Endurance exercise performance is markedly reduced in hot compared with temperate environments. The mechanism underlying this response may involve hyperthermia as the independent cause of fatigue (21,32). During exercise in hot conditions, fatigue in trained humans has been associated with the attainment of a "critical" core temperature (∼40°C) (32,34) despite different initial temperatures and rates of heat storage (21). This decrement in performance is proposed to originate from a hyperthermia-induced inability of the central nervous system (CNS) to activate sufficient skeletal muscle to produce or maintain a required force (i.e., central fatigue) (33,34).
The influence of hyperthermia-induced central fatigue on force production has been evaluated during both brief and sustained maximal voluntary isometric contractions (MVC). Nybo and Nielsen (34) observed that after the development of exercise-induced hyperthermia, force production during a 2-min MVC declined in association with a progressive reduction in voluntary activation. In contrast, voluntary activation was maintained throughout an MVC after exercise in thermoneutral conditions. A similar response has been observed during passive heating, with force production and voluntary activation declining progressively with the rise in core temperature from 37.2°C to 39.5°C (30,45). A decline in voluntary activation reducing force production during moderate hyperthermia is also supported by isometric muscle function observations made after dynamic exercise (43). These findings indicate that force production is not limited by the attainment of a specific core temperature but throughout the development of hyperthermia. However, it has recently been demonstrated that voluntary activation and force production capacity decrease similarly during a 20-s MVC after a self-paced exercise in hot and cool conditions, despite differences in sustained power output and core temperature (35). The extent of decline in voluntary activation was shown to be maintained during the sustained MVC. As a result, part of the decrease in force was attributed to peripheral fatigue (i.e., alterations distal to the neuromuscular junction) (25,28). Nevertheless, the relative contribution of peripheral versus central factors limiting force production during passive and active hyperthermia remains unclear. Moreover, the "critical" core temperature at which fatigue occurs during prolonged constant-load submaximal exercise often coincides with significant cardiovascular strain. Several studies have reported heart rate (HR) at exhaustion in excess of 95% of maximum (HRmax) (9,21,44) and significant declines in central blood volume, stroke volume (SV), and cardiac output (Q˙) (21,42). During maximal exercise in thermoneutral and hot conditions, the attainment of HRmax and a decline in Q˙ are associated with impairments in blood flow and oxygen delivery to exercising muscles (19,31). As such, the increase in cardiovascular strain and decrease in maximal oxygen uptake (V˙O2max) associated with prolonged exercise in the heat (2) may represent the foremost factor precipitating fatigue.
The aim of the present study was to isolate the influence of exercise heat stress and passive heating on neuromuscular function. Force production capacity and voluntary activation were therefore evaluated during a sustained MVC of the knee extensors after passive and exercise-induced hyperthermia. Brief maximal handgrip flexion was also evaluated to determine the level of force a nonexercised muscle group can produce and to separate the influence of active versus passive hyperthermia on short-duration skeletal muscle performance. It was hypothesized that voluntary activation during the sustained MVC would decrease after both interventions and that the decrement in force production would be amplified after exercise. Our premise for this hypothesis is based on previous contractile activity contributing to peripheral fatigue. An additional aim of the study was to test the hypothesis that prolonged exercise in hot climatic conditions is limited by severe cardiovascular strain-the attainment of HRmax and declines in SV and Q˙, coupled with a decline in mean arterial pressure (MAP).
Eight endurance-trained (>250 km·wk−1) male cyclists unacclimatized to heat volunteered for this study. The age, body mass, height, V˙O2max, HRmax, body fat percent, and sum of seven skinfolds of the subjects were 31.1 ± 5.1 yr, 74.5 ± 5.6 kg, 177.5 ± 4.8 cm, 4.9 ± 0.4 L·min−1, 185.0 ± 11.7 beats·min−1, 7.9% ± 2.9%, and 54.4 ± 18.4 mm, respectively (mean ± SD). Participants were informed of the study protocol and risks before providing their written consent. The study was approved by the Human Research Ethics Committee of the University of Sydney (ref. No. 10433) and conformed to the current Declaration of Helsinki guidelines.
Before their participation in the hyperthermic intervention phase of the study, measures of body fatness (23), height, and nude body mass (Mettler ID1, Greifensee, Switzerland) were obtained from each subject. Maximal oxygen uptake was determined on an electronically braked SRM cycle ergometer (Schoberer Rad Meßtechnik, Jülich, Germany) in a thermoneutral environment (20°C, 40% relative humidity, and 10 km·h−1 air velocity). The subjects were required to cycle at four submaximal steady-state power outputs, each 5 min in duration, followed by an increase in power (25 W·min−1) until volitional fatigue. External power output and V˙O2 attained during the final minute of each submaximal workload were used to formulate a linear regression equation (V˙O2: power output) from which the workload for the hyperthermic exercise intervention was derived. Saddle and handlebar position were adjusted by the subject to their preferred cycling position and remained unchanged for all trials. Before and after the V˙O2max test, the subjects were familiarized with the MVC/electrical stimulation protocol by replicating the contractions to be performed during the experimental sessions. Most subjects had previously taken part in a study involving neuromuscular stimulation.
Each subject underwent two randomized hyperthermic interventions separated by 4-7 d. Before each visit, the subjects were asked to refrain from strenuous exercise and avoid the consumption of caffeine and alcohol for at least 24 h. Testing commenced at the same time of day and was performed in an identical environment (38°C and 60% relative humidity). On arrival at the laboratory (∼60 min before testing), subjects emptied their bladder, changed into cycling or bathing shorts, and inserted a rectal thermistor probe. They then sat resting for 30 min in a thermoneutral environment (20°C-22°C and 50% relative humidity) while being instrumented. A venous cannula was inserted into a ventral forearm vein and a resting blood sample was taken. The cannula remained in the vein until completion of the trial and was systematically flushed with saline after sample collection to maintain patency. After instrumentation, the subjects moved to a custom-built chair to perform the preintervention MVC (control). After completion of the MVC protocol, subjects entered the climate chamber, were weighed, and further instrumented with a skin blood flow laser sensor while sitting (∼5 min). They then either moved to the cycle ergometer to undertake the exercise-induced hyperthermia trial or sat resting in a hot water bath to elicit passive hyperthermia. On completion of each intervention, subjects were weighed, exited the climate chamber, and repeated the MVC protocol. This sequence was completed within ∼3 min of trial completion while subjects were covered with blankets to conserve heat and ensure that core temperature did not fluctuate.
Exercise-Induced hyperthermia (ExH).
Subjects mounted the cycle ergometer and began cycling at 150 W for 3 min to "warm up." Thereafter, power output was increased to 60% of V˙O2max (222.1 ± 26.5 W). Each subject was instructed to cycle until exhaustion, which was defined as the point of volitional fatigue or when power output could no longer be maintained at a cadence >60 rpm. An experimental end point rectal temperature (Tre) of 39.9°C was enforced to comply with the ethical approval and ensure subject safety. A fan was mounted to provide convective airflow at 10 km·h−1. Oxygen uptake and Q˙ were measured at 10, 30, and 45 min and at exhaustion. Venous blood samples were taken at the same intervals as the respiratory gas collections. Ratings of perceived exertion (RPE), thermal comfort scores, and MAP were recorded every 10 min, whereas HR, skin blood flow, and skin and rectal temperatures were recorded continuously.
Passive hyperthermia (PaH).
Passive hyperthermia to a Tre of 39.5°C was induced by sitting immersed to the upper chest in a water bath (40.7 ± 0.5°C). The cannulated arm remained dry as blood samples were collected at 37.5°C, 38.5°C, and 39.5°C. Oxygen uptake and Q˙ were measured at the same intervals, whereas MAP and thermal comfort were recorded every 0.5°C Tre elevation beginning at 37.0°C. HR, skin blood flow, and skin and rectal temperatures were recorded continuously.
Voluntary activation and force production were evaluated using percutaneous electrical muscle stimulation before and after each intervention. The force signals were amplified, sent through an A/D board and sampled at 200 Hz by data acquisition hardware and software (LabVIEW; National Instruments, Austin, TX). The protocol consisted of a 45-s MVC of the knee extensor muscle group. A 250-ms tetanus was superimposed at 100 Hz during the MVC with a maximum voltage of 400 V, using two oval carbon rubber electrodes (8 × 13 cm) placed proximally and distally on the quadriceps (35). The tetanus was superimposed at 15, 30, and 44 s at an intensity (300.6 ± 44.6 mA) established during the preexperimental session on the relaxed muscle by increasing the current via a high-voltage stimulator (Digitimer Stimulator DS7; Welwyn Garden City, UK). At this frequency, tetanic stimulation was limited by subject tolerance and terminated by request, or when force elicited ∼75% of MVC (12). The MVC was performed on a custom-built adjustable chair with the hips and knees flexed at 90°. Subjects were secured at the waist and across the shoulders and chest to prevent extraneous movement with the ankle attached to a force transducer (XTran Load Cell S1W; Applied Measurement, Sydney, Australia). During all MVC, the chair was reclined at an angle of 12° to enhance ventricular filling pressure and reduce the effects of transient hypotension after the hyperthermic interventions. The central activation ratio was used to calculate voluntary muscle activation as a percent by dividing the MVC force with the total force (i.e., the sum of MVC and superimposed stimulus amplitude) and multiplying by 100 (26). Motivation was maximized during all MVC by providing both a visual display of force production on a computer monitor and standardized verbal encouragement. Brief (2-3 s) maximal handgrip flexor force was calculated as the mean of three trials with a hydraulic hand dynamometer (Chattanooga Group, Inc., Hixson, TN) after each knee extensor MVC.
Rectal temperature was measured and recorded on a portable data logger (T-Logger; University of Sydney) as an index of core temperature by a thermistor probe (YSI 400 Series; Mallinckrodt Medical, Kansas City, MO) inserted to a depth of 12 cm past the anal sphincter. Skin temperature was measured at four sites using iButton™ temperature sensors/data loggers (Maxim Integrated Products, Sunnyvale, CA). Rectal and skin temperatures were sampled at 1-min intervals. The T-Logger and iButtons™ were calibrated before and after the study in a water bath with temperatures ranging from 15°C to 50°C with a calculated accuracy of ±0.05°C and ± 0.01°C, respectively. An area-weighted mean skin temperature (Tsk) was calculated from the four sites (40). Skin blood flow was continuously measured at the level of the right medioventral forearm and recorded via a laser-Doppler perfusion monitor (Moor Instruments Ltd., Devon, UK).
Expired respiratory gases were obtained using the Douglas bag method and analyzed for fractions of O2 and CO2 using zirconium cell-based O2 and CO2 sensors (Pm1111E and IrI507, respectively; Servomex, Sugar Land, TX). Cardiac output as measured via the CO2 rebreathing method (11), and SV was calculated using the Fick equation. HR was monitored telemetrically with a Polar transmitter-receiver (T-31; Polar Electro, Lake Success, NY), and MAP was recorded manually using a sphygmomanometer (Accoson, Essex, UK).
Blood glucose and lactate measurements were performed using heparinized capillary tubes and analyzed in duplicate using the automated glucose oxidase and lactate oxidase methods, respectively (EML 105; Radiometer Pacific, Copenhagen, Denmark). Hematocrit percentage and hemoglobin concentration were analyzed in triplicate (KX-21N; Sysmex, Kobe, Japan) and derived to determine percent changes in resting plasma volume (13). Values are reported as means for duplicate and triplicate measurements, respectively.
Hydration, RPE, and Thermal Comfort
Subjects were given 300 mL of water to drink before each trial and permitted to drink ad libitum during each experimental session. Body mass changes were evaluated after each trial to determine sweat production (37) and corrected for moisture loss due to the exchange of O2 and CO2 (29), fluid ingested, and sweat trapped in clothing. The subjects were also asked to keep a 24-h food diary before testing and replicate their diet before the second hyperthermic intervention. RPE were elicited using the Borg category scale (7), and thermal comfort was evaluated using the Bedford Thermal Comfort Scale (4). Subjects were instructed and familiarized with the scales before testing.
All statistical calculations were performed using Statistica 7.0. A two-way (time × trial) repeated-measures ANOVA was performed to test the significance between and within treatments. Where significant interaction effects were established, pairwise differences were identified using the Tukey HSD post hoc analysis procedure. Pairwise comparisons between Tre measurements were performed using Student's t-tests. An analysis of power using conventional α (0.05) and β (0.20) parameters indicated that eight subjects would provide sufficient power (48) to detect meaningful differences in neuromuscular function equal or greater to the coefficient of variation. This estimate was based on the calculated mean coefficient of variation for voluntary activation (5%) and force production (12%) of the first four subjects of the investigation. Force and normalized force contrasts were performed on 10 data points taken at 5-s intervals. The significance level was set at P < 0.05. All values are expressed as means ± SD unless otherwise indicated.
Time to exhaustion during ExH was 64.4 ± 13.9 min, whereas 44.9 ± 12.9 min was required to reach 39.5 ± 0.1°C in the PaH intervention. Initial Tre was similar between ExH and PaH increasing significantly throughout both interventions (Fig. 1A; P < 0.01). During PaH, Tre increased more rapidly and was significantly higher at 25, 30, 35, and 45 min (P < 0.01). At ExH exhaustion, Tre (39.8°C ± 0.3°C) was significantly higher than that of PaH (P < 0.05). Exercise was terminated prematurely at a Tre of 39.9°C in four of eight subjects to comply with ethical approval. There was no significant difference in the initial Tsk between ExH and PaH (Fig. 1B). From 5 min onward, Tsk was significantly higher during PaH (P < 0.01). The elevated Tsk partly reflects the skin temperature of submerged body segments on which an iButton™ was attached. Skin blood flow increased significantly under both conditions from rest to 10 min, after which time a plateau was reached (n = 7; P < 0.01). Skin blood flow was significantly higher at 10 min during ExH compared with PaH (Fig. 1C; P < 0.05). Hydration state was similar before each intervention as body mass was within 0.6 ± 1.0 kg. Body mass deficits (718.0 ± 375.6 and 687.5 ± 541.1 g) were similar between ExH and PaH, as were percent body mass loss (1.0% ± 0.5% and 1.0% ± 0.8%), fluid intake (1164.4 ± 505.5 and 885.3 ± 214.9 mL), and sweat production (1.7 ± 0.3 and 2.2 ± 1.1 L·h−1). RPE and thermal comfort ratings increased significantly from 11.6 ± 1.1 and 5.3 ± 0.4 at 10 min of ExH to 17.5 ± 1.6 and 6.9 ± 0.4 at ExH exhaustion, respectively (P < 0.01). Similarly, thermal comfort scores during PaH increased with the rise in Tre from 5.5 ± 0.5 at 37.0°C to 6.9 ± 0.4 at 39.5°C (P < 0.01).
Cardiorespiratory and hematological responses.
HR and V˙O2 rose significantly from 10 min to ExH exhaustion, whereas significant decreases in SV and MAP were noted (P < 0.05). Although a slight decline in Q˙ was observed throughout exercise, it was not significant (Table 1). During PaH, HR and Q˙ increased significantly relative to a rise in Tre of 37.5°C to 39.5°C, whereas MAP decreased (P < 0.05). Blood lactate increased significantly during ExH from 1.5 ± 0.4 mmol·L−1 at rest to 3.3 ± 1.3 mmol·L−1 at exhaustion (P < 0.01). During PaH, blood lactate levels remained low, increasing only from 1.3 ± 0.2 mmol·L−1 at rest to 1.8 ± 0.4 mmol·L−1 at completion. Final ExH blood lactate was significantly higher than that of PaH (P < 0.01). No significant difference was observed in blood glucose levels from rest (5.1 ± 0.8 mmol·L−1) to ExH exhaustion (5.1 ± 0.9 mmol·L−1). In contrast, a significant rise was noted during PaH from rest (4.8 ± 0.6 mmol·L−1) to completion (5.3 ± 0.5 mmol·L−1; P < 0.01). Plasma volume decreased significantly during both ExH and PaH, as a 7.6% ± 3.0% decline was noted after 10 min of ExH and a 4.3% ± 3.6% decrease observed at a Tre of 37.5°C during PaH (P < 0.01). Final plasma volume values indicated an 11.9% ± 3.7% (ExH) and 10.9% ± 4.4% (PaH) decrease compared with 10 min and 37.5°C measurements, respectively (P < 0.01).
Mean voluntary activation during ExH and PaH was significantly reduced compared with the preintervention control (Fig. 2; P < 0.01). Despite this pre/postintervention main effect, the extent (i.e., rate and degree) of decline in voluntary activation was maintained throughout the MVC (i.e., voluntary activation did not progressively decrease), and no difference was observed between or within treatments. Final voluntary activations of the knee extensors at 44 s were 91.3% ± 5.7% and 91.2% ± 6.8% during ExH and PaH, respectively. The mean force production after both ExH (437.9 ± 106.3 N) and PaH (445.8 ± 126.0 N) was significantly decreased from control (512.1 ± 104.3 and 497.4 ± 116.5 N) (Fig. 3; P < 0.01). Peak force during the initial seconds of the MVC was also depressed after both hyperthermic interventions (P < 0.01). When expressed as a function of normalized peak force (i.e., as a percentage; Fig. 4), a significantly greater rate of decline was noted throughout the ExH MVC compared with control and PaH (P < 0.05). The mean normalized force was 83.6% ± 8.0% of peak force before ExH but declined to 77.8% ± 9.8% after ExH (P < 0.05). In contrast, no difference was observed in mean normalized force production between control and PaH MVC (86.4% ± 10.5% and 88.0% ± 13.8%, respectively). Similarly, maximal handgrip flexor force was unaffected by ExH and PaH (Fig. 5). A slight decrease was noted during ExH from 434.2 ± 61.8 to 414.3 ± 50.4 N, whereas force was reduced from 421.8 ± 62.0 to 405.3 ± 53.6 N after PaH.
The purposes of this study were to isolate the residual effects of exercise versus passive hyperthermia on neuromuscular function during sustained and brief MVC and to investigate whether endurance performance in the heat is limited by an increase in cardiovascular strain. To our knowledge, we are the first to evaluate neuromuscular function in the same group of subjects during passive and active hyperthermia beyond a core temperature of 39°C. We have demonstrated that sustained maximal force production is significantly impaired after both ExH and PaH, but to a greater degree after ExH (Fig. 3). However, the novel findings of this study are that 1) central fatigue accounted for <42% of the total decrease in force production capacity and 2) voluntary activation was maintained at ∼90% throughout both hyperthermic MVC. Therefore, the loss of force production observed during hyperthermia originated from both central and peripheral factors, with the latter enhancing the rate of decline after exercise. In contrast, force production was unaffected during brief maximal handgrip flexion after either ExH or PaH. Moreover, we noted that volitional fatigue during submaximal exercise under heat stress was associated with the attainment of a maximum or near HRmax and declines in SV and MAP (Table 1). We speculate that the elevated thermal strain and concomitant cardiovascular strain are the main underlying factors that mediate this fatigue response by precipitating the attainment of limits to cardiac function (8,19).
Our findings indicate that CNS drive was significantly reduced after PaH and ExH (Fig. 2). However, they further indicate that voluntary activation did not progressively decline during the 45-s MVC of the knee extensors. When evaluating the additional decline in mean voluntary activation observed during PaH (4.3%) and ExH (4.8%) with that of force production, it can be estimated that central fatigue accounted for 41.5% and 33.1% of the 10.4% and 14.5% decline in force production during PaH and ExH, respectively (Fig. 3). The loss of force production capacity after PaH and ExH therefore cannot be fully attributed to impairments in CNS drive (25) because central and peripheral components to fatigue were present. Alternatively, Nybo and Nielsen (34) associated the decline in force production during a 2-min MVC of the knee extensors and nonexercised handgrip flexors to a decrease in voluntary activation after cycling to exhaustion. Compared with exercise in thermoneutral conditions, voluntary activation in the active limb declined progressively by 28% after exercise in the heat. As an additional component to the study, the authors compared handgrip flexor force during a 2-min MVC in two passively heated subjects to a core temperature of 39°C. Their results indicated that force production followed the same pattern of response as with exercise-induced hyperthermia (34). Although force production was compromised during the sustained MVC, no difference was observed between conditions at the onset of contraction. Interestingly, they also noted that knee extensor force production during 40 consecutive brief MVC was unaffected by hyperthermia. These findings corroborate previous observations in which heat stress did not alter force production in both exercised and nonexercised limbs during a brief MVC (32). Conversely, Saboisky et al. (43) reported that a decline in voluntary activation attenuated force production in exercised muscle during a brief (5 s) MVC under heat stress. However, nonexercised forearm flexors were unaffected by previous cycling to exhaustion at a core temperature of 38.8°C. Similarly, we observed no difference in the ability of the handgrip flexors to briefly produce high force outputs during ExH and PaH compared with preintervention control (Fig. 5). This is consistent with observations made after self-paced exercise in hot and cool conditions (35). The maintained force production capacity noted in nonexercised skeletal muscles during hyperthermia may relate to task dependency (17,39). During an MVC of short duration, CNS drive may activate sufficient motor units to generate a force similar to normothermia. Alternatively, variations in fiber composition between muscle groups could explain the ability of the smaller upper limb muscles to briefly generate high levels of force (5). Fast-twitch motor neurons, predominant in the knee extensors, have higher recruitment thresholds and are therefore more difficult to fully activate (5,22). However, various factors including a mixture of muscle fiber types (16), supraspinal modulation (38,47) and muscle wisdom (17) can contribute to confound the etiology of fatigue development. Nevertheless, our results extend the current understanding of neuromuscular function by demonstrating that similar levels of CNS drive can be attained and maintained when performing a sustained MVC during passive and exercise-induced hyperthermia.
Although it is suggested that the passive development of hyperthermia progressively reduces voluntary activation and maximal isometric force production (30,45), we have recently demonstrated a similar decrease in force during a sustained MVC after self-paced exercise in hot and cool conditions (35). Despite the presence of central fatigue and a Tre difference of 0.8°C at the termination of exercise, voluntary activation was similar between conditions and represented 20% of the decline in force production. This decline was therefore associated with central and peripheral fatigue, the latter possibly due to the influence of prior exercise on skeletal muscle metabolism (3,25,28), contractile function (6,47), and cellular integrity (1,18). The present study further illustrates the enhanced fatigability of previously active muscles, as ExH normalized force declined at a significantly faster rate than during PaH (Fig. 4). A possible explanation may lie with the 0.3°C difference in Tre, or change in muscle temperature. However, Tre during PaH was within the range in which CNS drive and force production have been shown to decline (30,43,45). In addition, although muscle temperature was not measured, Tsk was ∼1.6°C higher at PaH completion (Fig. 1B). Thus, the inability to sustain a rate of force production similar to PaH after ExH seems to originate from the combination of heat stress and previous contractile activity. Accordingly, because several subjects terminated the exercise prematurely, it may be argued that absolute work performed differed with those reaching volitional fatigue, which may have confounded the neuromuscular function results. However, the level of thermal and cardiovascular strain observed in the subjects terminating exercise because of ethical restrictions was near that of exhaustion. Along with RPE measures, it appears that fatigue was impending. Moreover, even in subjects volitionally terminating exercise, time to exhaustion and absolute work varied.
Cardiovascular strain and exercise.
Cycling at a constant load in the heat lead to severe cardiovascular strain with HR increasing >96% of HRmax at exhaustion. However, four of eight subjects attained a Tre of 39.9°C and had to be stopped because of ethical restrictions. In these subjects, HR was ∼10 beats·min−1 lower than HRmax (95%) when exercise was terminated. In the four remaining subjects who reached exhaustion (i.e., volitional fatigue), HR rose to 98% of HRmax. These results are consistent with previous observations of HR increasing to 97%-99% of HRmax at exhaustion in conjunction with a core temperature of ∼40°C (21). Along with the increase in HR, SV was significantly depressed, and blood lactate concentration significantly increased. The increase in HR was highly correlated with the rise in Tre (R2 = 0.99), which supports evidence linking the composite factors of thermal strain (i.e., an increase in core and elevated skin temperature) to an increase in cardiovascular strain (10,21,36,42). High Tsk and Tre combine to decrease the Tre-Tsk gradient and increase thermoregulatory skin blood flow requirements, creating a shift in blood volume that challenges the maintenance of MAP and Q˙ (41). Recent studies have highlighted the effect of a narrow Tre-Tsk gradient on aerobic performance in hot conditions and suggested that the displacement of blood to the skin results in a decrease in V˙O2max and increase in relative exercise intensity (14,24). Consequently, subjects exercise at a progressively increasing fraction of V˙O2max that cannot be maintained. Our results indicate a Tre-Tsk gradient of 2.8°C ± 0.7°C at exhaustion, which is consistent with the suggestion that a decrease in central blood volume and compromise in muscle perfusion may impair prolonged exercise in the heat (10,24). However, in the present study, the decline in Q˙ was not significant, possibly because of the four of eight subjects terminating exercise before volitional fatigue and not reaching a higher HR and lower SV. In the subjects reaching exhaustion, a higher HR was noted along with a reduction in Q˙. Correspondingly, a final RPE of ∼19.0 was observed in these subjects, compared with ∼16.5 in those having to prematurely terminate exercise. Changes in plasma volume and body mass losses of ∼1%, along with the maintenance of blood glucose, are consistent with euhydrated exercise in the heat and indicate that neither dehydration nor glycogen depletion were precipitating fatigue factors.
It has been shown that severe exercise leads to restrictions in systemic and locomotor muscle blood perfusion, vascular conductance, oxygen delivery, and aerobic metabolism (31), which cannot be compensated for by an increase in oxygen extraction (19). Under conditions of heat stress, when workload approaches V˙O2max, the impairment in oxygen delivery to locomotor muscle stems from a reduction in blood perfusion, secondary to declines in Q˙ and MAP (19). In contrast, fatigue during prolonged submaximal exercise in the heat has been associated with alterations in the CNS that lead to central fatigue (33,34). However, González-Alonso et al. (20) recently suggested that rather than a "critical" core temperature, fatigue during prolonged exercise in hot environments may be mediated by the interaction between hyperthermia and cardiovascular strain. Our observations of a rise in both thermal and cardiovascular strains agree with this suggestion (Fig. 1 and Table 1). In addition, although fatigue often coincides with a core temperature of ∼40°C in well-trained subjects during laboratory experiments, athletes have been observed to reach or exceed core temperatures of 41°C during sporting events with no signs or symptoms of heat illness (27,37). These differences in core temperature between laboratory experiments and sporting competitions may be attributed to differing levels of fitness, heat acclimation, exercise modality, motivation, and ethical constraints. Nevertheless, they question the relationship between an elevated core temperature and reduced CNS drive to locomotor muscle impairing aerobic exercise performance (15,27,46).
In conclusion, we clearly demonstrated that PaH and ExH are associated with significant declines in voluntary activation and force production during a sustained MVC. However, despite hyperthermia-induced central fatigue, voluntary muscle activation was not progressively impaired during the MVC in either condition. Moreover, voluntary activation was similar between ExH and PaH. In contrast, the magnitude of decline in force production capacity was significantly greater during ExH. The loss of force production therefore originated from both central and peripheral factors, with the combination of exercise and heat stress potentiating the decline. Alterations in the contractile properties of hot skeletal muscles as well as disturbances in muscle metabolism and cellular integrity are suggested as possible peripheral influences on force production. In addition, our results indicate that volitional fatigue during constant-load submaximal exercise in the heat is associated with an increase in cardiovascular strain. This may compromise the ability of the circulatory system to meet the increased demand for blood flow to the skin, exercising muscles, and possibly the brain.
This work was supported by the University of Sydney Faculty of Health Sciences.
There are no conflicts of interest to report.
No outside funding was received for this study.
The authors thank Dr. Mike White and Dr. Martin Lakie for their constructive technical comments regarding percutaneous electrical stimulation. The authors also thank all the subjects who participated in this investigation, as well as Fionnuala Crowe and Carol Finn for their help with data collection.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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