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1 School of Human Movement Studies, Charles Sturt University, Bathurst, NSW 2795, Australia
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Abstract |
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40°C and 60% relative humidity. Before and immediately following the cycle protocol, subjects performed a series of 25 continuous isokinetic shortening and lengthening maximal voluntary contractions (MVCs) of the leg extensors and forearm flexors. Voluntary activation for shortening and lengthening contractions for the forearm and leg was assessed prior to and following the 25 MVCs by superimposing a paired electrical stimulus to the femoral nerve and the biceps brachii during additional MVCs. Exercise to exhaustion increased rectal temperature to 39.35 ± 0.50°C. Voluntary activation remained unchanged following the prehyperthermia endurance set of shortening and lengthening maximal contractions in both the forearm flexors and leg extensors. Similarly, voluntary activation remained at prehyperthermic levels for the single MVCs immediately following the cycle trial. However, by the time of completion of the posthyperthermia endurance contractions, voluntary activation had declined significantly by 5.87 ± 7.56 and 8.46 ± 9.26% in the shortening and lengthening phases, respectively, for the leg extensors but not for the forearm flexors. These results indicate that the central nervous system (CNS) reduces voluntary drive to skeletal muscle performing both shortening and lengthening contractions following exercise-induced hyperthermia. The reductions in voluntary activation were only observed following a series of dynamic movements, indicating that the CNS allows for initial and brief ‘re-activation’ of skeletal muscle following exercise-induced hyperthermia.
(Received 9 September 2004;
accepted after revision 8 December 2004; first published online 16 December 2004)
Corresponding author F. E. Marino: School of Human Movement Studies, Charles Sturt University, Bathurst, NSW 2795, Australia. Email: fmarino{at}csu.edu.au
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Introduction |
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Traditionally experimental work on muscular force, especially when it necessitates muscle or motor unit recording, has used constant-load isometric contractions. Isometric contractions, however, may not be representative of muscle activity and fatigue development during human locomotion (Green, 1995). In addition, it has been suggested that the recruitment order of motor units changes when subjects perform lengthening contractions (Nardone et al. 1989). Available data also suggest that the development of fatigue may be specific to contraction type (Tesch et al. 1990) and that the CNS regulates neuromuscular function differently depending on the type of contraction (Enoka, 1996). As such, it is unclear how the interaction between contraction type and whole body hyperthermia influences neural loading during repeated shortening and lengthening contractions.
Therefore, the purpose of this study was to examine the effect of whole body hyperthermia on the voluntary activation of exercised and non-exercised skeletal muscle performing shortening and lengthening contractions.
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Methods |
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and maximum heart rate were 21.9 ± 4.0 years, 75.6 ± 7.5 kg, 180.9 ± 5.6 cm, 58.8 ± 8.2 ml kg–1 min–1 and 187 ± 8 beats min–1, respectively. Experimental procedures
Subjects were required to attend the laboratory on two occasions. The initial visit involved familiarization with experimental procedures and equipment and the acquisition of descriptive data. Subjects also undertook a progressive incremental test to exhaustion for the determination of 
. A week later participants returned to the laboratory for the experimental session. Subjects were required to abstain from ingestion of alcohol, caffeine and tobacco for 24 h prior to each session.
Experimental sessions required subjects to perform a series of voluntary and evoked lengthening and shortening contractions of the leg extensors and forearm flexors prior to and immediately following exercise to exhaustion in a hot environment (39.8 ± 0.7°C; 60.0 ± 0.8% relative humidity). The exercise protocol involved cycling at 60% of 
on an electrically braked ergometer (Ergo-line 800S, Ergometric, Hamburg, West Germany). Cycling was terminated when power output could no longer be maintained for 20 s consecutively or upon reaching preset ethical limits of a rectal temperature of 40.5°C. On arrival subjects voided, were weighed nude and a rectal thermistor was inserted. Electromyographic (EMG) electrodes and a heart rate monitor chest strap were secured and subjects performed prehyperthermic muscle assessment. Skin thermistors were then attached and subjects entered the temperature-controlled room and mounted the cycle ergometer in preparation to cycle. Throughout all trials subjects were permitted to consume water ad libitum and were dressed in shorts and shoes. Immediately following exercise subjects were returned to the isokinetic dynamometer and muscle assessment procedures were repeated.
Muscle function assessment
Muscle function was assessed using an isokinetic dynamometer (Kin-ComTM, Chattanooga Group Inc., Hixon, TN, USA). Two crossover shoulder harnesses and a belt limited extraneous movement of the upper body across the abdomen. The axis of rotation for the dynamometer was visually aligned with the lateral epicondyle of the femur, with the lower leg attached to the lever arm at the level of the lateral malleolus. Lengthening and shortening contractions were performed isokinetically between 20 and 80 deg for lengthening contractions and between 80 and 20 deg for shortening contractions, with full extension acting as the reference point (0 deg). For the forearm flexors the axis of the dynamometer was aligned with the epitrochlea–epicondlye axis, with the forearm attached to the lever at the level of the styloid process. The range of motion of the elbow joint during contractions was from 75 to 165 deg for lengthening and from 165 to 75 deg for shortening contractions (full extension, 180 deg). During lengthening contractions of both the leg extensors and forearm flexors each subject maximally resisted the downward movement of the lever arm. Conversely, during shortening contractions each subject extended (leg extensors) or flexed (forearm flexors) as forcefully as possible. Subjects were instructed to maintain maximal torque throughout the range of motion.
Resting twitch properties, maximal torque and superimposed torque were obtained before and immediately following a series of 25 maximal endurance contractions, repeated for the forearm flexors and leg extensors in a counterbalanced fashion. All actions were produced in series (i.e. shortening followed by lengthening) and were performed isokinetically at 30 deg s–1, with the exception of the endurance contractions, which were performed at 60 deg s–1. Pilot work indicated that 25 continuous lengthening and shortening contractions performed in series at 30 deg s–1 was extremely difficult for subjects to complete. A percentage change in torque was calculated for the 25 endurance contractions using the following equation:
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Electrical stimulation
For assessment of muscle contractile properties, activation of the leg extensors and forearm flexors was achieved by percutaneous stimulation of the femoral nerve and biceps brachii motor point, respectively, using self-adhesive stimulating electrodes. The current was delivered via a stimulator (Digitimer DS7, Digitimer Ltd, Welwyn Garden City, Herts, UK) linked via a host computer to the data acquisition and analysis system using a paired square-wave stimulus with a width of 200 µs (400 V; 150–800 mA).
Twitch evoked at rest
To obtain resting twitch properties a custom-designed AMLAB (AMLAB Technologies Pty Ltd, Sydney, Australia) instrument triggered the stimulator at a constant 50 deg knee flexion and 120 deg arm extension as the muscle was passively shortened and lengthened (30 deg s–1). All twitches produced on the relaxed muscle were corrected by the resistive torque related to the weight of the relevant limb and lever arm and the passive viscoelastic forces. To find the appropriate corrections, torque was measured as the relevant limb was moved passively (30 deg s–1) without stimulation. Muscular relaxation was checked by the absence of the vastus lateralis or biceps brachii electromyogram signal. The stimulus was adjusted in incremental steps until no observable increase could be noticed in peak tension. The current was increased by another 20% to ensure supramaximal stimulation.
Superimposed twitch torque
Electrical stimuli were superimposed on maximal lengthening and shortening contractions by the same custom-designed AMLAB program at the same fixed angles as for passive twitch properties. During contractions, torque was changing over the entire range of motion as a consequence of length and lever arm changes and degree of activation. Torque was increasing at the point of stimulus during lengthening contractions and decreasing during shortening contractions. Therefore, superimposed twitch torque was calculated by deducting the twitch torque immediately poststimulus from the torque that would have occurred in the absence of the stimulus at that angular position. The torque without stimulation was estimated by linear extrapolation of the slope of the prestimulus voluntary torque beyond the point of stimulation (Fig. 1). This extrapolation has previously been shown to be accurate by Babault et al. (2001) because the torque–time curve is linear before stimulation. The period for extrapolation was calculated over 25, 50 and 200 ms for all subjects. As with previous investigations (Gandevia et al. 1998), no significant differences were found for extrapolation duration and so only results relating to the 200 ms duration were subsequently reported. This method based on extrapolation has been used previously for isometric, shortening and lengthening contractions (Allen et al. 1995; Gandevia et al. 1998; Babault et al. 2001).
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To calculate the level of voluntary activation during a contraction the torque elicited during the interpolated twitch, referred to as superimposed torque (corrected superimposed twitch torque + voluntary torque), was compared with the voluntary torque achieved during maximal efforts using the following equation:
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Electromyography
Electromyographic data were obtained using paired (8 mm diameter for lower limb and 4 mm diameter for the arm) Ag–AgCl bipolar electrodes (Biopac Systems Inc., Santa Barbara, CA, USA) connected to a terminal box linked to a data acquisition and analysis system (AMLAB Technologies Pty Ltd) and host computer. Electrodes were attached to the vastus lateralis and biceps brachii muscles with an electrode spacing of 20 mm. The electrodes were placed longitudinally on the muscle approximately halfway from the motor point area to the distal part of the muscle. EMG signals were sampled during the voluntary and evoked conditions with a gain of 800 and 1000 V V–1, for the vastus lateralis and biceps brachii, respectively, at a rate of 2500 Hz. Raw data were passed through a bandpass filter with cut-off frequencies of 19.835 and 411.427 Hz. The filtered EMG was subsequently smoothed using the root mean square (r.m.s.) calculated by linear averages extending over 125 data points. EMG amplitude was calculated over a 200 ms period corresponding with a 6 deg range of motion prior to the mid-point of shortening and lengthening actions.
Peak power output
Peak power output was determined using an electrically braked ergometer (Ergo-line 800S, Ergometric, Hamburg, West Germany). Following a brief warm-up at a self-selected cadence the test commenced at 100 W. The workload was increased by 50 W every 2 min until the subject could no longer maintain the required intensity (at a cadence of 80 r.p.m.). Subjects breathed through a two-way non-rebreathing valve (series 2700 large, Hans Rudolph, St Louis, MO, USA). Expired air passed through respiratory tubing to an automated gas analyser (Quinton Instrument Company, Bothell, WA, USA). The pneumotach (Hans Rudolph) and gas analysers were calibrated prior to analysis using a 3 l syringe and gases of known concentration. Expired air passed through a mixing chamber of 5.5 l volume and was sampled at 15 s intervals.
Thermoregulatory measurements
Rectal temperature (Tre) was monitored as an index of core temperature using a 12 gauge disposable thermistor (Mona-Therm, Millinkrodt Medical Inc., St Louis, MO, USA) inserted 10 cm beyond the anal sphincter. Skin temperature was assessed at four sites using thermistors (427 series, YSI, Yellow Springs, OH, USA) placed on the left side of the body. Skin and rectal thermistors were connected to an eight-channel telethermometer (Zentemp 5000, Zencor Pty, Victoria, Australia) and were monitored continuously and recorded at rest, at 5 min intervals during the hyperthermic protocol and at exhaustion. Mean skin temperature (Tsk) was calculated using the equation derived by Ramanathan (1964).
Heart rate and subjective responses
Heart rate (HR) was recorded using a chest transmitter strap and wristwatch receiver (Polar Electro Oy, Kempele, Finland). Heart rate was recorded at rest, at 15 s intervals during exercise and after the completion of exercise and transferred to a computer for analysis. Subjective ratings of perceived exertion (RPE) and thermal comfort were obtained at 5 min intervals during exercise using the scales of Borg (1982) and Bedford (1964), respectively.
Statistical analyses
Descriptive data were generated for all variables and are presented as means ±
S.D. Statistical analyses were performed with a factorial analysis of variance (ANOVA) for repeated measures on time (pre and post exercise-induced hyperthermia) x mode (shortening and lengthening contractions). Tukey's HSD post hoc test was performed to locate the source of significance. Student's paired t tests were conducted where appropriate. Pearson's correlation coefficients were undertaken to examine the relationship between terminal rectal temperatures, 
and subsequent neuromuscular performance. Significance was accepted when P < 0.05.
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Results |
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During the hyperthermic trial Tre increased continuously from 37.22 ± 0.23°C at the commencement of exercise to 39.35 ± 0.5°C at exhaustion (P < 0.001), resulting in an increase of 2.13°C. Similarly, Tsk increased from 31.68 ± 0.65°C at rest to 37.33 ± 1.07°C (P < 0.001) at exhaustion. In parallel with the increase in Tre, heart rate increased from 71 ± 7 beats min–1 at rest to 187 ± 10 beats min–1 at exhaustion (P < 0.001). Values for RPE from 10 ± 1 to 19 ± 1, P < 0.001 and thermal pleasantness (from 4.8 ± 0.7 to 7.0 ± 0, P < 0.001) increased throughout exercise.
Maximal voluntary contractions
Figure 2 shows the maximal torque during shortening and lengthening contractions for the leg extensors and forearm flexors before and after the initial endurance set of 25 contractions and before and after the second set of endurance contractions performed following exercised-induced hyperthermia. Pre-exercise maximal voluntary torque during shortening contractions of the leg extensors measured at a 50 deg constant angular position (131.75 ± 28.61 N m), was significantly less (P < 0.001) than maximal torque during lengthening contractions (200.81 ± 45.80 N m). Subjects were able to maintain similar torque levels for both shortening (120.26 ± 30.14 N m) and lengthening contractions (188.24 ± 41.95 N m) following the initial set of 25 contractions. However, the second set of 25 endurance contractions performed after exercise-induced hyperthermia resulted in significant changes in torque levels. Torque during shortening was reduced from 109.21 ± 30.20 to 89.77 ± 27.64 N m (P < 0.01) following the second set (Fig. 2A), while torque during lengthening declined from 159.97 ± 28.87 to 134 ± 48.02 N m (P < 0.001) (Fig. 2B). Maximal torque during shortening and lengthening contractions was also significantly reduced as a result of the cycle exercise, with initial posthyperthermic values being significantly lower than the initial prehyperthermic values (P < 0.001).
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EMG
Corresponding values for r.m.s. voluntary EMG are presented in Fig. 3. Vastus lateralis r.m.s. EMG during maximal shortening movements commenced at 0.25 ± 0.17 V and was significantly reduced by the completion of the second set of endurance contractions (P < 0.05; (Fig. 3A). Vastus lateralis r.m.s. EMG during lengthening movements was initially 0.35 ± 0.23 V, declining to lower levels at both the commencement (P < 0.05) and conclusion (P < 0.01) of the second set of endurance contractions compared to initial levels (Fig. 3B). Biceps brachii r.m.s. EMG displayed no change from initial values as a result of the endurance sets or the cycle protocol for either shortening or lengthening contractions (Fig. 3C and D).
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Subjects experienced greater reductions in torque during the endurance set performed in the leg extensors than in the arm flexors after exercise-induced hyperthermia for both contraction types. Both the pre- (P < 0.05) and posthyperthermic sets (P < 0.001) resulted in a significant decline in torque during shortening. However, the 13.66 ± 23.37% reduction during the initial set was significantly smaller (P < 0.05) than the 35.15 ± 17.11% decline experienced during the hyperthermic endurance set. Similarly, each set resulted in a significant (P < 0.01) decline in average torque during lengthening. Again, however, the 23.55 ± 26.48% decline experienced during the initial set was smaller (P < 0.05) than the 47.45 ± 15.02% reduction following exercise-induced hyperthermia. The percentage decrease in torque experienced pre- and posthyperthermia was comparable for shortening and lengthening phases. Finally, the averaged torque during shortening and lengthening contractions was significantly lower at the commencement of the second set of contractions when compared to the initial set (P < 0.05).
Subjects experienced significant reductions in average torque during both the pre- and posthyperthermic endurance sets for the shortening and lengthening modes performed for the forearm flexors (P < 0.001). However, the 41.89 ± 11.85% decline during the initial set of shortening contractions was not significantly different to the 36.40 ± 17.81% experienced during the hyperthermic set. Likewise, the 30.29 ± 20.32 and 32.66 ± 13.18% torque decrements for lengthening sets performed pre- and posthyperthermia, respectively, were not different. The decrease in average torque during endurance sets was similar for both shortening and lengthening phases. Finally, average torque at the commencement of the pre- and posthyperthermic sets was not significantly different.
Contractile twitch and neural propagation
Typical contractile twitch responses for the leg extensors and forearm flexors are illustrated in Figs 4 and 5, respectively. The peak tension evoked by relaxed muscles for lengthening movements of the leg extensors was 52.15 ± 10.45 N m, which was significantly greater than the 35.21 ± 7.62 N m elicited during shortening movements (P < 0.001). Peak tension during shortening was significantly lower than initial values following the cycle protocol (P < 0.05) and following the second endurance set (P < 0.01). There were no differences in peak tension during shortening contractions from the commencement to the conclusion of either the pre- or posthyperthermic endurance sets. Similarly, peak tension during passive lengthening was significantly reduced following the cycle protocol (P < 0.01) and following the second endurance set (P < 0.01) when compared with initial values. Again there were no changes in peak tension from the commencement to the conclusion of each set.
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Average rate of twitch torque development was significantly slower from initial to final values (P < 0.05) for the leg extensors and from initial to all other measures (P < 0.001) in the forearm flexors when performing lengthening contractions. No other differences were observed for either forearm flexors or leg extensors for average rate of twitch torque development, half-relaxation times or twitch contraction time. Peak-to-peak amplitude, duration and latency of the M-wave for biceps brachii and vastus lateralis showed no changes during any of the repeated measures.
Voluntary activation levels
Voluntary activation levels obtained in the forearm flexors and leg extensors for the two contraction modes are presented in Fig. 6. The initial mean voluntary activation during maximal shortening contractions of the leg extensors (89.69 ± 5.31%, range 80.99–98.53%; Fig. 6A) was comparable with levels achieved during maximal lengthening contractions (92.76 ± 3.63%, range 85.25–98.43%; Fig. 6B). Voluntary activation remained unchanged following the initial endurance set of contractions for each contraction mode. Similarly, voluntary activation immediately following the cycle protocol was not significantly altered when compared to the levels achieved prior to the inducement of hyperthermia. However, the endurance set performed following the inducement of hyperthermia resulted in a significant decline in voluntary activation in both contraction types. Initial postcycle exercise activation while shortening was 88.51 ± 5.23% (range 78.43–95.20%), which declined to 83.82 ± 5.23% (range 60.76–93.97%) following the second endurance set (P < 0.05; Fig. 6A). Initial postcycle exercise activation during lengthening was 90.74 ± 3.87% (range 82.87–96.63%), which declined to 84.30 ± 9.88% (range 61.21–93.21%) by the completion of the second set (P < 0.05; Fig. 6B). While the overall decline in activation during shortening (5.87 ± 7.56%) was less than that experienced in the lengthening mode (8.46 ± 9.26%), this difference was not significant.
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Correlation between terminal rectal temperature, 
and voluntary activation
Rectal temperatures at exhaustion were poorly correlated with voluntary activation at the completion of the trial for both shortening and lengthening contractions of the leg extensors (r
=
–0.21 and r
=
–0.23, respectively, P > 0.05) and the forearm flexors (r
=
–0.38 and r
=
–0.23, respectively, P > 0.05). In addition, 
was poorly correlated with voluntary activation for both shortening and lengthening contractions of the leg extensors (r
=
–0.18 and r
=
–0.43, respectively, P > 0.05) and the forearm flexors (r
=
–0.54 and r
=
–0.16, respectively, P > 0.05). To confirm this observation further, subjects were grouped for comparisons according to those who terminated exercise at rectal temperatures above (higher temperature) or below (lower temperature) 39.5°C. The terminal rectal temperature of the higher temperature group (39.8 ± 0.4°C; n
= 4) was significantly greater than that of the lower temperature group (39.0 ± 0.1°C; n
= 9, P < 0.05). However, there were no significant (P > 0.05) differences in the voluntary activation achieved between the two temperature groups from the commencement to the completion of the trial for either the shortening or lengthening contractions for either the leg extensors or the forearm flexors.
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Discussion |
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Changes in maximal torque observed in the forearm flexors during the trial occurred following each of the endurance sets. Those changes in maximal torque were probably the result of peripheral fatigue; that is, a failure within the contractile apparatus of the muscle. This was evidenced by the changes in peak tension developed during the passive twitch before and immediately following the completion of each endurance set. The reductions were unlikely to be caused by failure in neural drive because no significant alterations in voluntary activation as assessed by twitch interpolation were observed. To further corroborate this possibility, there was also no significant alteration in voluntary EMG. Torque levels achieved in the forearm flexors prior to each endurance set were not different, indicating that by the commencement of the second endurance set this muscle group had recovered from the initial endurance set and, as expected, experienced no further effects as a result of the cycling protocol. These findings are supported by a restoration of the passive twitch and maintenance of voluntary activation similar to initial values for the commencement of the second set of endurance contractions.
The leg extensors experienced significant reductions in maximal torque following the second endurance set performed after exercise-induced hyperthermia. The small but non-significant reduction in torque by the completion of the initial set could be attributed to peripheral factors relating to failure within the contractile apparatus of the muscle and not a reduction in neural drive. This is confirmed by both a reduction in the size of the passive twitch and a lack of change in either voluntary activation levels assessed using twitch interpolation or voluntary EMG prior to and immediately following the initial endurance set. Similarly, the second endurance set induced peripheral alterations which altered torque output. In contrast to the initial set, the second set, which was performed after exercise-induced hyperthermia, led to significant alterations in neural drive as evidenced by a reduction in both voluntary activation and voluntary EMG.
The reduction in peak torque which occurred in the leg extensors immediately following the endurance trial appeared to be the result of a further development in peripheral fatigue, which was confirmed by a further reduction in tension developed during the passive twitch immediately following the completion of cycling. Surprisingly, during lengthening the twitch tension was reduced following the completion of the cycle trial, which was unexpected given that cycling involves minimal eccentric activation. Sahlin & Seger (1995) have previously observed reductions in lengthening MVCs following cycling. Therefore, previous and present findings suggest that muscle function impairment, whether central or peripheral in nature, may not be specific to the type of exercise performed.
Voluntary activation levels at the commencement of the trial for both the leg extensors and forearm flexors in each phase were similar to those observed in previous investigations for similar angular velocities and stimulation angles (Allen et al. 1995; Babault et al. 2001). A novel finding was that the CNS appears to reduce the neural output to the exercising muscle group (leg extensors) performing the shortening and lengthening contractions. It has been suggested that neural downregulation does not occur during dynamic contractions (Nielsen & Nybo, 2003). This assumption is based on the lack of change in amplitude or mean spectral frequency of the EMG signals from the vastus lateralis during dynamic exercise with progressively developing dehydration and hyperthermia (Ftaiti et al. 2001; Nybo & Nielsen, 2001). However, voluntary EMG is relatively insensitive to small changes in neural drive and motor unit recruitment cannot be tethered to a maximal output (Gandevia et al. 1992), suggesting that conclusions based on EMG data alone are limited.
The alterations observed in maximal torque, endurance performance and voluntary activation were consistent across contraction type (shortening versus lengthening). But this does not preclude the possibility that the lengthening phase may experience greater neural downregulation during hyperthermia. Indeed, nine of the 13 subjects showed a greater reduction in neural drive during lengthening contractions following the inducement of hyperthermia when measured by the twitch interpolation method. Similarly, 11 of 13 subjects experienced a greater reduction in voluntary EMG during muscle actions which involved lengthening following exercise-induced hyperthermia. Clearly, further research needs to be conducted to establish the effect of exercise-induced hyperthermia on neural drive to muscles contracting in various ways. This is particularly important given that small activation differences between contractions, even in the magnitude of the 2.6% differences observed here, are indicative of large changes in motoneuronal excitation (Herbert & Gandevia, 1999).
Interestingly, subjects were able to regain full activation to the leg extensors immediately posthyperthermia. Thereafter, there was a significant reduction in voluntary drive when performing a series of repetitive shortening and lengthening muscle movements. These findings support recent observations made by Cheung & Sleivert (2004), who found no reduction in force for two brief isokinetic MVCs performed following passively induced hyperthermia. Thus, it would appear that during brief contractions, force and activation are well preserved, whereas the ability to sustain these levels seems to be impaired during dynamic contractions. This may also hold true for isometric contractions. Nybo & Nielsen (2001) also observed no initial reduction in voluntary activation following exercise-induced hyperthermia but when the contraction was maintained over the subsequent 120 s period activation was attenuated. In contrast, Saboisky et al. (2003) observed an immediate reduction in neural output to the exercised (vastus lateralis) muscle group during a 5 s isometric contraction. The reason for this discrepancy remains unclear but may involve the difference in the type of contraction (isometric versus anisometric).
The present results are in contrast to those of Nybo & Nielsen (2001), who ‘inferred’ a reduction in neural drive to non-exercised muscle groups from force data which indicated reduced output. However, that investigation did not use twitch interpolation or EMG on the non-exercised muscle group and evidence for definitive changes in voluntary drive was not provided. However, Morrison et al. (2004) showed reductions in voluntary activation of 11% when core temperature was increased to 39.4°C by passive heating. Differences in results for the non-exercised limb might be attributable to different contraction modes. The previous investigations which have attained differences in non-exercised muscle have used long-lasting (at least 10 s) isometric contractions. Cheung & Sleivert (2004) showed that during isokinetic knee extensions peak torque was not altered when rectal temperature was increased to 39.5°C. It follows that these findings suggest that no change in voluntary activation occurred. The authors suggested that the effects of hyperthermia on force production may be dependent on the mode of exercise or alternatively that hyperthermia may only attenuate the ability to sustain maximal force for a short period of time. Hence, it is likely that for anisometric contractions it is the interaction between previous activation history and changes induced by hyperthermia that is responsible for the reductions observed in torque and voluntary activation.
However, the present study has some limitations. While the forearm flexor muscle group effectively acts as a passively heated control and allows us to conclude that hyperthermia is not the only cause of the reduction in neural drive to the leg extensors during lengthening and shortening contractions, it does not preclude the possibility that this reduction was caused entirely by the cycling exercise. Millet & Lepers (2004) have recently suggested that reductions in neural drive after prolonged running are evident, but similar central changes do not exist or are of lower amplitude for cycling or skiing. Cycling exercise involves mainly concentric contractions and therefore induces lower muscular damage compared with running. For cycling exercise, central fatigue has not been detected (Lepers et al. 2000; Millet et al. 2003) or was lower (Lepers et al. 2002) compared with running. Despite this limitation the present study provides important information about the neural control of skeletal muscle performing lengthening and shortening contractions.
Another limitation may be the nature of the sample. For example, the present study used a more heterogeneous group of subjects than was used by Nybo & Nielsen (2001). Maximal oxygen consumption was 58.8 ml kg–1 min–1, which is substantially lower and more variable than that reported by Nybo & Nielsen (2001; 65 ml kg–1 min–1). Subjects also reached a higher terminal core temperature in the study by Nybo & Nielsen (2001; 40.0°C) compared to the present study (39.3°C) despite the fact that every individual in the present experiment showed an increase of at least 1.8°C. Several authors have shown that a high level of cardiorespiratory fitness is associated with an improved exercise heat tolerance (Henane et al. 1977; Havenith & van Middendorp, 1990; Cheung & McLellan, 1998). Given this relationship, it is possible that those who were aerobically fitter and so reached higher terminal rectal temperatures may have experienced different responses in voluntary activation to the exercised and non-exercised limb. For example, those subjects who reached higher core temperatures may have displayed a decrease in forearm flexor function that was not evident in those that achieved smaller increases in rectal temperature. Hence, we assessed the interaction between terminal rectal temperature and voluntary activation changes. On balance, however, the correlation analyses between rectal temperatures at exhaustion and voluntary activation were low, so it does not seem likely that terminal rectal temperatures per se, either above or below the common critical limiting temperature of 39.5°C, or peak aerobic capacity are the primary reasons for a reduced motor command. Rather, it seems that rising temperature alone might be responsible for the reduction in efferent drive during exercise-induced hyperthermia.
It is still unknown what input is responsible for alerting the CNS to the impending dangerous development of hyperpyrexia to begin altering efferent command to skeletal muscle. Since force inhibition occurred only to previously exercised and not to the non-exercised muscle, it appears that localized alterations in certain stimuli played a role in afferent feedback and subsequent neural downregulation. One likely mechanism is reflex inhibition of the motoneurone pool caused by alterations in the firing rates of small-diameter motor afferents. Several investigations have shown reflex inhibition of the motoneurone pool related to muscle fatigue (Woods et al. 1987; Garland, 1991). The mechanism underlying this reflex is believed to be associated with activity of small-diameter type III and IV afferents (Bigland-Ritchie et al. 1986; Garland, 1991). One possible factor may be the localized alterations in muscle temperature. Although not measured in this study, muscle temperature has been shown to exceed core temperature at all but very low workloads (Saltin & Hermansen, 1966). Previous investigations have found that group III and IV muscle afferents increase their firing rate in response to heat (Hertel et al. 1976; Kumazawa & Mizumura, 1977; Mense & Stahnke, 1983). However, Ray & Gracey (1997) indicated that exercise in conjunction with rising localized muscle temperature led to differential activation of mechanosensitive (group III) and not metabosensitive (group IV) muscle afferents. The present findings indicate that the ‘exercising’ leg extensors may provide feedback via selective sensitization of group III afferents due to: (1) a higher metabolic heat build-up when compared with non-exercised forearm flexors; and (2) changes in the chemical milieu, which interacts with the metabolic heat to produce discharge of mechanosensitive afferents preferentially.
Increased afferent feedback as a result of the increased muscle temperature may not protect the muscle itself but may provide advance warning of impending danger to vital organs. It has been suggested that physiological changes leading to reduced CNS drive need to occur in anticipation of reaching the critical limiting temperature (Marino et al. 2004). Since muscle temperature increases in advance of core temperature, it would provide an ideal anticipatory mechanism to alert the CNS of impending thermal load and to adjust motor efferent command to active skeletal muscle accordingly.
In conclusion, this study provides evidence that the ability to activate skeletal muscle is adversely affected following exercise-induced hyperthermia when performing a series of shortening and lengthening contractions. Previous research has only been attempted using isometric contractions. The reduction in neural output was only observed in the exercised muscle group, confirming that core temperature per se is probably not the only cause of the reduced central drive to muscle. Furthermore, the differences in activation levels were only observed in the exercised limb following a series of dynamic movements, which indicates an ability to ‘re-recruit’ skeletal muscle for brief periods even after the attainment of high internal temperatures.
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) and after (
) the completion of endurance sets performed pre- and post -hyperthermia. Values are means ±
S.D., n
= 13. *P < 0.05, **P < 0.01, ***P < 0.001.
