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Departments of 1 Physiology and 4 Biochemistry, St. George's Hospital Medical School, Tooting, London SW17 0RE; 3 Centre for Exercise Science and Medicine, University of Glasgow, Glasgow G12 8QQ, United Kingdom; 5 The Center for Activity and Ageing, School of Kinesiology, and Department of Physiology, The University of Western Ontario, London, Ontario, Canada, N6A 3K7; and 2 Department of Medicine, Division of Physiology, University of California, San Diego, CA, 92093-0623
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The dynamics of pulmonary
O2 uptake (
O2) during the
on-transient of high-intensity exercise depart from monoexponentiality as a result of a "slow component" whose mechanisms remain
conjectural. Progressive recruitment of glycolytic muscle fibers, with
slow O2 utilization kinetics and low efficiency, has,
however, been suggested as a mechanism. The demonstration of high- and
low-pH components of the exercising skeletal muscle 31P
magnetic resonance (MR) spectrum [inorganic phosphate (Pi)
peak] at high work rates (thought to be reflective of differences
between oxidative and glycolytic muscle fibers) is also consistent with this conjecture. We therefore investigated the dynamics of
O2 (using a turbine and mass
spectrometry) and intramuscular ATP, phosphocreatine (PCr), and
Pi concentrations and pH, estimated from the
31P MR spectrum. Eleven healthy men performed prone
square-wave high-intensity knee extensor exercise in the bore of a
whole body MR spectrometer. A O2 slow
component of magnitude 15.9 ± 6.9% of the phase II amplitude was
accompanied by a similar response (11.9 ± 7.1%) in PCr
concentration. Only five subjects demonstrated a discernable splitting
of the Pi peak, however, which began from between 35 and
235 s after exercise onset and continued until cessation. As such,
the dynamics of the pH distribution in intramuscular compartments did
not consistently reflect the temporal features of the
O2 slow component, suggesting that
Pi splitting does not uniquely reflect the activity of
oxidative or glycolytic muscle fibers per se.
O2 uptake kinetics; magnetic resonance spectroscopy; exercise; intramuscular pH; Pi peak splitting; phosphocreatine
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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THE PULMONARY
OXYGEN UPTAKE (O2) response to
dynamic muscular exercise has been characterized with the use of
various dynamic forcing regimes and at various intensities (e.g., Refs.
2, 8, 19, 22,
25, 33, 35, 38,
54). This has allowed both estimation of the systems'
parameters and attempts to elucidate features of the physiological
control mechanisms.
During the on-transient of high-intensity cycle ergometry
exercise, the dynamics of O2 depart from
monoexponentiality (as expressed in the moderate-intensity domain) as a
result of a slowly developing supplementary component of delayed onset
(25, 52). This may be termed the "excess"
O2 (43) or the
"O2 slow component"
(55). The O2 slow component
constitutes an inefficiency of force production as the greater
O2 requirement of constant work rate (
) results in
an increased "gain" of response (i.e., 
O2/). This inefficiency is
manifest even without accounting for the simultaneous anaerobic
energy-contributions to the energy transfer. The
O2 slow component can cause
O2 to climb inexorably toward the
maximum O2 and therefore contributes to
limiting exercise tolerance. Reductions of the
O2 slow component have been demonstrated
after interventions such as training (37) or when preceded
by a bout of high-intensity exercise (8, 15, 22, 29).
The mechanisms underlying this slow component have been the focus of
much recent attention; however, they remain conjectural. The time
course and magnitude of such potential mediators as increased catecholamines (14), increased body (predominantly muscle)
temperature (21), and ventilation (50) have
been shown not to be well matched to those of the
O2 slow component. Altered proportional utilization of the malate-aspartate and the 
-glycerophosphate shuttles in type I and type II muscle fibers has been suggested as a
possible mechanism (55), as has increased respiratory, cardiac, and/or unmeasured work from auxiliary muscles with increased (Refs. 7, 50; although
epinephrine-induced hyperpnea had no influence on
O2 during heavy exercise; Ref.
14). Interestingly, the characteristics of the blood
lactate concentration ([Lac]) response to high-intensity exercise
have been shown to correlate well with those of the
O2 slow component, and under
interventions such as training (37) both responses are
reduced, suggesting that lactate may be involved in the
mediation of the O2 slow component.
However, Poole et al. (39) were unable to increase the
O2 response by lactate infusion in
working dog gastrocnemius; in addition, Roth et al. (44)
could demonstrate no influence on recovery
O2 of blood lactate being experimentally
increased to 4 or 5 mM.
Perhaps the most persistent theory is that the
O2 slow component is a consequence of
the progressive recruitment of fast-twitch, type II muscle fibers.
These have been suggested to constitute a higher proportion of the
recruited fibers as increases (17), to have a high
energy cost of force production, and to evidence slow O2
utilization kinetics in vitro (10). The latter
contentions, however, have been challenged during cycle ergometry in
humans (4).
Yoshida and Watari (59, 60) and Mizuno et al.
(28), among others, have described the existence of high-
and low-pH regions within skeletal muscle during high-intensity
exercise, discerned from the Pi peak characteristics by
using phosphorus magnetic resonance spectroscopy (31P-MRS).
These high- and low-pH regions can be discerned from a splitting of the
Pi peak, which is manifest by the low-pH Pi
peak apparently emerging from the high-pH Pi peak during
exercise; it, therefore, indicates a fall in the average intramuscular
pH. These authors have suggested that these regional pH differences are
consistent with differences between oxidative and glycolytic muscle
fibers (i.e., a high-pH region consistent with predominantly aerobic,
type I, fibers and a low-pH region consistent with acid-producing, type
II, fibers). We therefore wished to examine the dynamic features of the
31P-MRS spectrum proposed to reflect fast-twitch, type II
fiber recruitment (e.g., Pi peak splitting) in concert with
those of O2 in exercising humans, with
particular reference to the development of the
O2 slow component.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Eleven healthy men [age 26 ± 11.2 yr (mean ± SD); range 20-59; height 186 ± 4.3 cm; mass 89.9 ± 10.1 kg] provided informed consent (as approved by the Local Research Ethics Committee) to participate in the study and were cleared to exercise inside the bore of the magnetic resonance scanner. Each subject initially performed comprehensive habituation tests in the Laboratory of Human Physiology in the same prone position and using the same ergometer (see below) as used for the 31P-MRS studies. This allowed both 1) subject familiarization and 2) selection of the appropriate high-intensity work rates for the subsequent 31P-MRS experiments, i.e., a level that caused the subject to fatigue after ~10 min.
The methods employed here have been described previously by Rossiter et
al. (41). Briefly, simultaneous determinations of pulmonary O2 and intramuscular
phosphocreatine (PCr) concentration ([PCr]) were made from 44 experiments (on an average of 4 visits by each subject, with each test
on a separate day). Subjects lay prone inside the bore of the 1.5-T
superconducting magnet (Signa Advantage, GE, Milwaukee, WI) with their
feet suspended in the rubber stirrups of a custom-designed, plastic
insert into the magnet bore (56). This ergometer permitted
high-intensity exercise to be undertaken by means of rhythmic
alternate-leg knee extensions of constant excursion and frequency (in
response to an audible cue). The required work rate for each subject
could be estimated (~) by using the known elastic coefficient
of the rubber stirrups; these ranged between 60 and 120 W among all the
subjects (see Ref. 56). The contraction phase of the knee
extensors of the nondominant leg was synchronized to occur in unison
with the 31P-MRS interrogation of the quadriceps of the
relaxed dominant leg. The subject was strapped down to the scanner
table by means of a nondistensible strap placed over the hips.
Subjects performed high-intensity square-wave exercise of 4 min at
rest, 6 min of exercise, and 6 min rest (recovery). The number of
repeats required for each subject was governed by the extent to which
increasing test repeats improved the overall signal-to-noise characteristics of the averaged O2 and
[PCr] responses, thereby allowing appropriate convergence and
confidence limits (24, 40) for the subsequent parameter
estimation procedures.
31P-MRS sequence. A one-pulse 31P-MRS acquisition was employed by using a surface radio frequency (RF) coil (8-in. transmit and 5-in. receive) tuned to a frequency of 25.85 MHz for phosphorus placed under the quadriceps muscle of the dominant leg midway between the knee and hip joint (56). The coil was securely fastened to the table; this, together with the hip strap, ensured that the region of interest (ROI) in the muscle from which the 31P spectra were acquired was always in the same position relative to the coil at the time of each signal acquisition.
Initially, a series of axial gradient-recalled echo images of the thigh was acquired to confirm the correct RF coil position. Shimming (optimization of the magnetic field homogeneity) was performed by using the proton signal of muscle water over the ROI. The 31P-RF excitation pulse was set at a level to give maximum [PCr] signals at 1,875 ms repetition rate from an 80-mm-thick axial slice of muscle. Free induction decays for 31P spectra were collected every 1,875 ms throughout the entire square-wave exercise test protocol (rest-exercise-recovery) with a spectral width of 2,500 Hz and 1,024 data points. 31P-MRS data were averaged over eight acquisitions (providing a 31P spectrum every 15 s) to estimate the relative signal intensities of the three ATP peaks (,
, and 
), PCr, and Pi every 15 s.
Signal intensities, frequencies, and line widths of each resonance were
calculated (as a batch job) by means of the time-domain variable-projection fitting program VARPRO (49), by using
the appropriate prior knowledge of the ATP multiplets
(45). The T1 (longitudinal relaxation time)
saturation factor was assumed to remain constant for each resonance
throughout the experiment. Intramuscular pH was estimated from the
chemical shift of the Pi peak relative to the PCr peak in
the 31P spectrum using the relationship determined by Moon
and Richards (27)
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(1) |
is the chemical shift of the Pi peak
relative to the PCr peak.
Pulmonary gas exchange measurement.
O2 was determined breath by breath
(Clinical and Scientific Equipment, Gillingham, Kent, UK)
simultaneously with the phosphate metabolite determination, by use of
the algorithms of Beaver et al. (5), as previously
described by Whipp et al. (56). Inspired and expired
volume was measured by a custom-designed nonmagnetic turbine and a
volume-measuring module (VMM, Interface Associates, Laguna Niguel, CA).
This was calibrated with a 3.0-liter syringe before each experiment
(Hans Rudolph, Kansas City, MO). The concentrations of respired gases
(O2, CO2, and N2) were measured by
use of a quadrupole mass spectrometer (QP9000, CaSE, Gillingham)
calibrated against precision-analyzed gas mixtures. Gas was drawn
continuously from the mouthpiece along the extended 45-ft capillary
sampling line, which had a 5-95% rise time of <80 ms and a
transit delay of 1,900 ms (56).
Kinetic analyses.
The kinetic analyses were performed on the
O2, [PCr], and [Pi]
responses by nonlinear least-squares fitting (Origin, Microcal; similar
to previous studies, Refs. 40, 41). The
[PCr] data were converted to changes relative to the resting baseline
(%), which was taken as 100%. Occasional outlying data points
(outside 4 SD) were initially edited (41), after
which the repeated exercise responses were time aligned (exercise onset
corresponding to time zero), interpolated on a
second-by-second basis, and averaged (10 s for
O2 and 15 s for [PCr] and
[Pi]) for each subject.
O2,
[PCr], and [Pi] on-transients were modeled as being
monoexponential, beginning at time zero (for [PCr] and
[Pi]) or after the "cardiodynamic" or phase I
duration (for O2)
![&Dgr;PCr<SUB>(<IT>t</IT>)</SUB> = PCr<SUB>0</SUB> − &Dgr;PCr<SUB>ss</SUB>[1 − <IT>e</IT><SUP>−<IT>t</IT>/&tgr;</SUP>]](/content/vol93/issue6/fulltext/2059/img002.gif)
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(2) |
![&Dgr;P<SUB>i (<IT>t</IT>)</SUB> = P<SUB>i 0</SUB> + &Dgr;P<SUB>i ss</SUB>[1 − <IT>e</IT><SUP>−<IT>t</IT>/&tgr;</SUP>]](/content/vol93/issue6/fulltext/2059/img003.gif)
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(3) |
![<A><AC>V</AC><AC>˙</AC></A><SC>o</SC><SUB>2 (<IT>t</IT>)</SUB> = <A><AC>V</AC><AC>˙</AC></A><SC>o</SC><SUB>2 0</SUB> + &Dgr;<A><AC>V</AC><AC>˙</AC></A><SC>o</SC><SUB>2 ss</SUB>[1 − <IT>e</IT><SUP>−(<IT>t</IT> − &dgr;)/&tgr;</SUP>],](/content/vol93/issue6/fulltext/2059/img004.gif)
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(4) |
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O2 0,
PCr0, and Pi 0 are the values of
O2, [PCr] and [Pi] at
time (t) = 0;
O2 ss, PCrss, and Pi ss are the asymptotic
values to which O2, [PCr], and
[Pi] are assumed to project; 
is the time constant of
the responses; and is a delay term similar to (but not equal to)
the phase I-to-phase II transition time (e.g., Refs. 54, 24). Because the responses of [PCr] and [Pi]
would not be expected to display a cardiodynamic phase, the term
was not included in the model for these variables; we have previously
found that does not significantly differ from zero for [PCr]
(42). The confidence limits for the parameter estimation
(40) and the 
2 value were also obtained;
confidence was set at 95% and tolerance at 5% (i.e., P 
0.05). The off-transients of [PCr] and
O2 have been previously described
(42); however, the off-transient of [Pi] was
fit in a similar manner to the on-transient described above (see Ref.
42 for further details).
The fitting strategy was designed to identify, a posteriori, the
onset of a putative delayed "slow component" in the response profiles (41). The fitting window extended from exercise
onset (i.e., from t = 0 s for [PCr] and
[Pi] and t = time at the end of phase I
for O2) initially only 60 s into
the exercise. The window was lengthened iteratively, until the
exponential model fit demonstrated a discernible departure from the
measured response profiles. Two alternative indexes were used to
determine the goodness-of-fit: 1) the maintenance of a flat
profile of the residual plot (i.e., signifying a good fit to measured
data), as judged by visual inspection, and 2) the
demonstration of a local "threshold" in the 2 value.
This allowed estimation of the fundamental steady-state value for
O2 [PCr] and [Pi]. The
magnitude of the slow component for
O2 [PCr] and [Pi] was
then estimated from the steady-state amplitude of the fundamental
(i.e., O2ss, [PCr]ss, and [Pi]ss) and
the amplitude of the final value, averaged from the last 15 s of
the response (termed
O2end, [PCr]end, and [Pi]end).
Thus the percentage contribution of the slow component to the total
response of variable y is equal to
[(yend 
yss)/yss] × 100.
The differences between parameter values were examined by Student's
t-test or ANOVA with Scheffé's post hoc testing where appropriate. The significance of all the fits to the responses was also
estimated by using the 2 goodness-of-fit test. Values
are given as means ± SD, or 95% confidence intervals
(C95) where indicated, and a P value of <0.05 was used as the criterion for the rejection of the null hypothesis.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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[PCr] and O2.
We found no evidence of alterations in the three phosphoryl residues of
ATP (, , and ) throughout the rest-exercise-rest protocol;
however, the [PCr], which began to decrease at the onset of exercise
with no discernable delay, continued to fall throughout the exercise
bout, i.e., with no steady state being attained. As such, a
monoexponential fit to the [PCr] response to high-intensity exercise
was, as expected, not adequate to characterize the response (Fig.
1A) and, therefore, the fit
was limited to the fundamental exponential region (see Kinetic
analyses for methods; Fig. 1B). This was also the case
for the on-transient of the O2 response (Fig. 1A). The fundamental values for [PCr] and
O2 were not different from each other
and averaged 39 ± 5 and 42 ± 6 s, respectively. The
C95 limits for parameter estimation were established to
within, on average, 6 s.
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O2 averaging 15.9 ± 6.9%, i.e.,
~130 ml/min. These were not different from each other; however, there
was a large variability of responses among subjects. The estimated time
of onset of the slow components were 227 ± 39 s for [PCr] and
223 ± 33 s for O2; these were not
significantly different.
Intramuscular [Pi].
The [Pi] response during high-intensity exercise was more
complex than the simple inverse of [PCr] unlike the moderate
intensity (3); furthermore, the [Pi]
response was not consistent between subjects. During high-intensity
exercise, two [Pi] peaks were manifest, suggestive of
both a high- and a low-pH regions of the ROI, but unlike previous
reports (59, 60) this was not consistently the case and
occurred in 5 of the 11 subjects. Two stack-plot examples of the
responses are shown in Fig. 2,
top. Fitting these peaks as separate regions of the
31P-MRS spectrum proved problematic because the smaller
(higher frequency) peak emerged out of the larger (low-frequency) peak. However, fitting each spectrum "manually" with the VARPRO fitting software (rather than automatically as a batch job) enabled a time
course of the splitting process to be estimated; the onset of the
[Pi] peak splitting averaged 121 ± 82 s and
varied between 35 and 235 s after exercise onset in the five
subjects and did not correlate to the time of the onset of the [PCr]
or O2 slow components. In fact, in only
1 of the 11 subjects were the three events temporally related; the
emergence of a second [Pi] peak occurred at 235 s,
with the O2 and [PCr] slow components
emerging at 210 s and 248 s, respectively (with an average
resolution of 15 s). At exercise cessation, [Pi]
fell to values below that of the preexercise baseline (on average 39%
of the preexercise baseline; range 0-74%); however, in 4 of the
11 subjects this was so extreme that the [Pi] peak could
actually not be resolved from the noise in the 31P
spectrum. This resulted in [Pi] estimates of 0% of the
baseline resting value. This off-transient behavior of
[Pi] has previously been described by Bendahan et al. (6;
see discussion).
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value for it), and neither did it
consistently demonstrate a clear fundamental and slow component, as was
the case for [PCr]: representative examples of subjects expressing a
single or a split Pi peak are shown in Fig.
3. Figure 3A shows a typical
example in which the [Pi] rose rapidly over the first
~45 s of exercise, before decreasing by a magnitude that varied among
subjects, often, but not exclusively, to attain a new steady state. The
example in Fig. 3B shows how the two regions of the
[Pi] response sum to give a total [Pi]
response. This also was not consistently well fit by an exponential;
however, accounting for the two Pi peaks often improved the
fit, as demonstrated here. It was not possible, however, to provide a
single typical characterization of the temporal responses of the two
[Pi] peaks (in subjects who expressed a split
Pi peak) because the peak split at such a wide range
of time after exercise onset (35-235 s). However, the amplitudes of the two peaks were more consistent by the end of the exercise, with
the high-pH region averaging 69 ± 7% of the total.
Consequently, because of the variability of the [Pi]
response, even when the model fit was restricted to the early phase of
response (as with O2 and [PCr]), the
exponential model did not provide a good fit to the data in most cases.
Interestingly, however, the off-transient was better fit by a single
exponential, when possible (i.e., when [Pi] did not fall
to functionally zero) with a of 43.9 ± 12.1 s and
C95 of 3.5 ± 1.7 s (n = 7).
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Intramuscular pH. Estimation of the pH was complicated by the nonconsistent behavior of the [Pi] peak. Of the five subjects who expressed a clearly discernable splitting of the [Pi] peak, two "regional" pH values were estimated (the Pi peak amplitude, the weighted average of which was used to calculated the mean pH for each subject). The lower of the two pH regions (pHlo) averaged 6.62 ± 0.13 in the five subjects and the higher of the two regions (pHhi) averaged 7.05 ± 0.04. Figure 2 (middle) shows the responses from two subjects; one without (A) and one with (B) Pi peak splitting. The off-transient dynamics of pH were similarly problematic, because the characteristic fall of [Pi] to values below resting during the off-transients resulted in difficulties in resolving the peak center and hence the chemical shift. At the off-transient, accurate estimates of pHhi and pHlo were complicated by the disappearance of [Pi] in the spectrum.
With appropriate analysis to take into account the splitting behavior of the Pi peak, the mean intramuscular pH followed a similar time course in all 11 subjects (similar to the individual examples in Fig. 2). For the 4 min at rest before exercise, the intramuscular pH averaged 7.06 ± 0.03 (Table 1). At the onset of exercise, there was typically an alkaline shift in the overall pH that peaked (average 7.12 ± 0.04) after ~30-45 s. This was followed by a progressive acidosis, causing pH to fall to an average of 6.95 ± 0.09 by the end of the exercise. Those five subjects who expressed a split Pi peak had a significantly lower end-exercise mean pH than those subjects who maintained a single Pi peak, presumably owing to a weighting of the pHlo region. Thus the change in pH in these five subjects between the onset and end-exercise values (SD) averaged0.2 pH units (0.07) compared with
0.1 (0.05) in the other six subjects.
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Comparison of pH distribution (Pi frequency
distribution) and O2 kinetics.
Despite the heterogeneity in the splitting of the Pi peak
during high-intensity exercise, the corresponding
O2 responses all showed a slow
component. Two examples are given in Fig. 2, demonstrating that the
existence of a O2 slow component (Fig. 2, bottom) was not dependent on a split Pi peak
(Fig. 2, top). Of the subjects who did show a separate
"region" of Pi corresponding to pHlo, the
average O2 slow component was greater in
magnitude than those who expressed a homogeneous Pi
response. However, whereas the "splitting" group showed a
O2 slow component of 18.1 ± 6.8%, the "nonsplitting" group still expressed a marked
O2 slow component of 14.1 ± 7.0%;
these were, however, not statistically different. Only the pH decrement
(Table 1) was different between the groups (presumably because of the
greater influence by the pHlo region in the subjects with a
split Pi peak), but this did not correlate to the existence
or absence of [PCr] or O2 slow
components. The parameters and variables distinguished by group (i.e.,
split Pi peak compared with single Pi
peak) are given in Table 1.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The contention that the high-intensity-exercise-induced
O2 slow component is due to progressive
recruitment of fast-twitch, type II muscle fibers remains to be
conclusively confirmed or refuted. In this study, we observed features
of the intramuscular 31P-MRS spectrum during exercise that
have been suggested (e.g., Refs. 59, 60) to reflect
fast-twitch fiber recruitment, and we have attempted to clarify their
relationships with the O2 slow
component. Repeated and simultaneous measurements allowed determination
of the kinetics of the 31P-MRS spectra and
O2 to be made with sufficient confidence
to allow the comparisons to be meaningful (e.g., Refs. 24,
40). The results, however, suggest that either 1)
fast-twitch, type II fiber recruitment is not required to elicit a
O2 slow component or 2) the
split Pi peak does not necessarily reflect recruitment of
fast-twitch muscle fibers. We favor the latter suggestion because other
features of the 31P-MRS spectrum, such as the [PCr] slow
component (which were closely coupled to
O2 slow component) and progressive
Pi line-width broadening, may be considered consistent with
progressive recruitment of lower efficiency muscle fibers (such as type II).
Dynamic coupling of the O2 and
[PCr] responses.
The O2 slow component may be regarded as
a characteristic dynamic feature of the
O2 response to heavy- and
very-heavy-intensity exercise (33) that is
superimposed on to what may be termed the "fundamental"
response to a step increase in work rate (2, 35, 39, 53).
The potential mechanisms determining the
O2 slow component have previously been
reviewed (55) and have been investigated in our laboratory
in relation to intramuscular [PCr] responses (41, 42);
however, its precise mechanism(s) remain(s) poorly understood. Poole et
al. (38) have demonstrated that the time course of
the O2 slow component was significantly
associated with O2 across the exercising
limb, such that, on average, ~86% of the slow component of
O2 arose in the exercising muscle. Other
authors (e.g., Refs. 7, 32), however, have suggested a
more significant role of increases in unmeasured work done by the arms
and other stabilizing muscles during heavy-intensity cycling exercise
or a greater contribution from cardiac and/or respiratory muscle work
during high-intensity exercise (9, 50). A further
suggestion (e.g., Ref. 55) is that a progressive recruitment of fast-twitch, low-efficiency muscle fibers causes the
O2 slow component during high-intensity
exercise. The findings of Poole and colleagues (36, 37),
that [Lac] and arterial pH were well correlated with the
O2 slow component is consistent with
this notion; that is, it is a manifestation of the recruitment of
fast-twitch, type II fibers that are predominantly glycolytic and hence
highly acid producing. Also further suggestions by Casaburi et al.
(9) and Poole et al. (37) that training
reduces both the O2 slow component and
the [Lac] responses to a specific work rate may be interpreted as
a smaller reliance on fast-twitch, type II muscle fiber contribution to
force production in the trained state.
O2 kinetics,
are consistent with previous findings from this laboratory (e.g., Refs.
41, 42) that the O2 slow component is a reflection of "excess" O2 consumption
(cf. Ref. 38). Similar to findings in cycle ergometry
(e.g., Refs. 2, 8, 33, 35), these data demonstrate that
the O2 slow component is superimposed on
the fundamental response in the knee extensor exercise model, causing a
reduction in the O2 utilization efficiency of the muscular
work (or an increase in gain, i.e.,
O2/). This kinetic feature
of [PCr] metabolism suggests that the low efficiency of
high-intensity exercise is more a manifestation of a high phosphate
cost of force production rather than a high O2 cost of
phosphate production (42). This notion is also consistent with the findings of Crow and Kushmerick (10) in mouse
muscle, that fast-twitch muscle fibers are kinetically slow and have a low oxidative efficiency. This notion (10), however, has
thus far not been demonstrated in human muscle and has been challenged by Barstow et al. (4), who suggest that during cycle
ergometry in humans fast-twitch muscle fibers express a low fundamental gain: that is, express a low O2 consumption-to-force
production ratio. Nevertheless, the progressive reduction in pH in the
present study, coupled with the manifestation of an intramuscular
[PCr] slow component, suggests that acid-producing fibers with poor energetic efficiency may be contributing to force production during this high-intensity exercise.
[Pi] response to high-intensity exercise. The surprising finding that the [Pi] kinetics were not consistently well modeled by an exponential function for the fundamental region (as was the case for [PCr]) may be explained by physiological and/or methodological mechanisms. Other authors have suggested that the [Pi] response to moderate-intensity exercise is well characterized by an exponential (3). However, the work rates in that study would have been unlikely to give rise to large changes in intramuscular pH or large alterations in the rate of glycolytic flux. High-intensity exercise in this study, by contrast, did lead to a progressive acidosis, which is suggested to be predominantly due to a significantly increased rate of glycolysis and hence lactate production. This may have a number of potential consequences on the 31P-MRS estimation of [Pi]. First, Bendahan et al. (6) have suggested that [Pi] may become trapped in the glycogenolytic pathway as determined by changes in the phosphomonoester (PME) concentration ([PME]). They noted that the postexercise undershoot of [Pi] could be accounted for by a buildup in [PME], a feature consistent with our findings. This notion is in accordance with the findings Duboc et al. (11) that the sequestering of Pi in the glycolytic chain as PME occurs during exercise but also at rest in subjects with enzyme deficiencies (e.g., of phosphofructokinase), although the total (i.e., [Pi] + [PME]) appears to be unchanged (6). Because [PME] increased throughout the 3 min of exercise in the study of Bendahan et al. (6), it is reasonable to assume that Pi-to-PME trapping may persist throughout the 6 min of exercise in the present study and that the high-intensity nature of the exercise (and hence the presumably high glycolytic flux) may exacerbate the flux of Pi to PME. Unfortunately, [PME] is not easily detectable at 1.5 T [Bendahan et al. (6) used 4.7 T for increased signal-to-noise], and as such we have no measure of this possible trapping. However, because of the (sometimes extreme) undershoot in [Pi] that we observed in recovery (range of the [Pi] asymptote was 0-74% of the resting baseline), it is likely that Pi disappears from the MRS-visible pool consequent to exchange with PME. This could lead to the nonexponential behavior that was typical of the [Pi] response to high-intensity exercise in this study. Furthermore, the more consistent exponential response of [Pi] in recovery supports this notion. Others (e.g., Ref. 51) have suggested that Pi may be taken up by the sarcoplasmic reticulum, a mechanism linked closely to the fatigue process; however, no measure of this was made in this study.
Another potential effect of pH on [Pi] estimation by MRS is a methodological concern. Newcomer and Boska (30) have attempted to elucidate the changes in T1 relaxation times of PCr and Pi on transition from rest to exercise at 1.5 T by using 90 s of voluntary submaximal isometric plantar flexion exercise. The fact that, in our experiments, the PCr and Pi signals are partially saturated (to maximize the temporal frequency of sampling) may cause measurement errors if the T1 of these variables changes significantly during exercise. The findings of Newcomer and Boska suggest that T1 for PCr may be reduced by up to 20%. However, these changes all occurred within the first sampling point (i.e., <10 s), which would result in little or no effect on the estimation of the time constants of subsequent PCr kinetics. The T1 for Pi, however, was found to increase by ~60% on transition to exercise and subsequently fall gradually throughout exercise. This alteration of T1 for Pi was found to be significantly correlated to pH; a 0.1-pH unit reduction reduced the T1 by ~50%. This suggests that [Pi] determination using partially saturated signals is only valid when the pH is stable. This isometric exercise modality is likely not to be directly applicable to our dynamic knee extensor exercise because, for example, changes in other ions and molecules would be expected to alter the Pi T1, e.g., [PCr] and Mg2+ (12, 23, 26). Also, the effect would be likely to be manifest in the opposite direction in recovery, whereas we found more consistent exponential behavior during the recovery phase. To our knowledge, the relevant studies for rhythmic exercise have not yet been made.Intramuscular features of the 31P spectrum consistent
with fast-twitch fiber recruitment.
Although the estimation of [Pi] is problematic, its
frequency in the 31P-MRS spectrum may be used as a valid
estimate of intramuscular pH (27). In the present study,
the intramuscular pH profile was consistent among subjects when
considered as a single manifestation of the average pH within the ROI
(Fig. 2, middle). The profile showed a progressive
acidification such that the end-exercise pH averaged 6.95 compared with the preexercise baseline value of 7.06. The
magnitude of the fall of pH, however, showed no correlation to the
magnitude of O2 slow component or the
[PCr] slow component, suggesting that low pH per se may not evoke
a O2 slow component. This
relationship was not improved if only the slow-component regions were
considered (i.e., comparing the O2
from the fundamental asymptote to the end of the exercise and the
simultaneously determined pH).
O2, an issue as yet unresolved.
Crow and Kushmerick (10) demonstrated in vitro that there
was a greater energy cost per unit force production for type II fibers
compared with type I. Gaesser et al. (13) indicated, in
vivo, that the O2 slow component was
considerably augmented by increasing cycling cadence from 50 to 100 rpm, suggesting that higher cadences, which elicit a faster twitch
fiber population, produced an increased
O2 slow component, although Barstow et al. (4) have opposed this view. However, it is presently
not clear whether the O2 slow component
is mechanistically linked to a progressive contribution of
low-oxidatively-efficient muscle fibers; this remains a commonly held
view (see Ref. 55 for review). This being the case, we
have demonstrated that there is a high energy cost, originating in the
exercising muscle in the form of increased [PCr] metabolism, which is
consistent with the recruitment of low oxidatively efficient muscle
fibers (presumably type II). Alternatively, the findings are also
consistent with a greater number of slow-twitch units contributing to
the energy exchange as force generation declines in the fatiguing
units. We were, however, unable to demonstrate any statistical
correlation between the O2 slow
component and the expression of a split Pi peak. That is,
all subjects expressed a O2 slow
component and a [PCr] slow component, but only five subjects showed a
split Pi peak (Fig. 2). This suggests 1) that
the expression of a split Pi peak is not consistent with
the expression of the O2 slow component, and, therefore, we feel that a split Pi peak is more likely
to reflect differences of force contribution from various muscle motor
units [similar to suggestions by Taylor et al. (47) and Jeneson et al. (20)], and 2) that the
O2 slow component and [PCr] slow
component may be evident even without muscle regions expressing
markedly decreased pH (i.e., arising from fibers with relatively high
mitochondrial density).
Furthermore, -ATP splitting has also been observed during exercise
and has been linked to pH (58). However, there were no
discernable alterations in -ATP in our studies. Additionally, Takahashi et al. (46) have suggested that metabolite
ratios (e.g., [PCr]/[ATP]) might be used to distinguish between
slow-twitch (type I, low [PCr]/[ATP]) and fast-twitch (type II,
high [PCr]/[ATP]) fibers of muscle by using 31P-MRS at
rest. However, we could see no evidence between the subjects that a
high resting [PCr]/[ATP] corresponded to a greater magnitude of the
slow components of either [PCr] or O2.
It may also be inferred that those subjects who expressed a split
[Pi] peak may manifest greater "local" fatigue
and hence a greater O2 slow component.
It has been clearly demonstrated, in vitro, that the diprotonated form
of Pi (H2PO
O2 slow component reflects a progressive
recruitment of muscle fibers with relatively slow kinetics, then these
five subjects might be expected to manifest either an earlier onset of
the O2 slow component or a
O2 slow component of greater magnitude.
This, however, was not apparent from our findings.
We have demonstrated that neither the time course nor the presence of
the splitting of the Pi peak is a functional correlate of
the O2 slow component during
high-intensity exercise. However, the pH distribution we observed
(estimated from the chemical shift of the Pi peak) appears
to be more complex than a simple peak doublet, suggesting that
Pi splitting may not uniquely reflect the activity of
oxidative or glycolytic muscle fibers per se. Rather, we feel that
Pi peak splitting is more likely to reflect heterogeneous
contributions to force production within the exercising muscle. We
have, however, demonstrated that a kinetically similar component of the
O2 slow component is evident in the
exercising muscle in the form of increased [PCr] metabolism. As such,
although the mechanism controlling the
O2 slow component remains conjectural, our findings add further weight to the suggestion that the
O2 slow component originates from the
exercising muscle and that progressive recruitment of muscle fibers
that possess lower oxidative efficiency and higher [PCr] utilization
at this high-intensity work rate may be contributory.
| |
ACKNOWLEDGEMENTS |
|---|
The authors thank Dr. Dominick McIntyre at St George's Hospital Medical School for the design of computer program to assist with data analysis in part of this study.
| |
FOOTNOTES |
|---|
Research was supported by The Wellcome Trust Grant 058420. H. B. Rossiter was supported by an International Prize Travelling Fellowship, The Wellcome Trust. F. A. Howe and J. R. Griffiths are supported by Cancer Research, UK, Grant SP 1971/0405.
Address for reprint requests and other correspondence: B. J. Whipp, CESAME, West Med Bldg., Glasgow Univ., Glasgow, G12 8QQ, United Kingdom (E-mail: bwhipp{at}rei.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.
August 30, 2002;10.1152/japplphysiol.00446.2002
Received 20 May 2002; accepted in final form 27 August 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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A. M. Jones, D. P. Wilkerson, N. J. Berger, and J. Fulford Influence of endurance training on muscle [PCr] kinetics during high-intensity exercise Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R392 - R401. [Abstract] [Full Text] [PDF]
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R. A. Howlett, C. A. Kindig, and M. C. Hogan Intracellular PO2 kinetics at different contraction frequencies in Xenopus single skeletal muscle fibers J Appl Physiol, April 1, 2007; 102(4): 1456 - 1461. [Abstract] [Full Text] [PDF]
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N. J. A. Berger, I. T. Campbell, D. P. Wilkerson, and A. M. Jones Influence of acute plasma volume expansion on VO2 kinetics, VO2peak, and performance during high-intensity cycle exercise J Appl Physiol, September 1, 2006; 101(3): 707 - 714. [Abstract] [Full Text] [PDF]
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S. Keslacy, S. Matecki, J. Carra, F. Borrani, R. Candau, C. Prefaut, and M. Ramonatxo Effect of inspiratory threshold loading on ventilatory kinetics during constant-load exercise Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2005; 289(6): R1618 - R1624. [Abstract] [Full Text] [PDF]
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S. C. Forbes, G. H. Raymer, J. M. Kowalchuk, and G. D. Marsh NaHCO3-induced alkalosis reduces the phosphocreatine slow component during heavy-intensity forearm exercise J Appl Physiol, November 1, 2005; 99(5): 1668 - 1675. [Abstract] [Full Text] [PDF]
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R. Beneke, M. Hutler, M. Jung, and R. M. Leithauser Modeling the blood lactate kinetics at maximal short-term exercise conditions in children, adolescents, and adults J Appl Physiol, August 1, 2005; 99(2): 499 - 504. [Abstract] [Full Text] [PDF]
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D. S. DeLorey, J. M. Kowalchuk, and D. H. Paterson Adaptation of pulmonary O2 uptake kinetics and muscle deoxygenation at the onset of heavy-intensity exercise in young and older adults J Appl Physiol, May 1, 2005; 98(5): 1697 - 1704. [Abstract] [Full Text] [PDF]
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S. G. Fawkner and N. Armstrong Longitudinal changes in the kinetic response to heavy-intensity exercise in children J Appl Physiol, August 1, 2004; 97(2): 460 - 466. [Abstract] [Full Text] [PDF]
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L. J. Haseler, C. A. Kindig, R. S. Richardson, and M. C. Hogan The role of oxygen in determining phosphocreatine onset kinetics in exercising humans J. Physiol., August 1, 2004; 558(3): 985 - 992. [Abstract] [Full Text] [PDF]
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Y. Fukuba, Y. Ohe, A. Miura, A. Kitano, M. Endo, H. Sato, M. Miyachi, S. Koga, and O. Fukuda Dissociation between the time courses of femoral artery blood flow and pulmonary VO2 during repeated bouts of heavy knee extension exercise in humans Exp Physiol, May 1, 2004; 89(3): 243 - 253. [Abstract] [Full Text] [PDF]
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M. Endo, S. Tauchi, N. Hayashi, S. Koga, H. B. Rossiter, and Y. Fukuba Facial cooling-induced bradycardia does not slow pulmonary V.O2 kinetics at the onset of high-intensity exercise J Appl Physiol, October 1, 2003; 95(4): 1623 - 1631. [Abstract] [Full Text] [PDF]
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H. B. Rossiter, S. A. Ward, F. A. Howe, D. M. Wood, J. M. Kowalchuk, J. R. Griffiths, and B. J. Whipp Effects of dichloroacetate on VO2 and intramuscular 31P metabolite kinetics during high-intensity exercise in humans J Appl Physiol, September 1, 2003; 95(3): 1105 - 1115. [Abstract] [Full Text] [PDF]
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) and phosphocreatine
concentration ([PCr]; 
) responses to high-intensity
constant-load exercise in a typical subject. The overlaid models
demonstrate that the kinetics of both variables are not well fit by a
monoexponential to the entire response (A), but the
fundamental components of 
, pHhi,
calculated from high-pH Pi peak; 
,
pHlo, calculated from low pH Pi peak.
Bottom: [PCr] (
