperature probes in both groups of rats were secured with 2-silk (4-0) sutures in cutaneous and connective tissue, and the probe locations in soleus and tibialis anterior muscles were later confirmed postmortem.
Experimental Protocols
Study I: Blood flow. Each rat was placed on a motor-driven treadmill (Stanhope Scientific), and the first microsphere label was infused while the animal stood either on a 0° incline (n = 7) or on a17°
incline (n = 9). The rat was then
walked at 15 m/min on the level or down the incline, and blood flows
were measured with microspheres at 15 min of walking. After the blood
flow measurements, pentobarbital sodium (35 mg/kg) was infused through
the carotid catheter, and the animals were euthanized by
exsanguination. Muscle and visceral tissues were excised, weighed, and
placed in counting vials for blood flow determination.
Study II: Muscle temperatures. Rats in these studies were placed on a level or downhill (17°) treadmill, and soleus (n = 6) or tibialis anterior (n = 6) muscle temperatures were measured during standing. The animals then walked either on the level or downhill at 15 m/min for 30 min while temperature was continuously monitored. The rats were returned to their cages, and after 60 min were again exercised at the same speed and for the same time but in the other treadmill position. Three rats from each group walked on the level treadmill first, and three in the inclined position first. In all cases, muscle temperature had returned to the preexercise level before the commencement of the second exercise bout.
Blood Flow Measurements
In study I, radiolabeled (46Sc, 85Sr, 113Sn, or 153Gd) microspheres (New England Nuclear), 15 µm in diameter, were used for blood flow measurements as previously described (14). Microspheres were suspended before infusion by 10 min of sonication followed by 1 min of agitation on a vortex mixer. After dissection, tissue samples were counted in a gamma counter (Packard Auto-Gamma 5780), and flows were computed (IBM PC computer) from counts per minute and tissue wet weights. Microsphere mixing with the blood was assessed by comparing bilateral kidney flows. Mixing was considered adequate if bilateral flows were within 15%.Arterial Pressure and Heart Rate Measurements
In study I, mean arterial pressure and heart rate were estimated from electronically averaged recordings and pulsatile arterial tracings, respectively, from the carotid catheter under each experimental condition. Measurements were made with a pressure transducer (Electromedical) and were recorded on a polygraph (Gould 2800). Recordings were made immediately before and after the microsphere infusions for blood flow measurements and were averaged. Simultaneous measurements were not possible because the same catheter was used for both the arterial pressure recordings and microsphere infusions.Statistical Analysis
For study I, mean arterial pressure, heart rate, and tissue blood flow were compared by using a one-between (downhill vs. level) and one-within (preexercise and 15-min exercise) repeated-measures ANOVA. In study II, soleus or tibialis anterior muscle temperatures in the level and downhill conditions were compared by using a two-within repeated-measures ANOVA for condition (downhill vs. level) and time. If a significant interaction was present, simple effects tests were used to determine the significance of differences between level and downhill means during exercise, and simple comparisons were used to compare preexercise and exercise means. For all analyses, the P < 0.05 level was used to indicate statistical significance.| |
RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Heart Rate and Arterial Pressure
There were no differences in preexercise heart rates or mean arterial pressures between the two groups, and there was no difference in mean arterial pressure during exercise between level and downhill walkers (Table 1). Heart rate, however, was higher during concentrically biased exercise than during eccentrically biased exercise.
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Blood Flow
Blood flow patterns for the hindlimb skeletal muscles are presented in Table 2. At rest, there were no differences in muscle blood flow between animals standing on a level treadmill surface and rats standing on a downhill incline. After 15 min of exercise, blood flow was higher than that at rest in all muscles, except the white portion of the gastrocnemius muscle during downhill locomotion. In several of the ankle extensor muscles (middle and white portions of gastrocnemius), blood flow was higher during level than during downhill exercise. Conversely, in the ankle flexor muscles (tibialis anterior and extensor digitorum longus), perfusion was higher during downhill walking. When muscle blood flow was expressed in milliliters per minute and flow to the leg extensor and flexor muscles was summed, total flow to the leg muscles was lower during downhill than during level exercise (Fig. 1).
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During preexercise, visceral blood flows were the same in the level and
downhill groups (Table 3). However, during exercise, blood flow decreased to the spleen and stomach during concentrically biased exercise but remained unchanged during eccentrically biased exercise.
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Muscle Temperature
The increases in soleus muscle temperature from preexercise (37.2 ± 0.2°C, level standing; 37.3 ± 0.2°C, downhill standing) to steady-state exercise was similar during level and downhill treadmill walking (Fig. 2). Temperature increased and stabilized by 5 min of exercise in both groups and remained constant for the remainder of a 30-min exercise bout. Mean temperature after 15 min of level walking was 39.5 ± 0.4°C (range 38.8-40.8°C), and during downhill walking it was 39.4 ± 0.3°C (range 38.5-40.7°C). Tibialis anterior muscle temperature increased from standing (35.5 ± 0.1°C, level; 35.7 ± 0.2°C, downhill) to 5 min of exercise and continued to increase above that at 5 min of exercise in both groups (Fig. 3). Temperature remained constant from 10 to 30 min of exercise. Mean tibialis anterior muscle temperature during 15 min of level walking was 36.2 ± 0.1°C (range 35.7-36.7°C), and during downhill walking it was 36.7 ± 0.1°C (range 36.2-37.0°C).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The purpose of the present study was to determine whether steady-state perfusion of individual muscles is different during eccentrically and concentrically biased exercise. More specifically, we sought to test the hypothesis that muscle blood flow during downhill locomotion is lower than that during level locomotion at the same speed. The data indicate that total flow to the musculature is lower during downhill exercise (Fig. 1). However, the hyperemic responses of individual muscles do not uniformly follow this single pattern but show three distinctly different patterns.
The first pattern of individual muscle flow corresponds to that of
total leg flow (Fig. 1); i.e., flow is lower during eccentric contraction-biased exercise. Because of the close correlation between
muscle metabolism and muscle perfusion (9, 11, 13, 15), the lower blood
flow in the middle and white portions of the gastrocnemius muscle
during downhill locomotion is consistent with the observations that
muscle metabolism is lower during eccentric contractions (4, 5). It
should also be noted that of the eight muscles or muscle parts studied
the middle and white portions of gastrocnemius muscle have the highest
composition of type IIB fibers (2, 8). Because the rat musculature is
predominantly (71%) composed of type IIB fibers (2, 8), it appears
that the lower whole body O2
and blood lactate concentrations during downhill exercise (1, 3, 17,
18) correspond to the lower blood flow in muscle having this fiber
composition. Alternatively, the middle and white portions of
gastrocnemius muscle make up ~53% of the total mass of the rat leg
muscles studied (8). Thus the lower whole body
O2 may correspond to the flow
pattern occurring in the largest mass of muscle.
The lower leg muscle blood flow during eccentrically biased exercise
may also reflect a lower cardiac output. Although cardiac output was
not measured, the lower heart rate (present study) and whole body
O2 (1, 3) indicate that the
exercise-induced elevation in cardiac output is less during downhill locomotion.
A second blood flow pattern emerged in ankle extensor soleus,
plantaris, and the red portion of gastrocnemius muscles, where perfusion was not different between eccentric- and concentric-biased contractions. Unlike what would be predicted from differences in whole
body O2 and blood lactate
concentrations, this blood flow pattern suggests that the metabolic
rate of these muscles is not different during downhill and level
exercise. Alternatively, it is possible that other control mechanisms
regulating muscle blood flow and vascular tone are modified by
eccentric contraction-biased exercise so that muscle metabolism and
perfusion are not precisely matched. For example, it is possible that
the efficacy of the muscle pump to elevate muscle blood flow is
enhanced during lengthening contractions or that a lower muscle
sympathetic nerve activity during eccentrically biased exercise might
offset a lower muscle metabolism so that perfusion is maintained at the
same level as that during concentrically biased exercise. Therefore, we
sought to test the first possibility that metabolic rate is equivalent in muscle exhibiting no difference in blood flow during downhill and
level exercise. To estimate muscle metabolism, we measured soleus
muscle temperature during downhill and level exercise, since
intramuscular temperature is the resulting difference between heat
production (mainly the result of metabolic rate) and heat elimination
(mainly the result of muscle perfusion). The similarity in soleus
muscle perfusion and temperature (Fig. 2) during downhill and level
exercise suggests a similar metabolism. This is in agreement with the
observations of Armstrong and Taylor (3), who reported that soleus,
plantaris, and the red portion of gastrocnemius muscle glycogen
concentrations as well as the muscle cross-sectional area showing
glycogen loss were similar after level and downhill locomotion. Thus
these data indicate that the metabolic rate is equivalent in some
muscles during eccentric and concentric contraction-biased exercise,
despite the existence of differences in whole body
O2 and blood
lactate concentrations. In addition, the elevations in soleus muscle
temperature during exercise are similar to the changes in colonic
temperature in rats performing level treadmill walking at the same
speed (10), suggesting that heat is effectively removed from
well-perfused active muscle during low-intensity exercise.
Whereas the first two patterns of exercise hyperemia occurred in ankle extensor muscles, the third pattern occurred in both ankle flexor muscles studied. This pattern is characterized by a higher muscle blood flow during downhill locomotion, although it should be noted that even during downhill locomotion these flexor muscles are performing concentric contractions. There are several possibilities for the elevations in blood flow in these muscles during downhill locomotion. One possibility is a lower sympathetic nerve activity to muscle. In support of this notion, there were a lower heart rate (Table 1) and higher blood flow to the spleen and stomach (Table 3) during eccentric exercise, indicating that the sympathetic outflow is lower. In addition, we have demonstrated a lower muscle sympathetic nerve activity in humans during nonfatiguing bouts of eccentric arm curls compared with concentric arm curls (6). The effect of a lower muscle sympathetic nerve activity would predictably be a diminished vasoconstrictor tone and, correspondingly, a higher muscle perfusion. Indeed, acute hindlimb sympathectomy of rats walking on the treadmill at the same speed results in a higher blood flow to ankle flexor muscles (16). However, we are skeptical that the higher perfusion rate of ankle flexor muscles during downhill locomotion results from a lower sympathetic nerve activity. Previous work has shown that sympathetic adrenergic control of blood flow is most predominant in muscle composed primarily of fast-twitch type IIB fibers (7, 12, 19). If a lower muscle sympathetic nerve activity was mediating the higher blood flow in the flexor muscles, we would also expect to see higher flows to the middle and white portions of gastrocnemius muscle, which have the highest composition of type IIB fibers (2, 8). For example, a lowering of muscle sympathetic nerve activity via acute hindlimb sympathectomy not only elevated perfusion of ankle flexor muscles during exercise but also increased blood flow to the white portion of gastrocnemius muscle (16). Thus these observations are inconsistent with a decrease in muscle sympathetic nerve activity being the primary mediator of the higher flexor muscle blood flow during downhill exercise.
A second possibility for the higher blood flow to ankle flexor muscles during downhill locomotion is a higher metabolic rate. To estimate flexor muscle metabolism, we measured tibialis anterior muscle temperature during downhill and level exercise (Fig. 3). After 10 min of exercise, tibialis anterior muscle temperature was significantly higher during downhill walking. The higher temperature, coupled with the greater perfusion, indicates that ankle flexor muscle metabolism is greater during eccentrically biased exercise. The higher rates of metabolism suggest greater muscle work or decreased efficiency. Regarding the latter, it is not unreasonable to assume that the muscles are not operating at the optimal muscle length during downhill walking, which could require increased activation of the muscle to produce the required shortening velocities.
In conclusion, the present study demonstrates differential effects of eccentrically biased exercise on tissue perfusion. Skeletal muscle blood flow is lower or the same in ankle extensor muscles and is higher in ankle flexor muscles during eccentric exercise. These patterns of flow appear to correspond primarily to muscle metabolic rate. Furthermore, the lower heart rate and greater perfusion of splanchnic tissue during downhill exercise indicate that sympathetic outflow is lower during eccentric contractions.
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ACKNOWLEDGEMENTS |
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This research was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases Grants AR-37098 (M. D. Delp and AR-44571 (C. A. Ray) and by the National Aeronautics and Space Administration Grants NAGW-4842 and NAG5-3754 (M. D. Delp).
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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: M. D. Delp, Dept. of Health and Kinesiology Texas A&M University, College Station, TX 77843 (E-mail: mdd{at}hlkn.tamu.edu).
Received 6 March 1998; accepted in final form 7 October 1998.
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REFERENCES |
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Introduction
Methods
Results
Discussion
References
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) and downhill
(
) exercise. Values are means ± SE.
