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00005768-200211000-0000700005768_2002_34_1733_crowther_measurements_11article< 96_0_16_6 >Medicine & Science in Sports & Exercise© 2002 Lippincott Williams & Wilkins, Inc.Volume 34(11)November 2002pp 1733-1737Fiber recruitment affects oxidative recovery measurements of human muscle in vivo[BASIC SCIENCES: Original Investigations]CROWTHER, GREGORY J.; GRONKA, RODNEY K.Departments of Physiology & Biophysics and Radiology, University of Washington, Seattle, WASubmitted for publication December 2001.Accepted for publication July 2002.Address for correspondence: Gregory J. Crowther, University of Puget Sound, Department of Biology, 1500 N. Warner Street #1088, Tacoma, WA 98416; E-mail: gcrowther@ups.edu.We thank S. A. Jubrias and E. G. Shankland for technical assistance and K. E. Conley, M. J. Kushmerick, M. J. Lambeth, D. J. Marcinek, and an anonymous reviewer for useful advice.This work was supported in part by NIH grants AR42928 and AR45184.AbstractCROWTHER, G. J., and R. K. GRONKA. Fiber recruitment affects oxidative recovery measurements of human muscle in vivo. Med. Sci. Sports Exerc., Vol. 34, No. 11, pp. 1733–1737, 2002.Purpose: Fast-twitch and slow-twitch muscle fibers are known to have distinct metabolic properties. However, it has not been clearly established whether such heterogeneity within mixed-fiber muscles can influence measurements of energy metabolism in vivo. We therefore tested the hypothesis that differences in muscle fiber recruitment can cause differences in whole-muscle oxidative recovery from exercise.Methods: We used 31P magnetic resonance spectroscopy to measure oxidative ATP synthesis in the ankle dorsiflexor muscles of eight healthy volunteers under a variety of recruitment conditions. Oxidative ATP synthesis after isometric exercise was quantified as the rate constant kPCr, the reciprocal of the time constant of PCr recovery.Results: kPCr was 37% higher after low-force ramp contractions (which primarily recruit slow-twitch fibers) than after ballistic contractions to the same peak force (which recruit both fast- and slow-twitch fibers). kPCr was also 24% higher after low-force ramp contractions than after high-force ramp contractions, presumably reflecting the recruitment of fast-twitch fibers at high forces.Conclusion: Our results indicate that the muscle fibers recruited first in voluntary contractions have a higher oxidative capacity than those recruited last. Such metabolic differences among fibers can confound whole-muscle measurements and thus need to be taken into account when studying voluntary exercise.Slow-twitch muscle fibers have lower force-specific contractile costs, lower glycolytic capacities, and higher oxidative capacities than fast-twitch muscle fibers, according to histochemical and in vitro data (3,11,25). However, it has not been clearly established whether such heterogeneity within mixed-fiber muscles can influence whole-muscle measurements of energy metabolism in vivo.In progressive exercise tests of isolated human muscle groups, numerous studies have identified a workload threshold above which the slopes of PCr breakdown and H+ production versus workload increase (14,16,17,26,30). Recruitment of the less oxidative, more glycolytic fast-twitch fibers at the higher workloads has been invoked as a possible explanation for this threshold (14,16). However, recruitment-independent explanations relating to blood flow, the oxidation of lipids, and the overall oxidative capacity of the muscle have also been offered (14,16,17). Thus, the impact (if any) of fiber heterogeneity on whole-muscle energetic measurements remains uncertain.One key energetic trait of skeletal muscles is their oxidative capacity—the maximum rate at which their mitochondria can synthesize ATP via oxidative phosphorylation. A muscle’s oxidative capacity is linearly related to its kPCr, a rate constant describing the oxidative resynthesis of phosphocreatine (PCr) after exercise (5,23). kPCr represents the recovery rate of the muscle fibers that were active during exercise; therefore, recruitment of different populations of fibers during different types of exercise could lead to different recovery rates after exercise and thus different estimates of kPCr. For instance, because slow-twitch muscle fibers generally contain more mitochondria than fast-twitch fibers, the kPCr of a muscle containing both fast- and slow-twitch fibers should be highest after an exercise bout in which only the slow-twitch fibers are used.The goal of this study was to determine whether variations in muscle fiber recruitment affect energetics measurements of human skeletal muscle in vivo. To vary recruitment, we varied the speed and peak force of the voluntary isometric muscle contractions performed by our experimental subjects. “Ballistic” contractions, in which the peak force is attained as rapidly as possible, generally recruit all muscle fibers at relatively low forces (20–30% of maximal voluntary contraction [MVC] force). In contrast, slow “ramp” contractions generally do not achieve complete recruitment unless the peak force is >60–80% of MVC force (9,10). We therefore asked two questions. First, is kPCr higher after low-force ramp contractions, which primarily recruit slow-twitch fibers, than after low-force ballistic contractions, which recruit both fast- and slow-twitch fibers? Second, is kPCr higher after low-force ramp contractions, which recruit slow-twitch fibers, than after high-force ramp contractions, which recruit both types of fibers?We chose to study the human ankle dorsiflexors because the tibialis anterior, the largest muscle in this muscle group, is known to contain a mixture of fast- and slow-twitch fibers (11) whose recruitment depends upon contraction speed and peak force, as described above (10).METHODSSubjects.Eight adults (six men and two women) aged 24–62 were recruited from a population of normal volunteers. The experimental protocols were approved by the Institutional Review Board of the University of Washington, and voluntary, written informed consent was obtained from each subject.Experimental setup, data acquisition, and analysis of spectra.The magnetic resonance (MR) methods employed here were identical to those of an earlier study (7). In brief, each subject lay supine in the bore of a 1.5-T magnet while the right leg and foot were held in place with a plastic holder to which a strain gauge was attached. The strain gauge measured the force exerted by the ankle dorsiflexor muscles and was linked to a computer running LabView data acquisition software (National Instruments, Austin, TX). A surface coil was used to collect 31P MR spectra of the dorsiflexors as previously reported (6). Spectra acquired with 6-s time resolution typically had a signal-to-noise ratio of 90:1 for the PCr peak after line broadening. PCr peak areas were converted into absolute concentrations based upon the PCr/ATP ratio of a fully relaxed spectrum and assuming the muscle [ATP] to be 8.2 mM (13). The chemical shift of the Pi peak relative to PCr was used to calculate muscle pH (27).Experimental protocol.Subjects completed several experimental trials in randomized order. Each trial consisted of the four steps described below. Ischemia was employed in steps A–C so that aerobic recovery from exercise (step D) could be delayed for 60 s beyond the end of exercise. Oxidative ATP synthesis was measured after 60 s of postexercise ischemia to ensure that this measurement was not contaminated by glycolytic ATP synthesis, because glycolytic flux remains high for the first 10 s after exercise but declines to basal levels within 20–30 s (8).Ischemic rest (300 s).Circulation to the ankle dorsiflexors was stopped by inflating a pressure cuff around the thigh to a pressure 40 mm Hg above the subject’s systolic blood pressure. PCr breakdown during this step was minimal (∼1 mM on average).Ischemic exercise (variable duration).Subjects exercised their ankle dorsiflexor muscles by performing voluntary isometric dorsiflexions against the resistance of the plastic foot holder. These contractions were done with either a ballistic time course or a ramp time course, depending on the trial. A ballistic contraction consisted of reaching the target force as quickly as possible and then relaxing immediately, whereas a ramp contraction consisted of gradually “ramping up” to the target force over 2 s and then resting for 2 s (Fig. 1). Subjects used a metronome to maintain the desired contraction frequency (1 Hz for ballistic contractions, 0.25 Hz for ramp contractions) and used visual feedback from a light-emitting diode (LED) display to achieve the desired peak force (∼20% or 80% of MVC force) with each contraction. FIGURE 1— Four-second samples of force records for ramp and ballistic muscle contractions.Postexercise ischemia (60 s).The subject’s leg was kept ischemic for 60 s beyond the end of exercise to allow glycolytic ATP production to fall to basal levels (8). [PCr] and pH measurements at the end of this period, just before the pressure cuff was deflated, are reported in Tables 1 and 2.TABLE 1. Low-force ramp and ballistic exercise data.Values given are means ± SEM for 5 subjects. Asterisks denote significant differences between ramp and ballistic trials. PCr and pH values “after ischemic exercise” represent measurements taken just before the ischemic pressure cuff was deflated.TABLE 2. Low-force and high-force ramp exercise data.Values given are means ± SEM for 8 subjects. Asterisks denote significant differences between low-force ramp and high-force ramp trials. Aerobic recovery (360 s).Oxidative ATP production by the mitochondria restores muscle [PCr] to resting levels during aerobic recovery from exercise (1). To quantify the kinetics of this process, each subject’s PCr recovery data were fit with a monoexponential function (20). The reciprocal of the time constant of this function was taken to be kPCr, the oxidative recovery rate constant (5,23,29), as shown in Figure 2. FIGURE 2— An example of calculating kPCr. PCr recovery data were fit with a monoexponential function whose time constant, tau, was 39.7 s in this example. kPCr is the reciprocal of tau.Statistics.Values reported are means ± SEM. Differences between means were tested for statistical significance with two-tailed paired t-tests. P-values below 0.05 were considered significant.RESULTSResting [PCr] was 33.7 ± 0.7 mM for the 8 subjects studied, whereas resting pH was 7.01 ± 0.01.Ramp vs ballistic contractions.Five subjects participated in the first part of this study, in which low-force ramp contractions were compared to low-force ballistic contractions. Subjects achieved approximately the same peak forces during the ballistic and ramp trials (Table 1), whereas force-time integrals were significantly larger for the ramp contractions (Table 1) due to the prolonged time course of these contractions (Fig. 1). Kinetic analysis of PCr recovery data (Fig. 3A) revealed that kPCr was 37% higher after ramp exercise than after ballistic exercise (Fig. 3B). FIGURE 3— PCr recovery after ballistic exercise and ramp exercise. [PCr] gradually returned to resting levels after the ischemic cuff was deflated at time 0 (A), and these recovery data were used to calculate kPCr (B). Data shown are means ± SEM for five subjects. Asterisks here and in Figure 4 indicate significant differences.FIGURE 4— PCr recovery after low-force ramp exercise and high-force ramp exercise. Data are presented as in Figure 3 except that the data shown are means ± SEM for eight subjects. For most points in (A), error bars are contained within the width of the symbols.Low-force ramp vs high-force ramp contractions.Upon completion of the ramp-ballistic comparison, a comparison of low-force ramp contractions and high-force ramp contractions was conducted. For this comparison, new experiments were performed on eight subjects: the five subjects studied previously plus three additional subjects.As expected, peak forces and force-time integrals were much higher in the high-force ramp trials than in the low-force ramp trials (Table 2). Kinetic analysis of PCr recovery data (Fig. 4A) revealed that kPCr was 24% higher after low-force ramp exercise than after high-force ramp exercise (Fig. 4B). DISCUSSIONFast- and slow-twitch muscle fibers have distinct energetic properties. For this reason, Meyer and Foley (21) note, “Muscle heterogeneity is a major limitation shared by both NMR and chemical assay... Variations in recruitment and fatigue rates among the fibers [complicate] the interpretation of data acquired during voluntary exercise in humans.” Although this concern certainly seems reasonable, it has yet to be justified by an empirical demonstration that variations in recruitment actually do influence whole-muscle energetics measurements in vivo.The present study examined the influence of recruitment on energetics measurements by comparing measurements made under different recruitment conditions. Desmedt and Godaux (10) have shown that isometric ballistic contractions to ∼20% of MVC force recruit nearly all the muscle fibers of the tibialis anterior, whereas isometric ramp contractions do not achieve complete recruitment except at much higher forces. According to Henneman’s “size principle,” the fibers not recruited by low-force ramp contractions are likely to be fast-twitch fibers with low oxidative capacities (2). Therefore, we predicted that oxidative PCr recovery would be rapid after low-force ramp contractions (which primarily recruit highly oxidative slow-twitch fibers) and less rapid after ballistic or high-force contractions (which recruit both fast- and slow-twitch fibers). This, in fact, is what we found. The oxidative recovery rate constant kPCr was significantly higher for low-force ramp contractions than for either ballistic or high-force ramp contractions. This result supports the idea that the muscle fibers recruited first in voluntary contractions have a higher oxidative capacity than those recruited last. Furthermore, it confirms that variations in recruitment can impact energetics measurements of intact mixed-fiber muscles.kPCr was used as an index of oxidative recovery because it appears to be independent of end-exercise [PCr] and pH within the ranges of PCr depletion (25–50%) and pH (6.9–7.05) encountered in the present study (15,19,20,28). It should be noted that kPCr does decrease under conditions of very low pH (12,29) and that there was a tendency for pH to be lower after exercise involving both fast- and slow-twitch fibers as compared with exercise involving only slow-twitch fibers (Tables 1 and 2). However, in the absence of clear evidence that small differences between near-neutral pH values can affect kPCr, we attribute the observed inter-trial differences in kPCr to differences in muscle fiber recruitment rather than to differences in end-exercise [PCr] or pH.We cannot rule out the possibility that the observed differences in kPCr were due to differences in oxygen delivery to the recruited muscle fibers rather than differences in the oxidative capacities of the fibers. According to this scenario, postischemia perfusion of the recruited fibers would be less adequate after exercise in which all fibers were recruited. We do not know of a plausible mechanism by which this would occur. Nevertheless, this possibility, in which differences in recruitment would lead to differences in blood flow and thus differences in kPCr, is consistent with our overall conclusion that variations in recruitment can influence whole-muscle energetics measurements.The focus of this study was kPCr, an indicator of oxidative capacity. Oxidative capacity is only one of several properties that differ between fast- and slow-twitch fibers; others include force-specific contractile costs and glycolytic capacities. However, our inter-trial differences in cost and glycolysis (data not shown) cannot be unambiguously attributed to differences in muscle fiber recruitment because measurements of these traits are also affected by the timing of muscle activation and relaxation, which also varied between trials. For example, under conditions of complete recruitment, cost per force-time integral and glycolytic flux per force-time integral are higher for brief intermittent contractions resembling ballistic contractions than for prolonged continuous contractions similar to ramp contractions (4,22,24). On the other hand, estimates of kPCr should be independent of such influences and thus provide clearer evidence of energetic differences among exercising human muscle fibers in vivo.We conclude that muscle fiber recruitment can influence whole-muscle energetics measurements, potentially complicating the interpretation of such measurements. In light of this, we suggest that, when quantifying fluxes through intracellular pathways, one should minimize the confounding effects of recruitment by ensuring complete recruitment of all muscle fibers. 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