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1Department of Medical Biophysics, The University of Western Ontario; 2Imaging Division, The Lawson Health Research Institute, and Department of Radiology, St. Joseph's Health Care; and 3School of Kinesiology and 4Department of Physiology and Pharmacology, The University of Western Ontario, London, Ontario, Canada
Submitted 12 October 2006 ; accepted in final form 14 February 2007
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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0.6 W/min) to volitional fatigue (Ramp); 2) Ramp preceded by 6 min of moderate-intensity, constant-load exercise below the intracellular pH threshold (pHT; Mod-Ramp); and 3) Ramp preceded by 6 min of heavy-intensity, constant-load exercise above pHT (Hvy-Ramp); the constant-load and incremental exercise periods were separated by 6 min of rest. 31P-magnetic resonance spectroscopy was used to continuously monitor intracellular pH, phosphocreatine concentration ([PCr]), and inorganic phosphate concentration ([Pi]). No differences in exercise performance or the metabolic response to exercise were observed between Ramp and Mod-Ramp. However, compared with Ramp, a 14% (SD 10) increase (P < 0.01) in peak power output (PPO) was observed in Hvy-Ramp. The improved exercise performance in Hvy-Ramp was accompanied by a delayed (P = 0.01) onset of intracellular acidosis [Hvy-Ramp 60.4% PPO (SD 11.7) vs. Ramp 45.8% PPO (SD 9.4)] and a delayed (P < 0.01) onset of rapid increases in [Pi]/[PCr] [Hvy-Ramp 61.5% PPO (SD 12.0) vs. Ramp 45.1% PPO (SD 9.1)]. In conclusion, prior heavy-intensity exercise delayed the onset of intracellular acidosis and enhanced exercise performance during a subsequent incremental exercise test. phosphorus-31 magnetic resonance spectroscopy; warm-up; phosphocreatine; intracellular pH; plantar flexion
O2) response and an attenuation of the subsequent O2 slow component in subsequent constant-load exercise (2, 4, 6, 10, 20, 23). These altered pulmonary O2 responses have been associated with decreased phosphocreatine (PCr) utilization (23). However, a recent study demonstrating the elimination of the O2 slow component following prior heavy exercise found evidence of increased PCr breakdown and reduced efficiency during subsequent exercise (24). Therefore, despite a general consensus in the literature on prior exercise reducing the O2 slow component and altering the phase II O2 response, the metabolic effects of prior exercise have yet to be elucidated.
A prior bout of heavy-intensity exercise may modulate the metabolic response to a subsequent bout via a number of mechanisms. One commonly proposed candidate is a vasodilation in the active muscle caused by the accumulation of vasoactive metabolites such as H+ (9, 19). This mechanism is proposed to increase blood flow and O2 delivery to exercising muscle, as well as reducing or eliminating regional perfusion heterogeneities that otherwise existed following the onset of heavy exercise (14). Accumulation of H+ is also expected to cause decreased binding affinity of hemoglobin for O2 (i.e., an increased Bohr shift of the hemoglobin-oxygen dissociation curve), resulting in increased O2 availability to the working muscle (9). However, evidence that a metabolic acidosis is not a prerequisite for the altered O2 response following prior exercise can be found in studies demonstrating that prior low- and moderate-intensity exercise that did not cause an elevated blood lactate concentration still resulted in a subsequent reduction of the O2 slow component (17, 18). These studies suggest that accumulation of H+ during prior heavy-intensity exercise does not directly contribute to modulating the O2 response.
In the present study, we studied the effects of an altered intracellular metabolic and acid-base status resulting from a prior bout of exercise on the subsequent metabolic response to incremental exercise. While it has previously been shown that prior heavy-intensity exercise causes a significant reduction in the total exercise-induced PCr concentration ([PCr]) decrement, the metabolic effects of prior exercise on an incremental exercise protocol are unknown. In contrast to constant-load exercise, an incremental exercise protocol begins at a very light intensity and gradually increasing ATP demands. Using whole body cycling exercise it has been previously shown that prior intense exercise results in a steeper O2-power output slope during subsequent incremental exercise only at exercise intensities above the gas exchange threshold (GET) (13). One interpretation of this observation may be that prior exercise does not affect the rate at which oxidative phosphorylation increases during the early stages of subsequent incremental exercise but that prior exercise may increase muscle O2 consumption above the GET. This may suggest that exercise economy at heavy work rates is sensitive to the prior activity of the exercising muscles. However, the effects of a prior bout of exercise on the intracellular metabolic and acid-base response during a subsequent incremental exercise have yet to be clearly identified.
Therefore, we used phosphorus-31 magnetic resonance spectroscopy (31P-MRS) to monitor the muscle metabolic and acid-base status during an incremental plantar-flexion exercise protocol with no prior exercise, prior moderate-intensity exercise, and prior heavy-intensity exercise. Prior moderate-intensity exercise was selected because it did not produce an accumulation of intracellular H+, while prior heavy-intensity exercise allowed comparison to exercise that did generate a significant acidosis. We hypothesized that a rightward shift of the intracellular pH (pHi)- and ([Pi]/[PCr])-power output relationships (where [Pi] is inorganic phosphate concentration) toward higher power outputs would be evident following prior heavy-intensity exercise because an accumulation of H+ would enhance local blood flow and perfusion. In contrast, we hypothesized this effect would not be evident after prior moderate-intensity exercise due to a lack of H+ accumulation. Finally, we expected the favorable metabolic response resulting from prior heavy-intensity exercise to be associated with enhanced exercise performance during the subsequent incremental bout.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Experimental protocol. Subjects were studied on three occasions: 1) progressive plantar-flexion exercise to fatigue (Ramp); 2) Ramp preceded by a bout of moderate-intensity exercise (Mod-Ramp); and 3) Ramp preceded by a bout of heavy-intensity exercise (Hvy-Ramp). The order of these experiments was randomized and separated by at least 72 h. In addition, each subject completed at least one familiarization progressive exercise protocol to ensure proper compliance with the exercise protocol. From the familiarization progressive exercise test(s), the onset of intracellular acidosis (described below) was determined to calculate work loads corresponding to Mod and Hvy.
Subjects reported to the laboratory at least 2 h after a light meal and after abstaining from caffeine-containing foods and beverages. Before the start of exercise, subjects lay supine on a table with the legs positioned in a custom-built magnetic resonance-compatible ankle exercise ergometer (21). The dominant leg of each subject was positioned in the ergometer, foot securely attached to a lever or footplate on the ergometer. The footplate was aligned such that the pivot of the lever centered on the axis of the ankle joint. The subjects remained supine throughout the entire protocol.
The exercise consisted of repeatedly depressing the footplate at a frequency of 0.5 Hz (1-s contraction/1-s relaxation) through a range of motion of 35°. This action raised and lowered a water reservoir, in which the resistance was manipulated by adding known volumes of water for the constant-load prior exercise bouts or by adding water in a constant ramplike fashion by means of a roller pump (Cole-Parmer Instruments, Chicago, IL). A metronome set at 0.5 Hz was used to help subjects maintain the proper contraction frequency. To ensure subjects maintained a consistent range of motion (ROM), the ergometer was interfaced to a computer data-acquisition system allowing a light-emitting diode (LED) to signal and record the start (i.e., 0°) and end (i.e., 35°) of plantar-flexion ROM. Exercise was terminated at volitional fatigue or at the point where subjects were unable to maintain the full ROM as determined by their inability to illuminate the LED at full ROM (i.e., 35° plantar flexion) on three successive contractions.
After a 3-min period during which resting measurements were recorded, subjects began exercise. In Ramp, exercise commenced at the same time that water started to flow continuously into the reservoir at a rate of 1.4 kg/min. Power output was calculated using the known repetition rate (0.5 Hz), the displacement of the suspended reservoir (0.08 m), and the weight of the reservoir plus water added [1.7 kg + (1.4 kg/min x exercise time)] using standard physical relationships. This produced a ramp slope of 0.6 W/min from an initial load of 0.7 W. The actual flow rate of water into the reservoir was calculated as the total volume of water added during the exercise test divided by the time to fatigue.
In Mod-Ramp and Hvy-Ramp, a 3-min period of resting data collection was followed by a 6-min bout of constant-load Mod or Hvy exercise. The power outputs corresponding to Mod and Hvy exercise were calculated for each subject from the familiarization progressive exercise test as follows. Logarithm-transformed intracellular hydrogen ion concentration ([H+]) data (i.e., pHi) were plotted as a function of power output for each subject, and a piecewise linear regression algorithm was applied to these plots for detection of a threshold or onset of rapid increases in intracellular [H+]. The power output corresponding to Mod was taken as the power output midway between the initial load and the load corresponding to the onset of a rapid acidification (i.e., pHT). Similarly, the power output corresponding to Hvy was taken as the power output midway between pHT and the peak power output (PPO) achieved. The actual power outputs employed in Mod and Hvy are summarized in Table 1. Following the completion of 6-min Mod or Hvy constant-load exercise, subjects rested comfortably for 6 min and then performed a ramp exercise protocol identical to that described above.
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Data analyses. Quantification of the 31P-MRS metabolite data was performed in the time (acquisition) domain by fitting each 31P free induction decay to a sum of damped sinusoids, which could be varied in terms of amplitude, phase, delay time, damping constant, and frequency. This method utilized prior knowledge and a nonlinear least squares algorithm to iteratively reduce the difference in error between the actual data and the experimental model. The concentrations of the phosphate compounds, [PCr] and [Pi], were determined from the amplitude of the exponential model function at time equal zero. Final metabolite concentrations were expressed relative to MDP concentration ([MDP]), an external reference standard of known concentration. Normalizing metabolite concentrations to the external standard allowed comparisons between subjects in absolute units and corrected for small changes in signal amplitude due to motion artifacts that may have been caused by the exercising muscle. pHi was calculated from the chemical shift (parts per million) of the Pi peak relative to PCr. ADP concentration [ADP] was calculated by assuming a total creatine concentration of 42 mM and that the creatine kinase reaction was at equilibrium. The equilibrium constant was adjusted for intracellular [H+], which was calculated from pHi.
For the purposes of plotting against time or power output, each spectra or data point was assumed to represent the midpoint of the acquisition time. To facilitate determination of the biphasic parameters of intracellular [H+] and [Pi]/[PCr], a logarithm-linear transformation was used. Thus, for intracellular [H+] data, pHi (pHi = –log[H+]) was plotted as a function of power output for each subject. Similarly, log([Pi]/[PCr]) facilitated detection of biphasic parameters in the [Pi]/[PCr] ratio. Piecewise linear regression analysis was then applied to these plots by use of an algorithm that estimated the slope and intercept parameters of two regression functions and determined an inflection at which the slope of the two lines diverged. An F-test (P < 0.05) was used to evaluate whether a single or multiple regression provided the optimal fit of the data. The location of the estimated inflection point was confirmed by visual inspection, and the estimation algorithm was could be adjusted if necessary to provide a fit that coincided with the best visual representation of the data.
Statistical analysis. Statistical analyses were performed using Sigmastat version 3.1 statistical program for the PC (Systat). The test-retest reliability of the incremental plantar-flexion exercise protocol was analyzed by comparing the familiarization protocol with the Ramp protocol. Pearson correlations, as well the coefficient of variability (CV) and the 95% confidence intervals (CI) of the CV, were calculated for this purpose (12). Differences between Ramp, Mod-Ramp, and Hvy-Ramp were examined with a repeated-measures ANOVA. A significant F-ratio was further analyzed via Student-Newman-Keuls post hoc analysis. In all cases, a P value <0.05 was used to determine the rejection of the null hypothesis. Data are presented as means (SD).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Data from a representative subject showing pHi throughout the entire Ramp, Mod-Ramp, and Hvy-Ramp protocols are presented in Fig. 1. During incremental exercise, pHi displayed a biphasic decline, with an initial slow and a later fast component (see Fig. 3). Piecewise linear regression analysis determined that in every subject, the data were best described by fitting two linear components compared with a single linear fit (P < 0.05). An inflection or transition point between the slow and fast linear components is represented by the pHT. The slope of the pHi-power output relationship was less (P < 0.05) below the pHT than above, with no differences in the rate of rapid pHi decline (above pHT) between conditions (Table 3). The onset of intracellular acidosis (Table 4) occurred at 45.8% PPO (SD 9.4) in Ramp, which was not different than Mod-Ramp [47.5% PPO (SD 15.9), P = 0.70]. However, in Hvy-Ramp, the pHT occurred at a higher power output during exercise [60.4% PPO (SD 11.7), P = 0.01].
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Data from a representative subject showing log([Pi]/[PCr]) throughout the entire Ramp, Mod-Ramp, and Hvy-Ramp protocols are presented in Fig. 2. In each condition and for every subject, [Pi]/[PCr] displayed a biphasic response (P < 0.05) that facilitated modeling using a logarithm-linear transformation. Thus log([Pi]/[PCr]) data demonstrated an initial slow and later fast component (Fig. 3). A inflection or region of transition (PT) from the slow to fast components was detected in all subjects. The slope of the log([Pi]/[PCr])-power output relationship was less (P < 0.05) below the PT than above. In each condition, the occurrence of the PT was also coincident and correlated with the pHT (Ramp: r = 0.97, P < 0.001; Mod-Ramp: r = 0.97, P < .001; Hvy-Ramp: r = 0.99, P < 0.001). In Hvy-Ramp, the rate of log([Pi]/[PCr]) increase above the PT was greater compared with Ramp (P = 0.02) or Mod-Ramp (P = 0.04) (Table 3). The onset of rapid increases in log([Pi]/[PCr]) occurred at 45.1% PPO (SD 9.1) in Ramp, which was not different from Mod-Ramp [44.8% PPO (SD 17.8), P = 0.93]. However, in Hvy-Ramp, the PT occurred at a significantly higher power output [61.5% PPO (SD 12.0)] than in Ramp (P < 0.01) or Mod-Ramp (P < 0.01).
Finally, calculated mean intracellular [ADP] data for all subjects is plotted relative to %PPO during the incremental exercise protocol in Fig. 4. There was significantly greater [ADP] at 90, 95, and 100% PPO in Hvy-Ramp compared with Ramp or Mod-Ramp (P < 0.001). There were no differences between Ramp and Mod-Ramp.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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One hypothesis of this study was that prior heavy-intensity exercise would cause a rightward shift in the pHi- and ([Pi]/[PCr])-power output relationships. The premise for this hypothesis was that an accumulation of intracellular H+ during prior Hvy exercise would cause an increase in [H+] in the surrounding vasculature, resulting in local vasodilation and a decreased binding affinity of hemoglobin for oxygen. For a given power output, this could provide greater convective and diffusive O2 delivery, possibly producing or causing a greater aerobic contribution to energy production. In Hvy-Ramp, the rightward-shift of the pHi- and ([Pi]/[PCr])-power output relationship indicates a more favorable metabolic status and a decreased reliance on substrate-level phosphorylation. Stable values of [Pi]/[PCr] indicate an adequate energy status, whereas rapid increases in this ratio reflect the inability of oxidative phosphorylation to meet ATP demands (7) and/or the metabolic adjustments (i.e., a reduction in the intracellular energy state) required to maintain oxidative phosphorylation (11, 26).
A further possible interpretation of the rightward shift in the ([Pi]/[PCr])-power output relationship is a decreased [ADP] signal required to stimulate or maintain oxidative phosphorylation at a given power output or ATP demand, suggesting a corresponding increase in muscle O2 availability (i.e., greater PO2) (26). This may suggest a greater contribution of oxidative metabolism during moderate to heavy work rates (and/or decreased reliance on anaerobic metabolism). However, in the region of the pHT and PT, we observed no differences in calculated [ADP] (Fig. 4). This observation may be interpreted as evidence that PO2 was not different between conditions. If this is true, the delayed onset of acidosis in Hvy-Ramp may have directly caused the delayed increase in [Pi]/[PCr] via the creatine kinase reaction. However, a greater contribution of aerobic metabolism during exercise intensities corresponding to the rightward shift pHT in Hvy-Ramp cannot be ruled out, as it has been shown that a given [ADP] produces a greater oxidative flux in the absence of intracellular acidosis (16).
It is noted that while a significant intracellular acidosis was created during the bout of prior heavy-intensity exercise, it was observed that in Hvy-Ramp, the pHi had returned to baseline during the ensuing 6 min of resting recovery. As local muscle blood flow, perfusion, or vasodilation were not measured in this study, it is unknown whether the recovery of pHi may have influenced or possibly mitigated the hypothesized response to H+ in the surrounding vasculature following heavy-intensity exercise. Thus, from our data, enhanced O2 delivery in Hvy-Ramp cannot be stated with certainty.
A secondary finding in this study was the observation of a greater rate of decline in [Pi]/[PCr] and greater [ADP] during the later stages of incremental exercise in Hvy-Ramp. This may be interpreted to suggest reduced exercise economy in this condition. Similarly, Jones and Carter (13) demonstrated a steeper O2/work-rate slope above the GET when incremental exercise was preceded by prior heavy-intensity cycling. Sahlin et al. (24) also demonstrated reduced gross efficiency and increased total PCr breakdown during 10 min of submaximal exercise preceded by prior heavy-intensity exercise. Together, this would imply that exercise economy at heavy work rates is sensitive to the prior activity of the engaged muscles. One explanation may be that fatigue or glycogen depletion of the type II fibers during the bout of prior heavy-intensity exercise resulted in a greater activation of the type I muscle fibers during the later portions of the subsequent incremental bout (1, 5). An increased O2 or ATP requirement for the same external work rate might therefore be expected if additional muscle fiber (of any type) were recruited when a bout of prior fatiguing or heavy-intensity exercise was present. However, the contribution and pattern of fiber activation and the recruitment of other muscles (e.g., soleus, medial gastrocnemius) cannot be determined from our data.
In this study, it was hypothesized that a rightward shift in the pHi-power output relationship would maintain a more favorable pHi status that would predispose to increased exercise tolerance (22). Other studies using cycle ergometry have found similar improvements in performance following prior heavy-intensity exercise (3, 15, 25). Metabolic acidosis has been shown to inhibit oxidative phosphorylation (16) and may contribute to muscle fatigue through mechanisms related to allosteric inhibition of the rate-limiting enzymes phosphofructokinase and glycogen phosphorylase, decreased release of Ca2+ from the sarcoplasmic reticulum, and a reduction in the number and force of muscle cross-bridge activations (8). Additionally, the effect of prior heavy-intensity exercise on muscle fiber activation may influence the balance between aerobic and anaerobic contributions to energy metabolism. An increased recruitment of the more aerobic type I muscle fiber may be responsible for an increased muscle O2 (13). An increased aerobic contribution of energy metabolism might result in reduced accumulation of metabolites such as H+ and Pi and decreased breakdown of PCr as was observed in the present study. However, reduced gross efficiency during heavy work rates may explain the lack of performance enhancement in some studies. Ultimately, whether the performance of prior heavy-intensity exercise will improve performance in a subsequent bout may depend on the balance between improvements in energy metabolism vs. reductions in gross efficiency and the extent to which variables such as duration or intensity of prior exercise will modulate these factors.
In summary, in this study we observed a delayed onset of intracellular acidosis during incremental exercise when preceded by a bout of heavy-intensity exercise 6 min prior. This delayed onset of acidification was also associated with a delayed onset of rapid changes in [Pi]/[PCr]. Together, these changes resulted in a greater exercise tolerance in Hvy-Ramp and may have been a result of a greater oxidative flux given the maintenance of a more favorable pHi. We suggest that possible mechanisms may include improved muscle blood flow and perfusion, greater activation of type I muscle fibers, or both.
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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. Section 1734 solely to indicate this fact.
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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O2 kinetics during heavy exercise are related to changes in muscle activity. J Appl Physiol 93: 167–174, 2002.O2 kinetics during moderate-intensity exercise in young adults. J Appl Physiol 98: 1371–1378, 2005.O2 slow component induced by prior exercise does not affect the time to exhaustion. Int J Sports Med 23: 262–267, 2002.[CrossRef][Web of Science][Medline]O2 kinetics in heavy submaximal exercise by hyperoxia and prior high-intensity exercise. J Appl Physiol 83: 1318–1325, 1997.O2 kinetics and limb blood flow. J Appl Physiol 99: 1462–1470, 2005.O2 slow component and reduces efficiency during submaximal exercise in humans. J Physiol 564: 765–773, 2005.This article has been cited by other articles:
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  A. M. Jones, J. Fulford, and D. P. Wilkerson Influence of prior exercise on muscle [phosphorylcreatine] and deoxygenation kinetics during high-intensity exercise in men Exp Physiol, April 1, 2008; 93(4): 468 - 478. [Abstract] [Full Text] [PDF]
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 M. Amann and J. A. Dempsey Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance J. Physiol., January 1, 2008; 586(1): 161 - 173. [Abstract] [Full Text] [PDF]
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) and log([Pi]/[PCr]) (
) in a representative subject (subject 2) during Ramp, Mod-Ramp, or Hvy-Ramp. Solid lines indicate piecewise linear regression best fit. Arrows indicate power output corresponding to the pHT (
) or PT (
) for this subject.