Effect of muscle temperature on rate of oxygen uptake during exercise in humans at different contraction frequencies
1
Centre for Biophysical and Clinical Research into Human Movement,
Manchester Metropolitan University, Hassall Road, Alsage, Alsager ST7 2HL,
UK
2
Institute for Fundamental and Clinical Human Movement Sciences, Vrije
University, Amsterdam, The Netherlands
*
Present address: Applied Physiology Group, Strathclyde Institute for
Biomedical Sciences, University of Strathclyde, Southbrae Drive, Glasgow G13
1PP, UK
Present address: Biomedical Sciences, University Medical School, Foresterhill,
Aberdeen, AB25 2ZD, UK
(e-mail: richard.ferguson{at}strath.ac.uk )
Accepted 14 January 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: contraction velocity, temperature, cycling exercise, human, efficiency/velocity relationship
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Surprisingly, the effect of a change in muscle temperature on the
efficiency of muscle contraction in humans in vivo has received
little attention. This is despite the fact that the in vivo
temperature of human skeletal muscles can vary over a wide range depending on
environmental conditions and the metabolic heat liberated in the muscle itself
(e.g. Asmussen and Bøje,
1945; Saltin et al.,
1968
). Indeed, it is common practice for athletes to perform
warming-up exercises prior to training or competition. However, the effect of
muscle temperature on the mechanical efficiency of exercise in humans may be
velocity-specific since it would imply a shift in the efficiency/velocity
relationship analogous to that previously reported for the power/velocity
relationship for human exercise (for a review, see
Sargeant, 1999
).
The purpose of the present study was therefore to determine whether an
increase in muscle temperature affected energy turnover and estimates of net
mechanical efficiency during sustained dynamic exercise in humans. It was
hypothesised that the effect of increasing muscle temperature on energy
turnover would be dependent on contraction frequency. It has previously been
speculated that the optimum pedalling frequency for efficiency of the type I
fibres during cycling might be approximately 60 revs min-1 (see
Sargeant, 1999). Any
temperature-related shift in the efficiency/velocity relationship towards the
right would mean that exercise at a low pedalling frequency of approximately
60 revs min-1 would be on the ascending limb of the relationship.
Thus, energy turnover would be greater for the same mechanical output.
Conversely, a fast pedalling rate would be on the descending limb of the
efficiency/velocity relationship, and any temperature-related rightwards shift
would lead to an increase in efficiency and, hence, energy turnover for a
given mechanical output would be expected to decrease.
We have tested this hypothesis (i) by estimating the energy turnover during cycling at 60 revs min-1 at normal muscle temperature and following passive heating and (ii) by estimating the energy turnover at normal and elevated muscle temperature when cycling at 120 revs min-1, this latter pedalling rate being chosen as the fastest pedalling rate that could be reliably sustained.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Pre-experimental procedures
Each subject performed two tests to determine the maximum rate of oxygen
uptake (O2max),
one at 60 and the other at 120 revs min-1, using a multi-stage
protocol on a friction-braked cycle ergometer (Monark 814, Varberg, Sweden).
Each stage lasted for 3 min, and expired air was analysed during the last
minute of each stage. From the relationship between power output and
O2, an external
power output equivalent to 85 % of
O2max was
calculated for each contraction frequency. All experiments were performed at
this intensity, which was chosen to enable exercise to be sustained while
eliciting a high
O2 so that small
changes in
O2
would be measurable. In addition, it should be noted that this intensity is
also typical of that during prolonged endurance events when small changes in
efficiency may critically affect performance. Prior to the experimental
trials, each subject performed at least one habituation trial to familiarise
himself with the experimental protocol.
Experimental protocol
The subjects arrived at the laboratory in the morning following an
overnight fast. In the normal temperature condition, subjects rested for 30
min at normal room temperature (20-22 °C; quadriceps muscle temperature
approximately 36 °C at 3 cm depth)
(Sargeant, 1987). In the
heated temperature condition, muscle temperature was increased by immersing
the legs, up to the gluteal fold, in a water bath at 42 °C for 30 min. On
these occasions, the subjects exited the water bath, briefly towelled dry and
put on their shoes before mounting the cycle ergometer (this typically took
less than 2 min). In a parallel study using the same heating protocol, muscle
temperature, measured by a needle thermistor (Ellab, Copenhagen, Denmark), was
found to be elevated by 2.4±0.2 °C immediately prior to the
commencement of exercise compared with normal temperature conditions. In
parallel experiments, it was also shown that the effect of exercise was to
increase muscle temperature by a further 0.5 °C in the `heated' conditions
and by 3.5 °C in control conditions. This indicates a convergence of
muscle temperature towards the end of the exercise period, although there was
still a significantly higher temperature in the pre-heated trials
(P<0.05).
Immediately after temperature manipulation or the 30 min rest period, the
exercise trial began. This consisted of a 3 min rest period whilst seated on
the cycle ergometer, after which subjects performed 3 min of unloaded cycling
followed immediately by a 6 min period of cycling at the predetermined power
output equivalent to 85 % of
O2max at 60 or
120 revs min-1. After the exercise bout, there was a final 5 min
period of rest seated on the ergometer. Pulmonary gas exchange was
continuously measured throughout the exercise trial. Blood samples for the
determination of blood lactate concentration were collected prior to leg
warming, immediately before exercise and at 0.5, 1.5, 3 and 5 min
post-exercise.
The experiments at normal and heated muscle temperatures and at 60 and 120 revs min-1 were performed, in randomised order, on separate occasions with at least 4 days between trials. The pulmonary gas exchange data were averaged between two repeated trials. Blood samples were obtained on only one occasion for each condition.
Metabolic measurements
Expired air was sampled continuously for percentage CO2 and
O2 content and volume on a breath-by-breath gas-analysis system
(2900 Metabolic Measurement Cart, Sensormedics, Netherlands). This was
calibrated with gases of known concentration and a 31 syringe immediately
prior to each testing session. Breath-by-breath
O2 data were
computed and then averaged over each minute of sampling for each trial. The
coefficient of variation for repeated
O2 measurements
was 3.4 %.
Arterialised venous blood samples
(Forster et al., 1972) were
taken via an indwelling butterfly needle (21G) inserted into a
superficial vein on the dorsal surface of the hand following immersion in hot
water (42 °C) for a minimum of 10 min. The needle was kept patent by
regular flushing with heparinised sterile saline. Blood samples (2.5ml) were
mixed thoroughly with EDTA (3 mg ml-1). From these samples,
duplicate aliquots (100 µl) of whole blood were immediately deproteinised
in 1 ml of ice-cold perchloric acid (2.5%) and stored at -20°C for later
analysis. The concentration of blood lactate was determined fluorimetrically
using the supernatant from the deproteinised blood
(Maughan, 1982
). The
coefficient of variation for duplicate samples was 3.9%.
Calculations
Aerobic energy turnover (kJ min-1) was calculated using the
respiratory exchange ratio (RER) and rate of oxygen uptake. Net
O2 was calculated by
subtracting resting from exercise
O2, with the exercise
O2 averaged over the final
3 min of exercise. Anaerobic energy turnover (kJ min-1) was
calculated on the assumption that 1 mmol l-1 of post-exercise blood
lactate accumulation yields the equivalent of 3.3 ml
O2kg-1 (for a review, see
Di Prampero and Ferretti,
1999
). Net blood lactate accumulation was calculated as the
difference between the peak post-exercise concentration and the corresponding
resting lactate concentration. Total energy turnover (kJ min-1) was
calculated as the sum of aerobic energy turnover and anaerobic energy
turnover. Total mechanical power output (W) was calculated as the sum of the
external power delivered to the cycle ergometer plus the estimated `internal'
power output. Internal power output (W kg-1) was estimated as
0.153(frequency)3, where frequency is in Hz
(Minetti et al., 2001
). Net
mechanical efficiency (%) was defined as the ratio between total mechanical
power output (W converted to kJ min-1) and the total rate of energy
turnover.
Statistical analyses
Data were analysed by either paired t-tests or two-way
(temperature and time) analysis of variance (ANOVA) with repeated measures,
where appropriate. When a significant effect was detected, differences were
located with post-hoc paired t-tests. Significance was
accepted at P<0.05. Data are presented as means ± S.E.M.
(N=6).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Pulmonary
O2
The effects of heating the legs in the water bath was to increase the
O2 of exercise by 0.151
min-1 when pedalling at 60 revs min-1 compared with the
control (P<0.05; Figs
2,
3;
Table 1). In contrast, when
pedalling at 120 revs min-1, the effect of the same prior hot water
immersion protocol was to decrease the exercise
O2 by 0.131
min-1, compared with the control (P<0.05; Figs
2,
3;
Table 1).
|
|
|
Blood lactate levels
Consistent with the changes in pulmonary
O2, the effect of heating
the legs was to increase (at 60 revs min-1) or decrease (at 120
revs min-1) the concentration of blood lactate by less than 2 mmol
l-1 (P<0.05; Fig.
4).
|
Energy turnover and mechanical efficiency
The estimated total rate of energy turnover (aerobic+anaerobic; see
Materials and methods) at 60 revs min-1 was 5.2% higher
(P<0.05) when the legs were heated compared with the normal
condition. In contrast, at 120 revs min-1, the converse was
observed, with a 5.9% decrease (P<0.05) in energy turnover
(Table 2). At 60 revs
min-1, the total rate of energy turnover (aerobic+anaerobic; see
Materials and methods) was higher when the legs were heated compared with the
control (P<0.05). Since the total mechanical power (internal and
external components) remained the same at 247 W, the estimated net mechanical
efficiency decreased by 1% (P<0.05) following passive heating.
Thus, a 1% decrease in absolute terms would represent a relative decrease in
the apparent net mechanical efficiency of 5%. At 120 revs min-1,
the total rate of energy turnover (aerobic+anaerobic; see Materials and
methods) was lower when the legs were heated compared with the control
(P<0.05). With the total mechanical power (internal and external
components) remaining the same at 259 W, the estimated net mechanical
efficiency increased by just over 1 % (P<0.05) following passive
heating. In this case, a 1 % increase in absolute terms would represent a
relative increase in net mechanical efficiency of just over 5 %.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
During exercise at 60 revs min-1, energy turnover was greater
when muscle temperature was elevated. This observation is perhaps not
surprising since the main determinant of total energy turnover for muscle
contraction is the cost of cross-bridge cycling. It is to be expected that the
rate of cross-bridge cycling will increase with an elevated muscle temperature
since, as with other enzymatic processes, myofibrillar ATPase activity is
temperature-dependent (see Stienen et al.,
1996; He et al.,
2000
). Indeed, in isometric contractions in humans, the economy of
muscle contraction had previously been reported to decrease, as shown by an
elevated ATP utilisation, when muscle temperature was increased from 22.5 to
38.6° C (Edwards et al.,
1972
). Just as increased cross-bridge cycling during isometric
contractions will require an increased energy turnover for the same sustained
force, at relatively slow contraction velocities, the effect of prior heating
could result in cross-bridge cycling that is faster than required by the
actinmyosin movement. Thus, we would propose that, in these
experiments, prior heating results in an inappropriately fast rate of
cross-bridge cycling at 60 revs min-1 leading to an increased
energy turnover and decreased efficiency.
This is illustrated by considering the schematic relationship between
mechanical efficiency and velocity as shown in
Fig. 5. The solid line
represents the efficiency/velocity relationship under control conditions. In
this schema, we have assumed that 60 revs min-1 (point a) is around
the optimum velocity for maximal efficiency, i.e. the velocity at which the
cross-bridge cycling rate is close to the required rate of actinmyosin
movement. Heating the muscle will increase the cross-bridge cycling rate,
shifting the efficiency/velocity relationship to the right (as shown by the
dashed line in Fig. 5). As a
consequence, the mechanical efficiency will be reduced at 60 revs
min-1 (point b), i.e. energy turnover for a given mechanical output
delivered will be increased. This shift in the efficiency/velocity
relationship of course reflects the change in the force/velocity relationship
of muscle that occurs when temperature is elevated
(Ranatunga, 1984). It should
also be noted that the shift is analogous to the difference in the mechanical
efficiency/velocity relationship between slow and fast muscle
(Woledge, 1968
;
Goldspink, 1978
;
Reggiani et al., 1997
;
He et al., 2000
).
|
In contrast to the effects seen at 60 revs min-1, our experiments show that during exercise at 120 revs min-1 energy turnover was lower after muscle temperature had been elevated. In the schematic illustration shown in Fig. 5, a pedalling rate of 120 revs min-1 lies to the right of the optimum velocity for maximum efficiency under normal conditions (point c), i.e. on the descending right limb of the efficiency/velocity relationship. Consequently, the effect of heating the muscle, as shown by the dashed line, is to shift the efficiency/velocity relationship to the right so that optimum velocity occurs at a higher pedalling rate and efficiency at 120 revs min-1 (point d) is increased.
In this Discussion, we have been concerned with the effect of local heating
on the energy turnover of the active muscles as a whole. Thus, changes in the
efficiency/velocity relationship refer to a `global' relationship of the
involved muscles and the recruited fibres of those muscles that have diverse
contractile and metabolic properties. It has not been possible to determine
the pattern of fibre type recruitment in the present experiments.
Nevertheless, at an exercise intensity of 85 % of
O2max at 60 revs
min-1, the power required probably represents less than 50 % of the
maximal power available at that velocity of contraction
(Greig et al., 1986
) (see
Sargeant and Jones, 1995
). It
is probable that the majority of the power required in those experiments could
be generated by type I muscle fibres acting alone if motor units were
recruited purely on a hierarchical size principle without any modulation due
to rate coding, i.e. a change in force generated due to the frequency of
stimulation (Sargeant, 1999
).
It is clear, however, that while the hierarchy of motor units is the major
determinant of recruitment there is some element of rate coding, as indicated
by studies of metabolic intermediates and glycogen depletion
(Greig et al., 1986
;
Ivy et al., 1987
). Thus, even
during relatively low-intensity exercise, type II muscle fibres will be
active, albeit at low firing frequencies and thereby making a minor
contribution to force production and metabolic cost.
It has previously been suggested that, at a contraction frequency of 60
revs min-1 in cycling exercise, human type I fibres might be
operating close to their optimum for maximum efficiency
(Sargeant and Jones, 1995).
Thus, a temperature-induced shift to the right of the efficiency/velocity
relationship for the recruited fibre population, as proposed schematically in
Fig. 5, would lead to a
decrease in efficiency; i.e. energy turnover for a given mechanical power
output would have to increase. The increased rate of oxygen uptake and
increased blood lactate concentration observed following passive warming when
cycling at 60 revs min-1 are entirely consistent with this
suggestion.
At 85 % of
O2max at a
contraction frequency of 120 revs min-1, the type I fibres would
have remained fully recruited in accordance with the hierarchical pattern of
recruitment (see Beelen et al.,
1993
; Sargeant and Kernell,
1993
). However, at a contraction frequency of 120 revs
min-1, the type I fibres may normally operate on the descending
right side of the power/velocity relationship and therefore also of the
efficiency/velocity relationship
(Sargeant, 1999
). Following
heating and the subsequent shift to the right of the efficiency/velocity
relationship, the type I fibres may be closer to their optimum velocity for
efficiency, as suggested by point d in Fig.
5. Hence, efficiency will increase and energy turnover for a given
mechanical power output will decrease, as we have observed.
In the present investigation, we have examined the effect of prior passive
heating of the active muscle fibres on the subsequent energy cost during
dynamic exercise. It will be realised that muscle temperature can also be
expected to rise during exercise as a result of the liberation of metabolic
heat. A number of authors have speculated that the so-called `slow component'
of O2 seen
during sustained exercise is a consequence of an increase in muscle
temperature (for a review, see Gaesser and
Poole, 1996
). It has been suggested that this is due to a decrease
in mitochondrial efficiency with increasing temperature (e.g.
Brooks et al., 1971
). The
present data do not, however, provide evidence to support this hypothesis. At
60 revs min-1, there was a temperature-related increase in energy
turnover; in contrast, while cycling at 120 revs min-1 with the
same heating protocol, the situation was reversed and energy turnover
decreased. Furthermore it is notable that during recovery, i.e. when the
mechanical efficiency/velocity relationship is no longer a factor, the
O2-off kinetics
were not demonstrably different between the heated and control conditions,
either at 60 or at 120 revs min-1
(Fig. 2).
If muscle temperature affected mitochondrial efficiency, as proposed by
earlier authors, it might be expected that an elevated
O2 would be
observed during recovery when the muscle was heated. Of course, it is still
just possible that there is a temperature-related decrease in mitochondrial
efficiency, but that at 120 revs min-1 the effect of this on the
total energy turnover may be obscured by the magnitude of the proposed shift
in the efficiency/velocity relationship as a result of elevated temperature.
Recent data, however, have also suggested that elevated muscle temperature
does not contribute to the slow component of
O2 during heavy
exercise (Koga et al., 1997
).
Notwithstanding the underlying mechanism for the slow component of
O2, this will
affect the estimated efficiency. In the present experiments where the
O2-on kinetics
(and off-kinetics) appear similar regardless of temperature conditions,
efficiency was calculated in the sixth minute. It should be noted however,
that the absolute efficiency values would change if exercise were prolonged as
a result of the increased energy turnover characterised as the `slow component
of
O2 kinetics'.
It should also be realised that heating the legs can be expected to have an
effect on core temperature (which has not been measured in this investigation)
and may have energetic consequences for pulmonary
O2, although the
existing evidence is equivocal (e.g.
Nielsen et al., 1990
;
González-Alonso et al.,
1998
). In our investigation, the impact of heating the legs on
core temperature would be the same at both 60 and 120 revs min-1,
but the unique observation is that
O2 changed in
opposite directions depending upon contraction frequency.
In conclusion, we believe that, in these experiments, the effects of
heating on energy turnover reflect the dominant contribution of type I muscle
fibres to the external power output at both 60 and 120 revs min-1.
These observations may also help to explain why athletes adopt relatively fast
cadences during sustained high-intensity exercise
(Sargeant, 1994). At low
cadences, there would be an additional increasing energy cost as a result of
an exercise-induced increase in muscle temperature. In contrast, at high
cadences, the increase in muscle temperature during exercise will lead to a
reduction in energy cost and a greater efficiency of locomotion.
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Asmussen, E. and Bøje, O. (1945). Body temperature and the capacity for work. Acta. Physiol. Scand. 10,1 -22.
Beelen, A., Sargeant, A. J., Lind, A., De Haan, A., Kernell, D. and van Mechelen, W. (1993). Effect of contraction velocity on the pattern of glycogen depletion in human muscle fibre types. In Neuromuscular Fatigue (ed. A. J. Sargeant and D. Kernell), pp. 93-96. Amsterdam: Academy Series, Royal Netherlands Academy of Arts and Sciences.
Bennett, A. F. (1984). Thermal dependence of
muscle function. Am. J. Physiol.
247,R217
-R229.
Binkhorst, R. A., Hoofd, L. and Vissers, A. C. A.
(1977). Temperature and forcevelocity relationship of
human muscles. J. Appl. Physiol.
42,471
-475.
Brooks, G. A., Hittelman, K. J., Faulkner, J. A. and Beyer, R.
E. (1971). Temperature, skeletal muscle mitochondrial
functions and oxygen debt. Am. J. Physiol.
220,1053
-1059.
De Ruiter, C. J. and De Haan, A. (2000). Temperature effect on the forcevelocity relationship of the fresh and fatigued human adductor pollicis muscle. Pflügers Arch. 440,163 -170.[Medline]
Di Prampero, P. E. and Ferretti, G. (1999). The energetics of anaerobic muscle metabolism: a reappraisal of older and recent concepts. Respir. Physiol. 118,103 -115.[Medline]
Edwards, R. H. T., Harris, R. C., Hultman, E., Kaijser, L., Koh, D. and Nordesjo, L.-O. (1972). Effect of temperature on muscle energy metabolism and endurance during successive isometric contractions, sustained to fatigue, of the quadriceps muscle in man. J. Physiol., Lond. 220,335 -352.[Medline]
Forster, H. V., Dempsey, J. A., Thompson, J., Vidruk, R. and
Dipico, G. A. (1972). Estimation of arterial
PO2, PCO2, pH
and lactate from an arterialised venous blood sample. J. Appl.
Physiol. 32,134
-137.
Gaesser, G. A. and Poole, D. C. (1996). The slow component of oxygen uptake kinetics in humans. Exerc. Sports Sci. Rev. 24,35 -71.
Goldspink, G. (1978). Energy turnover during contraction of different types of muscles. In Biomechanics, vol. VI-A (ed. E. Asmussen and K. Jorgensen), pp. 27-39. Baltimore: University Park Press.
González-Alonso, J., Calbet, J. A. L. and Nielsen, B.
(1998). Muscle blood flow is reduced with dehydration during
prolonged exercise in humans. J. Physiol., Lond.
513,895
-905.
Greig, C. A., Sargeant, A. J. and Vollestad, N. K. (1986). Muscle force and fibre recruitment during dynamic exercise in man. J. Physiol., Lond. 371, 176P.
He, Z.-H., Bottinelli, R., Pellegrino, M. A., Ferenczi, M. A.
and Reggiani, C. (2000). ATP consumption and efficiency of
human single muscle fibres with different myosin isoform composition.
Biophys. J. 79,945
-961.
Ivy, J. L., Chi, M. Y., Hintz, C. S., Sherman, W. M.,
Hellendall, R. P. and Lowry, O. H. (1987). Progressive
metabolic changes in individual human muscle fibres with increasing work
rates. Am. J. Physiol.
252,C630
-C639.
Koga, S., Shiojiri, T., Kondo, N. and Barstow, T. J.
(1997). Effect of increased muscle temperature on oxygen uptake
kinetics during exercise. J. Appl. Physiol.
83,1333
-1338.
Maughan, R. J. (1982). A simple, rapid method for determination of glucose, lactate, pyruvate, alanine, 3-hydroxybutyrate and acetoacetate on a single 20 µl blood sample. Clin. Chim. Acta 122,231 -240.[Medline]
Minetti, A. E., Pinkerton, J. and Zamparo, P. (2001). From bipedalism to bicyclism: evolution in energetics and biomechanics of historic bicycles. Proc. R. Soc. B 268,1351 -1360.[Medline]
Nielsen, B., Savard, G., Richter, E. A., Hargreaves, M. and
Saltin, B. (1990). Muscle blood flow and metabolism during
exercise and heat stress. J. Appl. Physiol.
69,1040
-1046.
Rall, J. A. and Woledge, R. C. (1990).
Influence of temperature on mechanics and energetics of muscle contraction.
Am. J. Physiol. 259,R197
-R203.
Ranatunga, K. W. (1982). Temperature dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J. Physiol., Lond. 329,465 -483.[Medline]
Ranatunga, K. W. (1984). The forcevelocity relation of fast- and slow-twitch muscles examined at different temperatures. J. Physiol., Lond. 329,517 -529.
Ranatunga, K. W. (1998). Temperature dependence of mechanical power output in mammalian (rat) skeletal muscle. Exp. Physiol. 83,371 -376.[Abstract]
Reggiani, C., Potma, E. J., Bottinelli, R., Canepari, M., Pellegrino, M. A. and Stienen, G. J. M. (1997). Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat. J. Physiol., Lond. 502,449 -460.[Abstract]
Saltin, B., Gagge, A. P. and Stolwijk, J. A. J.
(1968). Muscle temperature during submaximal exercise in man.
J. Appl. Physiol. 25,679
-688.
Sargeant, A. J. (1987). Effect of muscle temperature on leg extension force and short-term power output in humans. Eur. J. Appl. Physiol. 56,693 -698.
Sargeant, A. J. (1994). Human power output and muscle fatigue. Int. J. Sports Med. 15,116 -121.[Medline]
Sargeant, A. J. (1999). Neuromuscular determinants of human performance. In Physiological Determinants of Human Exercise Tolerance (ed. B. J. Whipp and A. J. Sargeant), pp. 13-28. London: The Physiological Society/Portland Press.
Sargeant, A. J. and Jones, D. A. (1995). The significance of motor unit variability in sustaining mechanical output of muscle. In Fatigue: Neural and Muscular Mechanisms (ed. S. C. Gandevia, R. M. Enoka, A. J. McComas, D. G. Stuart and C. K. Thomas), pp. 323-338. New York, London: Plenum Press.
Sargeant, A. J. and Kernell, D. (eds) (1993). Neuromuscular Fatigue, pp.190 -191. Amsterdam: Academy Series, Royal Netherlands Academy of Arts and Sciences.
Stienen, G. J. M., Kiers, J. L., Bottinelli, R. and Reggiani, C. (1996). Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J. Physiol., Lond. 493,299 -307.[Abstract]
Woledge, R. C. (1968). Energetics of tortoise muscle. J. Physiol., Lond. 197,685 -707.[Medline]