The effects of the circadian rhythm (over the 24 h of the complete circadian cycle) and the time of day (only daytime) on short-term performance have been well established. In temperate conditions, maximal performance is generally improved by the end of the afternoon, at the peak of the body temperature curve (7,9,11,19). Some studies have suggested that the simultaneous increases in both body temperature and muscular performance are causally related, and that the circadian rhythm of body temperature could be regarded as a passive warm-up effect (3,5,15). In parallel with the diurnal variation in body temperature, a variation in environmental temperature can also influence muscle performance by a passive warm-up effect (8,13). In a previous study conducted in a tropical environment, we failed to show any daytime variation in muscle performance. That suggests that the passive warm-up effect of the moderately warm and humid environment may have blunted the passive warm-up effect of time of day (17).
It was recently shown that muscular power displayed a significant diurnal increase in a neutral environment only, and that a 60-min moderately warm exposure increased muscular power in the morning only (18). That suggests that these two passive warm-up effects have no additional effect on the improvement in muscular power (18). The increase in muscular performance observed in the morning after a moderately warm exposure may be the result of (i) an improvement in muscle contractility, (ii) a modification in the central nervous command, or (iii) a combination of these two factors. The absence of additional effects of the diurnal increase in body temperatures and a warm exposure on the improvement on muscular performance suggests that the influence of each of these passive warm-up sources on local and central mechanisms of muscular contraction cannot be combined. That is, a ceiling of the possible beneficial effects of an increase in the body temperature is reached.
The purpose of this study was to verify whether a warm exposure and the diurnal increase in body temperature influence muscle contractility and central command the same way, and whether or not they could be combined.
Eleven male physical education students gave written informed consent to participate in this study after receiving a thorough explanation of the protocol. The study was approved by the local ethics committee. The mean (±SD) age, height, and body mass of the subjects were 26 (±4) yr, 1.79 (±0.1) m, and 67.9 (±10) kg, respectively. The subjects were classified as either “moderately morning type” (N = 1) or “neither type” (N = 10) from their responses to the self-assessment questionnaire of Horne and Östberg (12), which determines morningness–eveningness.
All subjects completed five sessions. The first session served to familiarize them with the required activities. The four following sessions were conducted in random order in the following conditions: morning/neutral, morning/moderately warm and humid, afternoon/neutral, and afternoon/moderately warm and humid. The mean laboratory temperature and humidity were 20.5 (±1)°C + 67 (±4)% and 29.5 (±0.8) °C + 74(±10) % for the neutral and moderately warm and humid conditions, respectively. The laboratory conditions were controlled by air-conditioning and an electric heater, and were recorded by an electronic thermometer–hygrometer (Novo 16755, Novo, France, precision 0.1°C). The morning experiments were conducted between 0700 and 0900 h, and the afternoon experiments were conducted between 0500 and 0700 h.
To assess the reliability of the experimental conditions, seven of the subjects (mean age 24.4 yr) were tested a sixth time in a control experiment performed a few days later (with a time delay corresponding to the time between the first and the last experiment of the four different sessions). The reliability experiment was performed in the morning/neutral conditions.
Sessions began with 60 min of rest in a seated position in either a neutral or a moderately warm and humid room. At the end of this period, rectal temperature (Trect) and muscular cutaneous temperature of the quadriceps femoris (Tskin) were measured by a clinical electronic thermometer (MT 1691 BMWC, Microlife Ltd, Taiwan, precision 0.1°C, insertion depth 2 cm) and a surface thermometer (Ecoscan, Eutech Instruments, The Netherlands), respectively.
After the acclimation rest period, subjects performed three maximal voluntary knee extensions (MVC) and one submaximal voluntary contraction each at 75%, 50%, and 25% of the MVC of the session. All the contractions lasted 5 s and were separated by a 2-min rest. Regarding the submaximal extensions at 75%, 50%, and 25% of MVC, the subjects were able to view the percentage of MVC being developed on a screen, with the target percentage to attain. The test session ended with two more MVC to verify the absence of fatigue (Fig. 1).
The subjects were seated on the edge of a padded bench approximately 1 m in height with a 2- to 3-cm gap between the back of the knee and the edge of the bench. The knee angle was set at 100°. The knee extension force was measured using a strain gauge connected between the stationary bench and the subject's ankle. The data were collected by an acquisition card (DAQ-Pad 6020E, National Instruments, Austin, TX) and analyzed using software developed in our laboratory with a LabVIEW interface (National Instruments). The force analyzed was the maximum strength generated during the three contractions before the submaximal contractions. Verbal encouragement was given throughout the session.
Electromyograms (EMG) were obtained using MP30 hardware (Biopac Systems Inc., Santa Barbara, CA) and BSL Pro Version 3.6.7 software (Biopac Systems Inc.). The electrical activity was recorded with two surface electrodes spaced 2 cm apart on the belly of the vastus lateralis. Before placing each electrode, the skin was lightly abraded and washed to remove surface layers of dead skin, hair, and oil. The impedances of the EMG collector were always lower than 10Ω and were not statistically different between test sessions. The skin was marked with indelible pen to aid the precision of subsequent electrode placement, so the markings remained for the duration of testing. The myoelectric signal was amplified and filtered (pass band 30–500 Hz, gain = 2000). All the contractions were isometric to avoid variations due to differences in muscle lengths. A recording is shown in (Figure 2.
The analyzed data were the root mean square (RMS) of the electromyographic activity during the MVC and the muscular contractility (MC = strength divided by RMS activity) during both maximal (MVC) and submaximal (75%, 50%, and 25% of MVC) contractions.
Each variable was tested for normality using the skewness and kurtosis tests with acceptable Z values not exceeding ±1. With the assumption of normality confirmed, parametric tests could be performed. The effect of ambient temperature on the time-of-day effect was verified by two-way analysis of variance with repeated measures (ANOVA 2R × 2R, time of day × environmental conditions). This analysis revealed the global effect of time of day, the global effect of the environmental conditions, and the effect of the interaction between time of day and the environmental conditions. When significant effects were noted with the two-way ANOVA, analyses were broken down into one-way ANOVA. Data are displayed as mean ± standard error of the mean and the statistical significance was set at P < 0.05.
There were no differences between the first three MVC and the last two of each test session. The control session did not demonstrate any statistical difference when the electromechanical parameters of the vastus lateralis were retested in morning/neutral conditions a few days later. The force values of the seven subjects who performed the reproducibility session were 751 (±65) N in the initial morning/neutral session and were 744 (±34) N in the reproducibility session in morning/neutral conditions.
Daytime and climatic changes in rectal and skin temperature.
The body temperature data are displayed in (Table 1. Trect (F = 25.200, df = 10, P = 0.001) and Tskin (F = 29.765, df = 10, P < 0.001) showed a significant diurnal increase and a significant Tskin increase after a moderately warm and humid exposure (F = 186.494, df = 10, P < 0.001). Trect failed to show a significant effect of climate but displayed an interaction effect between time of day and environmental conditions (F = 6.696, df = 10, P < 0.05).
Daytime and climatic changes in MVC.
We observed a significant increase in muscle force after a 60-min moderately warm and humid exposure (F = 8.870, df = 10, P < 0.05), and this increase tended (F = 4.184, df = 10, P = 0.068) to be dependent on time of day. These results were due to the significant increase in the morning MVC after moderately warm and humid exposure (F = 12.963, df = 10, P = 0.005), whereas MVC was independent of these environmental conditions in the afternoon (Table 2). A study of the percentage of diurnal variation (afternoon vs morning values) in MVC showed a significant effect of the environmental conditions on the diurnal increase in muscle force (Fig. 2, +12% in neutral conditions vs −3% in moderately warm and humid conditions, F = 5.815, df = 10, P < 0.05).
Daytime and climatic changes in electromyography activity during MVC.
Muscle activation, estimated by RMS activity, tends to display an interaction effect between time of day and environmental conditions (F = 4.586, df = 10, P = 0.058), but none of these factors showed any significant effect (Table 2).
Daytime and climatic changes in muscle contractility.
Skeletal muscle contractility (MC), estimated by the force/RMS ratio, showed both a significant environmental effect (F = 5.613, df = 10, P < 0.05) and a significant effect of interaction between time of day and the environmental conditions (F = 7.865, df = 10, P < 0.02). Post hoc analyses showed that MC significantly increased with time of day in the neutral climate (F = 11.547, df = 10, P < 0.01), but not in the moderately warm and humid climate. Moreover, MC was significantly enhanced (F = 14.470, df = 10, P < 0.005) in the moderately warm and humid conditions in the morning, but not in the afternoon (Fig. 3).
As observed during MVC, MC showed a significant effect of interaction (F = 9.500, df = 10, P < 0.02) between time of day and the environmental conditions when the contraction was performed at a high level (75%) of MVC (Fig. 3). This interaction effect was due to a significant diurnal increase in MC in neutral environment only (F = 7.346, df = 10, P < 0.05) and a significant increase in MC after a 60-min moderately warm and humid exposure in the morning only (F = 12.282, df = 10, P < 0.01). The interaction between time of day and environmental conditions was not statistically significant for MC at either 50% or 25% of MVC (Table 2).
The major finding of our study was an interaction effect of time of day and environmental conditions on the force/RMS ratio during a maximal isometric voluntary contraction. This effect suggests that muscle contractility was differently influenced by a moderately warm and humid exposure, depending on whether the tests were performed in the morning or in the afternoon, that is, depending on the initial level of body temperature.
The maximal effort testing would result in muscle damage and soreness, which would subsequently affect muscle performance. In this study, our subjects have performed two MVC at the end of each test session and the results did not show any fatigue effect after three MVC and three submaximal contractions. Furthermore, our test conditions were randomized and additional analyze did not show any order effect.
The EMG signal can be influenced by the position of the recording electrodes or by the environmental conditions. To avoid a displacement of the electrodes, we marked the skin with indelible pen; to avoid muscle displacement, our subjects performed an isometric contraction. Regarding the environmental conditions, Bell (2) concluded that the EMG/force relationship measured using surface electrodes may be influenced by ambient temperature, but the temperature exposures in his study covered a wider range than ours (30°C for Bell vs 9°C for us). To avoid any effect of environmental conditions on electrode conductivity, we recorded the impedances of the EMG collector in all test sessions and the skin areas of measurement were prepared accordingly (washed, shaved, abraded, and conductive gel was added). We thus assume that the results of this experiment were due to the variation in either time of day or environmental conditions, and not to methodological factors.
Our results showed a significant effect of the environmental conditions on the diurnal variation in knee extensor force (F = 5.815, df = 10, P < 0.05), with a diurnal variation of 12% in neutral conditions, which corresponds to the data of Callard et al. (4) and Gauthier et al. (11), but a diurnal decrease of 3% in moderately warm and humid conditions. These results were due to the significant increase in MVC in the morning after 60 min of exposure to a moderately warm and humid environment (F = 12.963, df = 10, P < 0.005), whereas MVC was independent of these environmental conditions in the afternoon (Table 2). This shows that muscle force was more sensitive to an external passive warm-up effect in the morning, when body temperatures are their lowest levels. However, muscle force does not seem to be sensitive to an external passive warm-up effect in the afternoon, when body temperatures are their highest levels. These observations were in accordance with the data of Cornwall (6), who observed a modification in maximal voluntary force after passive local cooling but not after passive local heating.
Gauthier et al. (10) explained the ∼8% (3.94% from mesor to peak) circadian variation in the torque developed during isometric contractions of the elbow flexors by diurnal fluctuation of both the central nervous system command (estimated by RMS activity) and the contractile state of the muscle (estimated by the force/RMS ratio, which represents MC). These authors suggested that the rhythm of muscle contractility seems to be dominant and responsible for the diurnal variation in isometric performance. In our study, as observed by Gauthier et al. (10), isometric force increases during the day in neutral climate (+12%), whereas RMS activity decreases (−11%, F = 13.467, df = 10, P < 0.01). These authors (10) suggested that the vulnerability of the organism is reduced by having the acrophase of different physiological parameters at different times. In our study as well, RMS activity displayed an opposite variation to MC. The body may well have a protective mechanism that compensates for a variation in the muscle contractile properties by an opposite variation in the central command.
To our knowledge, it was the first time that an interaction effect between time of day and environmental conditions (F = 7.865, df = 10, P < 0.02) was observed on muscle contractile properties. According to Gauthier et al. (10) and Martin et al. (14), MC was significantly greater in neutral climate in the afternoon than in the morning (F = 11.547, df = 10, P < 0.01). Furthermore, in the morning, MC was significantly increased in moderately warm and humid conditions in comparison with neutral environment (F = 14.470, df = 10, P < 0.005), whereas it did not vary in the late afternoon, which explains the lack of variation in MC in the moderately warm and humid conditions (Fig. 3). This model of evolution was the same as that previously observed by our group for dynamic exercise such as jump tests and cycle sprints (18), and this similarity suggests that the variations during the brief dynamic maximal exercise under the effects of both time of day and environmental conditions were the result of variations in skeletal muscle contractility. This hypothesis agrees with the results of Martin et al. (14), who observed a diurnal variation in isometric force developed by the adductor pollicis muscle, and attributed it to a modification in peripheral mechanisms. However, these authors advanced the hypothesis that these mechanisms were not only muscle temperature dependent but also controlled by the daytime hormonal fluctuations. Not enough data are currently available to explain the variation in muscle contractile state as a function of time of day or environmental climate. One theory advanced greater Ca2+ retention by the sarcoplasmic reticulum with a decrease in temperature (20,21). Moreover, Stephenson and Williams (22) concluded that calcium concentration and temperature have a substantial effect on force at temperatures below 25°C, with a decrease in the number of actomyosin interacting sites, but little effect at temperatures above 25°C. This ceiling would explain the increase in MC from the morning/neutral conditions (which shows the lowest values for both central and local temperatures) with either time of day or moderately warm temperature, whereas we failed to observe variation between the three other conditions. On the basis of the demonstrated relationship between the force produced by crossbridges and the concentration of inorganic phosphate (1,16), Martin et al. (14) suggested that circadian variations in intracellular inorganic phosphate could explain the changes in muscle contractility. At the present time, it is impossible to confirm exactly how the diurnal variations in temperature, or other factors such as hormones, influence muscle function.
The data on MC suggest that the effect of time of day and environmental conditions on isometric strength was due to peripheral modifications and not to changes in central factors like neural command. If we explain the variation in MC by a variation in muscle fiber concentration of calcium or inorganic phosphate, this would not influence MC during submaximal contractions, when the needs are lower. According to this hypothesis, the interaction of time of day and environmental conditions had a significant effect on MC during MVC and 75% of MVC (F = 9.500, df = 10, P < 0.02), but not during 50% and 25% of MVC (Table 2).
In summary, our data showed that both a warm exposure and the diurnal increase in body temperature influence muscle contractility to increase muscle strength, but that the improvement in muscle contractility after these two passive warm-ups cannot be combined to improve force to a greater level. That suggests that a ceiling of the possible beneficial effects of passive warm-ups is reached with either the diurnal increase in body temperature or a moderately warm exposure.
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