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Departments of Anatomy, Physiology and Kinesiology, Kansas State University, Manhattan, Kansas 66506-5802
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Muscle contractions evoke an immediate rise in blood flow. Distribution of this hyperemia within the capillary bed may be deterministic for muscle O2 diffusing capacity and remains unresolved. We developed the exteriorized rat (n = 4) spinotrapezius muscle for evaluation of capillary hemodynamics before (rest), during, and immediately after (post) a bout of twitch contractions to resolve (second-by-second) alterations in red blood cell velocity (VRBC) and flux (fRBC). Contractions increased (all P < 0.05) capillary VRBC (rest: 270 ± 62 µm/s; post: 428 ± 47 µm/s), fRBC (rest: 22.4 ± 5.5 cells/s; post: 44.3 ± 5.5 cells/s), and hematocrit but not the percentage of capillaries supporting continuous RBC flow (rest: 84.0 ± 0.7%; post: 89.5±1.4%; P > 0.05). VRBC peaked within the first one or two contractions, whereas fRBC increased to an initial short plateau (first 12-20 s) followed by a secondary rise to steady state. Hemodynamic temporal profiles were such that capillary hematocrit tended to decrease rather than increase over the first ~15 s of contractions. We conclude that contraction-induced alterations in capillary RBC flux and distribution augment both convective and diffusive mechanisms for blood-myocyte O2 transfer. However, across the first 10-15 s of contractions, the immediate and precipitous rise in VRBC compared with the biphasic and prolonged increase of fRBC may act to lower O2 diffusing capacity by not only reducing capillary transit time but by delaying the increase in the instantaneous RBC-to-capillary surface contact thought crucial for blood-myocyte O2 flux.
red blood cell velocity; red blood cell flux; capillary hematocrit; spinotrapezius muscle; red blood cell spacing
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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SKELETAL MUSCLE BLOOD
FLOW increases rapidly and biphasically at the onset of muscle
contractions. The initial phase of the hyperemia, which may last up to
20 s, is thought to arise from both mechanical (34,
37) and vasodilatory [metabolic (14), conducted
(3), for time course of vasodilation onset see Ref. 41] mechanisms (7, 35), whereas the second
phase (up to 2 min) may reflect regulatory or feedback control
necessary for matching O2 delivery
(
O2)-to-O2 uptake
(
O2) (19). An
immediate rise in leg O2 and concomitant
reduction in O2 extraction (for the first 10-15 s) at
exercise onset is interpreted to mean that bulk blood flow does
not limit the aerobic contribution to ATP production during this
crucial transition period (12). However, at exercise
onset, the distribution of red blood cells (RBC) within the
microcirculation, which is the principal site for O2 and
substrate exchange, is currently unknown.
Intravital microscopy techniques have quantified the increase in capillary RBC velocity (VRBC) after muscle contractions (3, 5, 6, 18, 26). However, both convective and diffusive transport mechanisms are important in O2 exchange. Mathematical modeling (10, 13) suggests that the RBC capillary surface area in contact with the myocyte at any given instant is a key determinant of transcapillary O2 flux. In this regard, Honig et al. (17) reported a substantial recruitment of previously unperfused vessels in response to muscle contractions, whereas others found either a more modest or no increase (e.g., Refs. 5, 18). By accepting that most muscle capillaries support continuous RBC flow at rest (4, 24, 30), perfusion of additional capillaries appears an unlikely mechanism for substantial recruitment of additional capillary surface area with exercise. However, conditions that elevate skeletal muscle blood flow (i.e., electrical and/or metabolic stimulation, vasodilation) do augment capillary hematocrit (Hctcap; Refs. 3, 8, 24, 26), and this will increase the RBC surface area-to-capillary luminal surface area. Accordingly, this will augment muscle O2 diffusing capacity (DmO2) independent of blood flow per se (10, 13).
Skeletal muscle capillary diameter (Dc) is not
altered appreciably with increasing perfusion pressures
(23) possibly due to structural interactions with
surrounding muscle tissue. Thus, as Hctcap increases, mean
RBC spacing must decrease. Federspiel and Sarelius (11)
theorized that from rest to maximal O2 consumption, RBC
spacing would have to narrow from ~4 to 1 cell length to avoid nonuniformities in capillary O2 flux. Federspiel and Popel
(10) extended this by demonstrating that, as adjacent RBCs
neared one another, O2 flow rate per RBC was reduced due to
diffusional interaction; however, total O2 flux per
capillary increased with decreasing RBC spacing due to the increased
RBC number per unit length of the capillary. From this, it may be
surmised that the precise matching of O2
to an elevated metabolic demand is critically dependent on capillary
hemodynamics [VRBC and RBC flux
(fRBC)] and also on RBC distribution
(functional capillary density, Hctcap, and RBC spacing)
within and between vessels.
Thus the purpose of this investigation was to develop an in vivo model for studying, on a second-by-second basis, capillary hemodynamics and microvascular RBC distribution across the transition to a bout of electrically induced contractions to test two general hypotheses: 1) that increased VRBC, due to mechanical factors, i.e., muscle pump, would precede increases in fRBC and that both would increase within the first few contractions; and 2) that contraction-induced hyperemia would result in increased Hctcap (as demonstrated previously) and a more uniform Hctcap distribution within the capillary bed. Furthermore, this increased Hctcap would result in a more homogeneous RBC spacing profile within individual capillaries, thus optimizing the effective capillary surface available for O2 exchange.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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A total of seven female Sprague-Dawley rats were used in this investigation. Successful experiments were performed on four (279 ± 6 g) of the seven rats. Three rats were not used in this investigation because of an inability to maintain the focal plane over the entire 3-min contraction protocol. All procedures and protocols were approved by the Kansas State University Animal Care and Use Committee. Surgical interventions were conducted under general anesthesia (40 mg/kg ip pentobarbital sodium). On completion, rats were euthanized via anesthesia overdose.
Muscle preparation. Initially, the right carotid artery was cannulated (PE-50, intramedic polyethylene tubing, Clay Adams Brand, Sparks, MD) for monitoring mean arterial pressure and heart rate. The spinotrapezius muscle was exteriorized as described previously (30). Particular care was taken to minimize overlying fascial disruption and maintain continuous superfusion (Krebs-Henseleit bicarbonate-buffered solution equilibrated with 95% N2-5% CO2). The spinotrapezius muscle was attached to a thin wire horseshoe at five equidistant locations around the caudal periphery. Stainless steel plate electrodes (2.5-mm radius) were placed on the dorsal spinotrapezius surface proximal to the motor unit and along the caudal periphery, facilitating indirect, whole muscle contractions. The rat was then placed on its side on a circulation-heated (38°C) Lucite platform. The horseshoe surrounding the spinotrapezius muscle was secured to the platform such that, during contraction, the scapula (origin of spinotrapezius) was drawn anteriorly while the caudal region remained in place, thus allowing the capillaries to remain in focus throughout the contraction protocol.
Experimental design. Once the muscle was positioned on the platform, several contractions were induced at a level consistent with a modest increase (i.e., approximately two- to threefold) in bulk blood flow (measured via microspheres; Ref. 2). Next, a microvascular field containing (typically) 6-10 capillaries (midway between arteriolar and venular ends to avoid phenomena related directly to the location along the capillary) in the midcaudal (dorsal surface) region of the muscle was selected, and sarcomere length was set at ~2.7 µm as verified via direct on-screen measurement. Resting data were obtained after a 15-min quiescent period. Thereafter, muscle contractions were elicited (1 Hz, 2-ms duration, ~5 V) for 3 min. Mean arterial pressure was monitored throughout the data acquisition period.
Data acquisition. Microcirculatory images were obtained by using bright-field microscopy (Eclipse E600-FN, Nikon; ×40 objective; numerical aperture = 0.8) and recorded (BR-S822U videocassette recorder, JVC, Elmwood Park, NJ) on super VHS cassettes (30 frames/s) for off-line analysis. Microvascular fields were viewed on a high-resolution color monitor (Trinitron PVM-1954Q, Sony, Ichinoniya, Japan) at a final magnification of ×1,184 (calibrated via stage micrometer; MA285, Meiji Techno, Japan).
Off-line analysis.
For each microvascular field, both structural and hemodynamic data were
acquired independently by two investigators. Neither investigator had
prior knowledge of the other's measurements. If a >10% difference
existed between independent observations, measurements were repeated.
Initially, each microvascular field (i.e., capillaries and myocyte
boundaries) was traced directly from the screen onto acetate paper, and
the proportion of capillaries supporting RBC flow was assessed. For all
capillaries in which hemodynamics were assessed,
Dc was measured (hand-held calipers) at two
sites per capillary before contractions (resting conditions) and within
5 s of the final contraction. Both VRBC and
fRBC were measured within two 5-s periods before
contraction onset and within the first 5 s postcontractions.
Between contractions, hemodynamic assessment was possible in ~15
frames. VRBC was acquired by following the RBC
path length over several frames. fRBC was
measured by counting the number of cells passing an arbitrary point.
VRBC was measured twice over each 5-s period
(before and after contraction) and once between contractions at 2, 4, 6, 8, 10, 12, 15, 18, 21, 24, 27, 30, 40, 50, 60, 75, 90, 105, 120, 135, 150, 165, and 180 s. fRBC was counted
over a 2-s period within each designated 5-s period before and after
contraction and over the entire time that RBC movement could be
assessed between contractions. Furthermore, under quiescent conditions
(i.e., before contraction) and immediately after the contraction
protocol (within the first 5 s), individual RBCs within
capillaries were traced over an ~100-µm length for assessment of
RBC spacing. For each capillary in which hemodynamic data were
gathered, Hctcap was calculated as
Hctcap = (RBC volume × fRBC)/[
× (Dc/2)2 × VRBC], where capillaries were approximated as
circular in cross section and RBC volume was taken to be 61 µm3 (1). In addition, Hctcap was
calculated (verified) from RBC spacing data as (RBC number × RBC
volume)/[ × (Dc/2)2 × capillary length].
Statistical analysis. All data are presented as means ± SE. Data distribution was assessed via the Kilmogorov-Smirnov test for normality. Resting and postcontraction data were tested statistically with the paired Student's t-test. Differences in methods of calculation for Hctcap as well as differences in capillary hemodynamics and hematocrit as a function of time were assessed via a one-way repeated-measures ANOVA. When the F value was significant, the Tukey's post hoc test was used for pairwise comparisons (compared with baseline for capillary hemodynamics). Data were regressed linearly by using least-squares techniques. Coefficient of variation (CV) was calculated as (SD/mean) × 100. A statistical significance level of P < 0.05 was accepted.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Neither mean arterial pressure (rest: 104 ± 6 mmHg; post: 106 ± 6 mmHg) nor heart rate (rest: 279 ± 17 beats/min; post: 280 ± 18 beats/min) differed (both P > 0.05) from rest to the postcontraction period. In addition, mean Dc did not differ between rest and postcontraction (rest: 5.9 ± 0.1 µm; post: 5.9 ± 0.1 µm; P > 0.05).
Rest vs. postcontractions.
The percentage of capillaries supporting continuous RBC flow rose,
although not significantly (P > 0.05), from rest
(84.0 ± 0.7%) to postcontraction (89.5 ± 1.4%). As
expected, contractions evoked a significant increase in both capillary
VRBC (rest: 270 ± 62 µm/s; post:
428 ± 47 µm/s; P < 0.005) and
fRBC (rest: 22.4 ± 5.5 cells/s; post:
44.3 ± 5.5 cells/s; P < 0.005; Fig.
1). The proportional increase in
fRBC was significantly greater
(P < 0.05) than that for VRBC.
As shown in Fig. 2, there was no
correlation between the resting value and the contraction-induced
increase for either VRBC (r = 0.24) or fRBC (r = 0.05).
Comparing mean ± SD data for four microvascular fields, the CV
for intercapillary fRBC values was similar
between rest and postcontraction conditions; however, the CV for
VRBC was significantly greater
(P < 0.05) after contractions compared with rest (Fig.
2).
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Temporal response of capillary VRBC, fRBC,
and Hctcap across the transition.
Figure 6 depicts the mean response for
both VRBC (Fig. 6A) and
fRBC (Fig. 6B) in 20 capillaries (of
the 31 capillaries from the 4 microvascular fields) in which these
hemodynamic data could be obtained over the entire 3-min contraction
bout. Intracapillary VRBC exhibited an
immediate, statistically significant rise (within 2 s) and
remained significantly elevated over the remainder of the 3-min
protocol. (Fig. 6A). The increase in
fRBC at contraction onset demonstrated a modest
increase to a short plateau for the first 12-20 s, followed
thereafter by a secondary rise to steady-state values (Fig.
6B). Given that there was no change in mean
Dc from rest to contraction, alterations in
Hctcap from baseline are based on the proportionality
between the contraction-induced changes in
VRBC and fRBC. Thus the
temporal profiles of both VRBC and fRBC were such that Hctcap was not
elevated and even tended to be reduced (although not statistically
significantly so) for the first 10-15 s after contraction onset
(Fig. 7). However, 18 s after
contraction onset, Hctcap became elevated significantly (P < 0.05) compared with baseline (rest) and
remained so for the duration of the contraction protocol.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This is the first investigation to describe the temporal and spatial distribution of the contraction-induced hyperemia within skeletal muscle capillaries across the rest-contractions transition. Key features of this response from rest to end exercise include 1) significant increases in VRBC, fRBC, and Hctcap and a concomitant reduction in mean RBC spacing, 2) increased capillary VRBC heterogeneity (assessed via CV determination) postcontraction with no change in this measure of heterogeneity for either fRBC or Hctcap, and 3) a rapid and immediate increase in VRBC (half time = ~1 s) at the onset of contractions in contrast to a more gradual increase in fRBC (half time = ~10 s). These findings support the notion that, during muscle contractions, RBC flow and distribution within skeletal muscle microcirculation are altered to augment both convective and diffusive mechanisms for O2 transfer. However, the differential time courses of VRBC and fRBC suggest that muscle O2 diffusion may be compromised in the immediate 10- to 15-s period after the onset of contractions.
Sample size. In the current investigation, we were able to observe one capillary network within the spinotrapezius muscles from 4 rats. Given this modest sample size, we must consider the possibility of introducing sampling error on the basis of spatial heterogeneity. What is remarkable and provides confidence that the capillaries sampled reflect the behavior within the majority of the capillary bed is that our measured fRBC response to contractions was remarkably similar to that seen at the arterial level in intact conscious preparations (e.g., Refs. 12, 35; Fig. 6; see Mechanisms of hyperemia at exercise onset below for further discussion). Thus, although spatial heterogeneity certainly does exist within contracting skeletal muscle, we consider the findings herein to be generally representative of those seen within skeletal muscle and to offer a first "look" at RBC hemodynamics and distribution within the capillaries of skeletal muscle capillaries across the rest-to-contractions transition.
Methodological considerations. In this investigation, the rat spinotrapezius muscle was utilized primarily due to its mixed fiber type, good optical qualities, and accessibility without disruption of nervous or primary blood supplies. As discussed below in Mechanisms of hyperemia at exercise onset, the muscle pump mechanism is thought to be crucial for driving immediate increases in blood flow at contraction onset. Whether this thin, postural muscle produces the intramuscular forces necessary to generate the extremely negative venular pressures thought to occur within the venular system of larger muscles and considered intrinsic to the "muscle pump" hypothesis of exercise hyperemia (e.g., Ref. 34) remains to be determined. However, the possibility does exist that the spinotrapezius muscle pump may not be as important for generating negative venular pressure swings compared with other in situ preparations where there is a defined and substantial muscle belly and thus may not participate as effectively in the immediate hyperemic response. Nevertheless, VRBC was increased within 1-2 s. Moreover, capillary hemodynamics could only be analyzed between contractions, and thus any mechanical impedance to flow during actual contraction will not have been observed. However, the 2-ms contraction period is quite short and allows for visualization of the capillaries throughout the majority of each second. Thus we consider any underestimation of fRBC or VRBC to be minimal.
Use of bipolar electrode techniques for inducing indirect muscle contractions elicits a different fiber recruitment pattern from that in humans performing rhythmic exercise. Specifically, electrical stimulation induces recruitment of all fibers, whereas, during voluntary exercise, recruitment of fibers and specific fiber types is thought to be dependent on exercise intensity and duration. In addition, the 2-ms stimulus duration may be long enough to activate sympathetic nerves supplying the arterioles. However, as shown by Behnke et al. (2), this contraction protocol is consistent with that which evokes a blood flow response (increase) compatible with moderate-intensity exercise, and at no time was blood flow observed to fall, as might be expected from rapid sympathetically mediated vasoconstriction. Although the contraction-induced increase in fRBC displayed a pattern similar to that reported for bulk blood flow (two-phase model as discussed below in Mechanisms of hyperemia at exercise onset; Ref. 35), the time course for this change may be slower. This may be related to an anesthesia-induced blunting of the neural and cardiovascular responses. Specifically, Honig and Frierson (16) reported that arteriolar dilation was reduced postcontraction after local anesthesia. However, as discussed below, the hemodynamic response of the anesthetized rat spinotrapezius preparation is similar to that seen in intact, unanesthetized preparations (12, 35). Thus we believe that the essential features of the response were preserved in the spinotrapezius preparation used herein. In this investigation, >80% of capillaries support RBC flow at rest. With brightfield microscopy, the possibility exists that capillaries that do not contain RBCs may not be observed. However, the purpose of the present investigation was to describe capillary hemodynamics and their implications for O2 transfer across the rest-contraction transient. If there are capillaries that flow but contain only plasma and not RBCs, the capacity of those vessels to deliver O2 will be trivially small. Moreover, our laboratory has published evidence that the techniques used have adequate resolution and clarity for identification of non-RBC-perfused capillaries. Specifically, in rodent disease models in which basal blood flow is reduced [i.e., chronic heart failure (21) and Type 1 diabetes (25)], we have detected an increased proportion (up to 50%) of capillaries that do not support RBC flow.Capillary hemodynamic heterogeneity.
At rest, wide distributions for both second order venular
O2 saturations (43.5 ± 15.6%, range = ~0-80%; Ref. 29) and midcapillary "tissue"
O2 partial pressures (27.8 ± 13.7 Torr, range = <5-75 Torr; Ref. 28) in rat spinotrapezius muscle
suggest significant intramuscular
O2-to-O2
mismatch. This diverse distribution of microcirculatory
O2 (and
O2-to-O2
matching) does not appear to be due to a substantial proportion of
non-RBC-perfused capillaries (22, 24, 30). Thus
differential RBC distribution between capillaries or metabolic
differences based on the heterogeneous fiber type distribution within
the spinotrapezius muscle (36) offer the most likely
explanations. Under quiescent conditions, Hctcap is
substantially less (i.e., 
50%) than systemic values (8, 24,
26), which is thought to be due, in large part, to the Fahreus
effect (31) and the presence of an endothelial glycocalyx
(40). Despite low mean values for Hctcap,
considerable intravessel variation exists (range:
0.05-0.40; Ref. 24). This wide variation in
Hctcap has been interpreted to mean that some structural
component intrinsic to the vessel architecture is important to
determine RBC distribution and hematocrit within the capillary network.
Specifically, greater within-microcirculatory unit Hctcap uniformity would be expected if capillary Hctcap were under
arteriolar control (20, 27, 33).
O2 and also whether RBC flow
heterogeneity within the microcirculation is changed by muscle
contractions (for review, see Ref. 9). For the purposes of
brevity, DISCUSSION will focus only on the relative
dispersion of VRBC, as determined via CV
assessment. Duling and Damon (9) contend that the CV for
both VRBC and fRBC is
unaltered from basal conditions to hyperemic states (induced via
postmicro-occlusion assessment, altered O2 availability,
postcontraction, and pharmacalogical-induced vasodilation). However,
this conclusion conflicts with that of Tyml (38, 39), who
found that the CV for VRBC was reduced
significantly after a contraction protocol in both amphibian
(38) and rat skeletal muscle (39). To our knowledge, the findings herein describe the first attempt to track changes in hemodynamics in the same capillaries from rest throughout a
contraction bout. VRBC heterogeneity within
microvascular fields (as assessed by CV) increased after contractions
(Fig. 2). However, in concert with the findings of Duling and Damon
(9), fRBC (arguably the most
important variable with respect to O2)
as well as Hctcap heterogeneity did not change from rest to
postcontraction. Furthermore, neither fRBC nor
VRBC at rest were good predictiors of the extent
to which flow increased within a given capillary during subsequent
functional hyperemia (Fig. 2).
A different and arguably less rigorous analysis of heterogeneity would
be to assess capillaries independent of microvascular field. Analysis
of the CV for all 31 capillaries (as a group of capillaries rather than
as 4 microvascular fields) suggests that CV may be reduced for both
VRBC (rest, 48.5% vs. post, 36.6%) and
fRBC (rest, 63.0% vs. post, 46.2%) after
contractions. This is in agreement with the findings of Tyml (38,
39) in which paired assessment of individual capillaries before
and after contractions was not performed. As we sought to characterize
O2 within microvascular fields, we
considered that our analysis should be consistent with that concept,
i.e., compare heterogeneity between microvascular fields rather than as
an arbitrary assembly of 31 discrete capillaries.
Mechanisms for hyperemia at exercise onset. As discussed in the introduction, the increase in blood flow at the onset of contractions is thought to occur in two phases. The first phase is characterized by an immediate rise in blood flow attributed largely to the muscle pump-induced mechanical compression of venous vessels and the subsequent negative venular pressures (34). However, evidence also exists for a concurrent vasodilatory mechanism (37) that may possibly be associated with neural, metabolic, endothelium-mediated, and/or myogenic control. At present, none of these putative mechanisms is supported by unequivocal empirical evidence (7). The second phase, which is initiated typically within 15-20 s of contractions, is thought to be related to vasodilatory mechanisms and/or metabolic feedback control. Increases in VRBC and fRBC at the microcirculatory level, as described herein, appear to follow different initial phase 1 responses from one another. In addition, increases in Hctcap thought to arise from arteriolar vasodilation (via the Fahreus effect) do not occur in the first ~10-15 s of contractions, and this suggests an initial lag in vasodilation of a similar time frame (Fig. 7). We argue that information regarding O2 transfer potential is to be found within the distribution of that flux and, further, that this may explain the temporal profile of O2 exchange described across the rest-to-exercise transition in human (12) and rat (2) muscle.
Implications for O2 transfer.
Measurements of leg O2 across the
rest-to-exercise transition demonstrate a delay of 10-15 s in the
increase of O2 followed by a
monoexponential rise to steady-state levels (12). In
concert with the mean intracapillary fRBC
profiles (Figs. 6 and 7), these data suggest that microvascular
O2 content and PO2 may be either unchanged for the first few contractions or even become elevated above
baseline levels before falling as O2
increases. Indeed, across the transition from rest to 1-Hz
contractions, microvascular PO2 (measured via
phosphorescence-quenching techniques) is either unchanged (70% of
instances) or increased slightly (30% of instances) for 15-20 s
before decreasing monoexponentially to its contracting steady state
(2). Ultimately, microvascular PO2
must be determined by the local
O2-to-O2
ratio, which is dependent on the local diffusive and perfusive
O2 conductances (32), where
O2 = O2(1 
is the slope of the O2 dissociation curve
in the physiologically relevant range. Thus %O2
extraction = O2/O2 = 1 O2,
O2 extraction is dependent on the relationship between
DmO2 and O2.
O2 (12) and microvascular
PO2 (2) responses seen at exercise onset. Moreover, these techniques permit the empirical testing of
models of O2 exchange within skeletal muscle in health and also the pathological underpinnings of muscle dysfunction in disease conditions (e.g., in diabetes and heart failure where slowed pulmonary O2 kinetics and impaired arteriolar
vasodilation may limit exercise tolerance). The present findings
support the thesis that functional hyperemia enhances both diffusive
(Hctcap) and conductive (fRBC) mechanisms at the microcirculatory level necessary to support an
increased O2 flux. However, increases of
VRBC and fRBC follow different time courses at the transition from rest to dynamic contractions such that the capacity for O2 exchange may not
increase and actually tends to decrease across the first few seconds of contractions.
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ACKNOWLEDGEMENTS |
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The authors thank John A. Russell for assistance in data analysis and Drs. Thomas J. Barstow and Timothy I. Musch for helpful conversation regarding data interpretation.
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FOOTNOTES |
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This work was supported, in part, by grants from the National Heart, Lung, and Blood Institute (HL-50306) and the American College of Sports Medicine (predoctoral award).
Present address of C. A. Kindig: Department of Medicine, Physiology Division, University of California-San Diego, La Jolla, CA 92093-0623.
Address for reprint requests and other correspondence: D. C. Poole, Dept. of Anatomy and Physiology, 228 Coles Hall, Manhattan, KS 66506-5802 (E-mail: Poole{at}vet.ksu.edu).
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. Section 1734 solely to indicate this fact.
First published February 15, 2002;10.1152/japplphysiol.01222.2001
Received 12 December 2001; accepted in final form 12 February 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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