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Time-of-Day Effects on Short-Duration Maximal Exercise Performance

Abstract

Time-of-day dependent fluctuations in exercise performance have been documented across different sports and seem to affect both endurance and resistance modes of exercise. Most of the studies published to date have shown that the performance in short-duration maximal exercises (i.e. less than 1 min - e.g. sprints, jumps, isometric contractions) exhibits diurnal fluctuations, peaking between 16:00 and 20:00 h. However, the time-of-day effects on short duration exercise performance may be minimized by the following factors: (1) short exposures to moderately warm and humid environments; (2) active warm-up protocols; (3) intermittent fasting conditions; (4) warming-up while listening to music; or (5) prolonged periods of training at a specific time of day. This suggests that short-duration maximal exercise performance throughout the day is controlled not only by body temperature, hormone levels, motivation and mood state but also by a versatile circadian system within skeletal muscle. The time of day at which short-duration maximal exercise is conducted represents an important variable for training prescription. However, the literature available to date lacks a specific review on this subject. Therefore, the present review aims to (1) elucidate time-of-day specific effects on short-duration maximal exercise performance and (2) discuss strategies to promote better performance in short-duration maximal exercises at different times of the day.

Introduction

Circadian rhythms are responsible for temporal regulation of numerous physiological phenomena in the human body. At a molecular level, circadian rhythms are defined as a function of clock gene expression levels over a 24-hour period1. Clock gene expression levels throughout the day set up the pace of sleep-wake cycles, hunger, hormone production, body temperature, as well as other physiological functions2. In mammals, biological rhythms are driven by a central pacemaker located in the suprachiasmatic nuclei (SCN) of the hypothalamus. It consists of approximately 20 000 neurons that exhibit independent rhythms of firing rate and gene expression3. The core clock system of the SCN works as a self-sustained transcriptional/translational feedback loop, involving a set of four integral proteins that act as activators or repressors within the system4. In addition, there is a group of kinases and phosphatases that regulate their localization and stability5. Apart from the core clock system in the SCN, circadian clocks and clock-controlled output genes (CCGs) are also present in peripheral tissues such as the liver, heart, kidney, pancreas, adipose tissue and skeletal muscle6,7,8,9,10,11,12. In this sense, the main synchronizer of the internal clock is solar light13, but it is known now that other non-photic stimuli such as feeding, social contact or physical exercise do also modulate the transcriptional activity of clock genes14,15,16,17. Likewise, internal clocks also play important roles on human behavior, accounting for variations in resting levels of neuromuscular, sensory-motor and cognitive performance throughout the day18,19,20,21. Recently, high-throughput transcriptomic and metabolomic analyses in mice have demonstrated that the time of day is a crucial factor to amplify the effect of exercise on systemic energy homeostasis and metabolic pathways within skeletal muscle22. In addition, exercise capacity exhibit diurnal fluctuations in mice and humans between the early and late part of their active phase23, which suggests that the time of day is a major modifier of exercise capacity.

Time-of-day dependent fluctuations in exercise performance have been documented across different sports and seem to affect both endurance and resistance modes of exercise24,25,26,27,28,29,30. Whereas differences in endurance exercise performance might be as large as 26%25, strength performance may vary as much as 41% throughout the day30. Short-duration maximal exercises (i.e. less than 1 min - e.g. all-out sprints, maximal jumps or isometric contractions) comprise both modes of exercise and are characterized by higher locomotor requirements31 and anaerobic energy contributions32 than longer exercises. Thus, they represent a robust model to explore time-of-day effects on the musculoskeletal system. Previous studies have shown that performance in short-duration maximal exercises exhibits time-of-day dependent fluctuations with amplitudes up to 29.4% between the morning and evening hours24,33,34,35,36,37,38,39,40,41,42,43,44,45. Considering the large variation in short-duration maximal exercise performance throughout the day, it is clear that the time of day at which our athletes train or compete is not trivial. However, the literature available to date lacks a specific review on this subject. Therefore, the present review aims to (1) elucidate time-of-day specific effects on short-duration maximal exercise performance and (2) discuss strategies to promote better performance in short-duration maximal exercises at different times of the day.

Methods

The present article provides an up-to-date review of the literature about the effects of time of day on short-duration maximal exercise performance. Articles were searched via three online databases (PubMed, PubMed Central and Google Scholar; 1924–2019). The literature search strategy included a combination of free terms using the Boolean operators “AND” and “OR”. The free terms used in the search were: time-of-day, circadian, chronotype, strength, neuromuscular, resistance, endurance, aerobic, anaerobic, short-duration, performance, isometric, isokinetic, dynamic, morning, evening, afternoon and night. The full search term strategy that was used for each scientific database is outlined in the supplementary material.

The studies retrieved from the databases that fit the inclusion criteria were imported to EndNote Web Software (Thomson Reuters, New York, USA) where duplicated articles were identified and excluded. Then, the titles and abstracts of the remaining articles were reviewed. Articles were excluded at this initial screening phase if they did not mention any specific effect of time of day on exercise performance. If this information could not be ascertained from the title or abstract, the article’s full text was reviewed in the next screening phase to determine whether it fitted the eligibility criteria. After the initial title/abstract screening process, the full texts of all the remaining articles were assessed to select those that fitted the inclusion criteria. The inclusion criteria that were applied to original articles included: (1) the study explored the effects of time of day (over a 24-hour period) on one or more aspects of exercise performance; (2) the study assessed time-of-day effects on isometric, isokinetic and dynamic short-duration maximal (i.e. less than 1 min) exercises (3) the study assessed the effects of either acute or chronic interventions on time-of-day dependent fluctuations in exercise performance; (4) the study assessed either direct (i.e. peak and mean power, isokinetic peak torque, total work, jump height) or indirect (i.e. RPE, neuromuscular efficiency, markers or muscle injury) features of exercise performance; (5) the study was published in indexed journals and was available in English. As a result, a total of 66 original articles were selected out of 545 initial results. A flow diagram of the article selection process is also outlined in the Fig. 1.

Figure 1
figure1

Flow diagram of the article selection process.

Results

A total of 66 articles were selected and then divided into dynamic and/or isometric/isokinetic short-duration maximal exercises. Forty-four articles assessed time-of-day effects on dynamic short-duration maximal exercise performance, including swimming, tennis, jumping, cycling, sprinting and resistance exercises (Table 1). On the other hand, 32 articles assessed time-of-day effects on isometric and isokinetic exercise performance, including electrically induced contractions, reflex contractions, maximal and submaximal voluntary isometric contractions, isokinetic leg contractions and magnetic stimulation of the cortex (Table 2). Most articles compared time-of-day effects on short-duration maximal exercise performance under acute exercise conditions; however, 11 articles assessed time-of-day effects on short-duration maximal exercise performance after a period of training (from 5 to 10 weeks) (Tables 1 and 2).

Table 1 Summary of the literature about time-of-day effects on dynamic short-duration maximal exercise performance.
Table 2 Summary of the literature about time-of-day effects on isometric and isokinetic exercise performance.

Discussion

Effects of time of day on dynamic short-duration maximal exercise performance

In order to explore the influence of time of day on dynamic short-duration maximal exercise performance, several studies have assessed the presence of time-of-day dependent fluctuations in both continuous and intermittent exercises. Dynamic short-duration maximal exercise performance seems to oscillate consistently throughout the day, peaking in the afternoon (i.e. between 16:00 and 20:00 h) with amplitudes ranging from 1.7 to 17.5% (Table 1). Except for two studies33,46, better short-duration maximal exercise performances were found in the afternoon when single bouts of exercise were performed under neutral climate conditions. Short-duration maximal exercises that are influenced by the time of day include all-out swimming trials47,48,49, tennis services37,40, all-out cycling13,23,24,27,28,35,36,38,42,43,50,51,52,53,54, maximal jumps2,23,36,38,40,41,42,46,49,55,56,57, repeated sprint ability2,33,44,46,56,58,59,60,61,62, one repetition maximum (1RM) assessments63,64,65,66 as well as other force-velocity based tests35,40,49,54,62,63,67.

Neuromuscular differences in dynamic short-duration maximal exercise performance throughout the day has been explored using electromyographic (EMG) activity recordings. Castaingts et al.55 analyzed variations in force and EMG activity of skeletal muscles throughout the day as well as the ratio between these parameters (i.e. force/EMG activity) during a natural movement (i.e. drop jump). Such relationship between the force and EMG activity is called neuromuscular efficiency (NME). In this study, they observed a higher jump height and NME in the evening than in the morning, which indicates that the process of storage-release of potential energy in muscle elastic elements is improved in the evening, without a parallel increase in motor unit activation55. A further analysis of time-of-day fluctuations in power and EMG activity of vastus lateralis, rectus femoris, vastus medialis and biceps femoris muscles recorded in a repeated sprint exercise protocol (5 × [6 s of maximal cycling sprint + 30 s of rest]) showed that total work, percentage of peak power decrement and peak power were higher in the evening than in the morning, although it was not accompanied by a time-of-day effect on EMG activity levels44. Similarly, Chtourou et al.24 recorded EMG activity changes during a Wingate anaerobic test and showed that power output and NME were higher in the evening during the first phase of the test (i.e. first 20 s), where peripheral mechanisms of muscle contraction have the main role in exercise performance. Yet, they were independent of the time of day during the second phase of the test (last 10 s), where central mechanisms of muscle contraction have a higher role in exercise performance. Thus, since most studies have shown that changes in muscle function throughout the day are not accompanied by changes in EMG activity levels, it has been suggested that adaptations at the muscle fibre level rather than changes of the neural drive, motor unit properties, and/or muscle membrane properties are more likely to cause time-of-day dependent variations in dynamic short-duration maximal exercise performance66.

Other studies have also suggested the existence of peripheral mechanisms which might explain diurnal oscillations in dynamic short-duration maximal exercise performance. For instance, Hammouda et al.58 observed that the neuromuscular performance during a repeated sprint ability test (5 × [6 s of maximal cycling sprint + 24 s of rest]) was higher in the evening and it was accompanied not only by higher levels of biological markers of muscle injury but also a lower antioxidant status at this time of the day. Furthermore, Racinais et al.61 assessed time-of-day differences on repeated sprint exercise performance and found a better performance and higher blood lactate concentrations in the evening than in the morning. Although the physiological basis of these time-of-day dependent oscillations has not been elucidated, the evidence suggests the existence of a muscle specific mechanism that accounts for time-of-day dependent fluctuations in neuromuscular performance, whose activity is at least partially independent of the central nervous system.

Effects of time of day on isometric and isokinetic exercise performance

The performance in isometric and isokinetic exercises fluctuates throughout the day over a wide variety of muscles, with amplitudes ranging from 3 to 29.4% (Table 2). Greater amplitudes in isometric and isokinetic exercise performance were found at around 17:00–19:00 h. These observations included assessments of maximal voluntary isometric contractions26,29,30,33,34,36,39,41,45,55,65,66,68,69,70,71,72,73,74,75,76,77,78,79,80, isokinetic leg contractions54,70,72,76,81,82,83,84, handgrip strength35,72,76 and electrically evoked contractions26,29,39,55,75,79.

The time of day influences isometric and isokinetic exercise performance in both lower and upper extremities. Regarding lower extremities, Guette, Gondin and Martin26 found a significant time-of-day effect on maximal voluntary muscle contraction (MVC) peak torque of the quadriceps muscles on the dominant and non-dominant leg, with the highest values occurring at 18:00 h. Regarding upper extremities, Gauthier et al.77 observed a time-of-day dependent rhythm in elbow flexor torque, whose acrophase was reached at around 18:00 h. This was accompanied by a time-of-day dependent rhythm in biceps muscle EMG activity. Thus, it is clear that upper and lower limb muscle contractility in isometric and isokinetic actions is affected by the time of day. In this sense, most of the studies have shown that when the performance is assessed at a peripheral level by means of peak power, mean power or total work, then a typical peak in performance is found in the evening29,30,34,35,36,41,45,54,61,68,70,72,73,76,77,78,79,81,82,83,84,85.

However, the ability to generate force in isometric and isokinetic exercises depends not only on peripheral but also on central mechanisms of muscle contraction. Central mechanisms include central nervous system command, alertness and motivation, being them all normally assessed by electromyographic activity recording of skeletal muscles68. When muscle performance is assessed at central level, higher morning values77,79, higher evening values80 or no differences throughout the day26,29,66,82 are observed. Such differences in EMG activity throughout the day observed among different studies are difficult to be explained. However, many researchers suggest that EMG activity recordings can be affected by the muscle groups examined. Strikingly, time-of-day dependent fluctuations in maximal isometric and isokinetic performance seem to be different between fast and slow muscles of the lower limbs. In this sense, a decrease in MVC peak torque of triceps surae muscles and soleus muscle EMG activity was observed in the evening in comparison to the morning. According to the authors, this is probably due to a higher fatigue state of the slow motor units as the day progresses39,79. It is worth noting that methodological factors associated with EMG activity recordings might also account for differences in central mechanisms of muscle contraction throughout the day.

Finally, some studies have suggested that diurnal fluctuations in short-duration maximal exercise performance may be partially controlled by the individual circadian typology/chronotype. Thus, inter-individual differences related to the chronotype might generate opposite responses in central and peripheral mechanisms of muscle contraction throughout the day. Chronotype is an individual’s characteristic pattern that reflects preferences towards morningness or eveningness, and it is usually evaluated using self-assessment questionnaires. The effect of the chronotype on isometric and dynamic exercise performance has not been extensively studied, but some studies have shown the importance of the individual typology on isometric exercise performance. For instance, Kuusmaa et al.68 showed that morning-type (M-type) individuals exhibited lower force values in the evening whereas evening-type (E-type) individuals exhibited lower force values in the morning, despite the fact that EMG activities where not different throughout the day in either group. Tamm et al.75 reported that E-type individuals showed parallel increases in cortical and spinal excitability over the day, which were reflected on an increased triceps surae EMG activity and MVC torque at 21:00 h. However, M-type individuals exhibited the highest cortical excitability at 09:00 h but the highest spinal excitability at 21:00 h, without significant differences in triceps surae EMG activity or torque produced during MVCs over the day. Such discrepancies have led some scientists to the conclusion that EMG activity and MVC torque could increase, remain constant or even decrease throughout the day, thus reflecting an orchestrated response between peripheral and central mechanisms in the control of skeletal muscle contractile properties55.

General mechanisms of time-of-day effects on short-duration maximal exercise performance

Performances in short-duration maximal exercises follow a time-of-day dependent rhythmicity, peaking in the afternoon at around 16:00–20:00 h. This effect was observed in children and adults35,66 and among different sports disciplines40,49,50. Diurnal amplitudes in short-duration maximal exercise performance range from 1.7 to 29.4% depending on the muscle feature, muscle group and assessment method. According to the scientific literature published to date, it is clear that a better short-duration maximal exercise performance is achieved in the evening than in the morning in both dynamic13,24,27,28,30,35,36,37,38,40,41,42,43,44,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,67,85,86,87,88,89,90 and isometric/isokinetic26,29,30,33,34,35,36,39,41,45,54,55,68,70,71,72,73,75,76,77,78,79,80,81,82,83,84,85 exercise modes. However, these differences may be blunted in warm and humid environments56,62. This also happens when appropriate warm-up protocols are used57,59 or if music is listened to during warm-ups13,86. The same effect may take place if intermittent fasting conditions are imposed50,85 or if regular exercise training is performed at a specific time of day30,36,45,54,63,64,65,66,69,73,74,78.

Effects of temperature

Since short-duration maximal exercise performance fluctuates in parallel with body temperature56,62, it has therefore been suggested that body temperature affects the contractile properties, viscosity and conduction velocity of action potentials in skeletal muscle as well as the extensibility of connective tissue91. In fact, Racinais and Oksa92 have found a positive and linear relationship between performance and muscle temperature, where performance improves from 2 to 5% with a 1 °C increase in muscle temperature. Hence, several research groups have been devoted to studying the effects of getting exposed to warm or cold environments on short-duration maximal exercise performance at different times of the day. In this sense, it was observed that a 60-min exposure to a moderately warm and humid environment (i.e. 28.1–29.5 °C, 62.6–74% relative humidity) blunts the diurnal variation in muscle function that is observed in neutral climate conditions (i.e. 20–20.5 °C, 57–67% relative humidity)56,62,71. Conversely, immersion in cold water (i.e. 16–16.5 °C) before performance testing in the evening has shown to reduce the force and muscle power towards morning values60,72. This is achieved through a “passive effect” of thermal conditions on muscle temperature92. In addition to the passive effect of climate conditions on body temperature, time-of-day dependent variations in muscle performance might also diminish or even disappear when extended warm-up protocols are used (i.e. 20 min cycling on a stationary bike at 150–200 W prior to the completion of the regular warm-up)57. Diurnal fluctuations in performance also disappear under active (i.e. 12 min of pedaling at 50% of VO2max interspersed with three brief accelerations of 5 s) but not passive (i.e. 3 min of pedaling at 70 rpm at 50% of VO2max) warm-up conditions59. The same can be stated when longer active warm-ups (i.e. 15 min of pedaling at 50% of maximal power output) are compared with shorter ones (i.e. 5 min of pedaling at 50% of maximal power output)42. The effectiveness of these protocols to increase performance in the morning towards evening values is due to an “active effect” on muscle temperature92. Thus, increases in muscle temperature might help athletes to minimize diurnal dependent variations in short-duration maximal exercise performance. This can be achieved by means of short exposures to warm and humid environments as well as by the inclusion of active warm-up protocols (e.g. 12–15 min pedaling at minimum intensities of 50% VO2max and interspersed with sprint exercises) before exercising.

Finally, although there is strong evidence to support that time-of-day dependent fluctuations in short-duration maximal exercise are dependent on body temperature, it is clear that there are additional factors which might affect such fluctuations. In this sense, it should be noted that in moderately warm and humid climate conditions better performances are achieved in the morning, when body temperature is at its lowest. However, this is not observed in the evening56,62,71. In this regard, it seems that the effects of the time of day on body temperature and those of warm and humid climate conditions do not interact to potentiate exercise performance in the evening. According to some authors, this is due to the similar effects of both variables on neuromuscular efficiency59, although there is no data to support this hypothesis. On the other hand, it has been observed that an increase in rectal morning temperature towards evening values does not increase muscle strength levels in the morning towards levels found in the evening76,87,89. This might suggest that a specific mechanism within the muscle is orchestrating the effects of time of day on short-duration maximal exercise performance. It is also worth mentioning that when passive exposure to hot environments increases the central temperature towards values close to 39 °C, there is a reduction in the neural drive and the maximal voluntary activation of muscles. This will negatively affect power production and short-duration maximal exercise performance92.

Effects of music

In addition to peripheral factors, it has been suggested that central factors related to alertness, motivation and mood might affect short-duration maximal exercise performance at different times of the day13,28,33,86,93,94. It has been well established that an auditory stimulus, such as music, is effective in increasing levels of arousal, reducing levels of perceived exertion and facilitating a better motor coordination during short-duration maximal exercises94,95,96,97,98. In this regard, Chtourou et al.13 observed higher performances in the Wingate anaerobic test when it was performed after warm-up with music [10-min warm-up while listening high tempo music (>120–140 bpm) through headphones] in comparison to warm-up without music conditions. Furthermore, listening to music during the warm-up period blunted time-of-day dependent variations in muscle power output. This effect was achieved due to a greater increase in performance in the morning than in the evening. Interestingly, a recent study carried out by the same research group showed that this beneficial effect of music on short-duration maximal exercise performance can be achieved when the 10-min warm-up is performed either under neutral (i.e. non-selected) or self-selected motivational music conditions86. In the same study, a greater effect of music on short-duration maximal exercise performance in the morning than in the evening was reported. According to the authors, the ergogenic effect of music could be related to better individual perceptions of self-esteem and sense of confidence in the morning, where the level of motivation seems to be lower among individuals. Thus, listening to music during the warm-up period could be an effective strategy to improve short-duration maximal exercise performance, especially in the morning hours.

Effects of testosterone and cortisol

Short-duration maximal exercises produce an acute increase in both serum testosterone and cortisol levels, affecting the anabolic and catabolic status in skeletal muscle99. In addition, testosterone and cortisol are under circadian regulation, both peaking in the morning hours100. This has raised the question of whether the exercise-induced hormonal response can be influenced by the time of day. In this regard, Bird and Tarpenning101 found that a single session of heavy resistance exercise produced a lower cortisol response when performed in the evening compared with the morning, without affecting the diurnal rhythmicity of testosterone. This suppression in the cortisol response after resistance training in the evening hours was also observed by Burley et al.102. The authors proposed that this reduction in the testosterone/cortisol ratio leads to a reduced catabolic environment which could favor muscle adaptations to resistance exercise in the evening hours. Interestingly, Sedliak et al.73 observed that a 10-week training period at a specific time of day gradually reduced morning but not evening cortisol levels. The authors attributed these changes to a lower anticipatory stress and a better accommodation to early waking rather than any chronic change in cortisol diurnal rhythmicity. However, this period of training at a specific time of day was enough to blunt the time-of-day effects on strength performance in these individuals. Moreover, the absolute increase in maximum strength at the end of the training period was similar in all individuals regardless the time of day at which training was conducted.

It is worth mentioning that, although some studies have observed a relationship between hormone levels, short-duration maximal exercise performance and the time of day, there are other ones that have not so63,64,74. For instance, Kūūsma et al.64 observed no changes in the typical diurnal variations in resting serum testosterone and cortisol concentrations after a 24-week period of training at a specific time of day. According to the authors, the effects of a temporary phase shift caused after a prolonged period of training might explain these results. Furthermore, Sedliak et al.74 observed that resting cortisol levels declined independently of the time of day after 11 weeks of training at a specific time of day in untrained young males. However, they did not find changes in resting testosterone levels after the training period in such individuals. Likewise, no significant changes were observed in resting testosterone levels in a group of healthy older women after 12 weeks of training at a specific time of day63. In summary, whereas resistance exercise training periods at a specific time of day do not seem to affect the circadian pattern of testosterone secretion, their effect on cortisol secretion diurnal pattern is more controversial. Therefore, further research is required to elucidate the role of the time of day on the exercise-induced hormonal response.

Effects of circadian systems

Recently, a large-scale transcriptomic analysis has revealed the existence of rhythmic and CLOCK-driven pathways in human skeletal muscle that affect ~8% of muscle genes103. This analysis showed that the transcription of human skeletal muscle clock genes was distributed into two phases of transcript accumulation at 04:00 and 16:00 h. The afternoon peak was enriched in genes related to muscle contraction and mitochondrial activity whereas the early morning peak was enriched in genes associated with inflammation and the immune response103. In addition, the use of genomic techniques has led to the identification of metabolic pathways regulated by clock genes within skeletal muscle, including those involved in glucose uptake, lipid metabolism and myokine secretion104,105,106. Dyar et al.104 observed that skeletal muscles of mice with a specific ablation of the core clock gene Bmal1 present an impaired insulin-stimulated glucose uptake due to (1) reduced protein levels of the insulin-dependent glucose transporter GLUT4 and the Rab-GTPase TBC1D1 involved in GLUT4 translocation to the plasma membrane and (2) a decrease in the activity of the glycolytic enzyme PDH. Furthermore, a high-resolution microarray analysis in a muscle-specific Bmal1 knockout mice model revealed a temporal separation of genes involved in carbohydrates and fatty acids use and storage over a period or circadian time of 24 h (CT 1 to 24)107. In this sense, circadian expression of genes involved in carbohydrate catabolism such as hexokinase-2 (Hk2; which catalyzes the first step of glycolysis) and pyruvate dehydrogenase phosphatase (Pdp1; which activates PDH) peak in the late inactive and early active phases of the day (CT 10–12). Moreover, the pyruvate dehydrogenase kinase gene (Pdk4; which inhibits PDH) peaks in the middle of the inactive phase of the day (CT 6). This circadian pattern of gene expression might promote an increase in the glycolytic flux during the active phase of the day (CT 12–24)107. On the other hand, genes involved in fatty acid uptake and β-oxidation such as acyl-carnitine translocase (Slc25a20; which transfers fatty acids into the mitochondrial matrix) and malonyl-CoA decarboxylase (Mlycd; which promotes β-oxidation by reducing malonyl-CoA levels) reach their peak expression in the middle of the inactive phase of the day (CT 7.5). Moreover, the gene that encodes for the nuclear PPARG co-activator 1 beta (Ppargc1b) which stimulates the activity of several transcription factors involved in mitochondrial biogenesis, fatty acid uptake and β-oxidation, also peaks in the middle of the inactive phase of the day (CT 7)107. Altogether, these results could suggest that there is a shift in the use of substrates from lipids to carbohydrates. This metabolic shift, which depends on the circadian gene expression in skeletal muscle, goes from the inactive (CT 1–12) to the active (CT 12–24) phase of the day. This circadian pattern of metabolic gene expression in skeletal muscle could explain the greater performance in short-duration maximal exercises observed in the evening hours (i.e. between 16:00 and 20:00 h). In this sense, a greater activation of the glycolytic pathway in the active phase of the day would promote greater performances in anaerobic exercises in the evening hours.

In spite of the typical temporary peak observed in the evening hours, many studies have demonstrated that regular training at a specific time of the day is able to blunt the diurnal fluctuations in maximal exercise performance30,36,45,54,63,64,65,66,69,73,74,78. The mechanisms responsible for the adaptations of training at a specific time of day in short-duration maximal exercise performance remain unknown. However, Sedliak et al.66 observed that the EMG activity during a maximal voluntary contraction of the knee extensors did not show any time-of-day specific adaptation after a 10-week training period at a specific time of day. This led the authors to suggest that peripheral rather than neural adaptations are the main source of temporal specificity in strength training. This could be caused by (1) an attenuation in training adaptations throughout the 10-week training period or (2) individual chronotype-related differences in responsiveness to training at a specific time of day. Likewise, intermittent fasting conditions, such as those imposed during the Ramadan period (i.e. 15–16 h starvation/day; from ≈ 04:00 h until ≈ 19:00 h) have shown to exert the same effect, minimizing the time-of-day dependent variations in exercise performance50,85. Chtourou et al.50 have suggested that Ramadan might act directly on the circadian rhythm of anaerobic performance by means of (1) inducing a phase advance or delay in the rhythm or (2) reducing the amplitude of the rhythm of the anaerobic power development. Despite the fact that none of these hypotheses have been tested to date, some of them have raised the question as whether circadian systems could account for time-of-day specific training adaptations.

There is evidence that scheduled exercise is able to cause phase shifts in the circadian system within skeletal muscle in mice15,16. Using a PER2::LUC circadian reporter mouse model, Wolff and Esser15 showed that four weeks of either voluntary or involuntary exercise for 2 hours/day were able to shift the phase of locomotor and molecular rhythms in skeletal muscle towards an earlier time of day. Furthermore, Edgar and Dement16 used two different wheel restriction schedules to determine whether exercise duration was an important determinant of feedback activity to the mouse circadian system. In this study, they found that more than 75% of total wheel activity occurred in the initial 2 hours over a 6-h or 12-h period of wheel availability. This led the authors to suggest that exercise intensity might be a primary determinant of the exercise-dependent phase shift strength. Thus, the ability of exercise to provide temporal feedback to the circadian system could explain why time-of-day effects on short-maximal exercise performance are blunted after a training period at a specific time of day. In humans, Zambon et al.17 found that the expression of circadian clock genes was affected in quadriceps muscles at 6 and 18 h after having performed a single session of one-leg resistance exercise. In this study, resistance exercise shifted the expression patterns of diurnal-regulated genes through two mechanisms: (1) by upregulating genes that are normally repressed in the morning; and (2) by downregulating genes that are normally activated in the morning. Among them, it was observed an upregulation of the gene that encodes for a regulatory subunit of protein phosphatase-1 (Ppp1r5), which is normally repressed in the morning. Protein phosphatase-1 is responsible for activating glycogen synthase while also inhibiting glycogen breakdown. Moreover, it was observed a downregulation of the gene that encodes for the mitochondrial uncoupling protein 3 (Ucp3), which is upregulated in the morning. Uncoupling protein 3 stimulates oxidative phosphorylation by creating proton leaks across the inner mitochondrial membrane. These data show that exercise represents an important circadian time cue and changes the phase of the molecular clock, specifically in peripheral tissues. Altogether, these results suggest that skeletal muscle molecular clocks might account for the adaptations of training at a specific time of day, suggesting a link between molecular clocks in skeletal muscle and exercise performance throughout the day.

Practical applications

Based on the studies summarized in this manuscript, it is clear that the time of day at which short-duration maximal exercise is conducted is an important variable for training prescription. However, to date, there are no guidelines to help athletes or coaches to achieve optimal performances or avoid deleterious effects of time of day on short-duration maximal exercise performance. Accordingly, some general remarks in this respect include: (1) under neutral climate conditions (i.e. 20–20.5 °C, 57–67% relative humidity), better short-duration maximal exercise performances are achieved in the afternoon (i.e. between 16:00 and 20:00 h) compared with the morning; (2) time-of-day deleterious effects on short-duration maximal exercise performance in the morning may be minimized after: (a) a 10-min warm-up period while listening to neutral or self-selected high-tempo music (>120–140 bpm) through headphones; (b) a 60-min exposure to warm and humid climate conditions (i.e. 28.1–29.5 °C, 62.6–74% relative humidity); (c) active warm-up protocols (e.g. 12–15 min pedaling at minimum intensities of 50% VO2max and interspersed with 5-s sprint exercises); (d) 2–4 weeks of intermittent fasting conditions of 15–16 h starvation/day from ≈04:00 h till ≈19:00 h (e) a training period of at least 5 weeks performed in the morning.

Conclusion

In summary, this review shows that, under neutral climate conditions, short duration maximal exercise performance is affected by the time of day, peaking between 16:00 and 20:00 h. However, a similar performance may be achieved in the morning hours if exercise is conducted after: (1) short exposures to moderately warm and humid environments; (2) active warm-up protocols; (3) intermittent fasting conditions; (4) warming-up while listening to music; (5) prolonged periods of training at a specific time of day. This suggests that time-of-day dependent fluctuations in short-duration maximal exercise performance are controlled not only by body temperature, hormone levels, motivation or mood states but also by a versatile circadian system within skeletal muscle.

Data availability

The datasets generated during and/or analyzed during the current study are available in the MEDLINE and Google Scholar repositories, https://www.ncbi.nlm.nih.gov/pubmed/, https://scholar.google.com/, respectively.

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Acknowledgements

Ministério da Educação, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) e Fundação a Pesquisa do Distrito Federal (FAPDF). We thank Diego López for the grammar and spelling correction of the manuscript.

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G.G.M. carried out the review and wrote the paper, R.S.M.N., D.A.V. and E.V. conceptualized the study, C.F. and E.V. acted as additional reviewers and assisted in the review of the final manuscript. G.G.M. design of the review, drafting the work, revising it critically for important intellectual content. R.S.M.N. drafting the work and search for articles in the data bases, revising it critically for important intellectual content. D.A.V. Search for articles in the data bases and revising it critically for important intellectual content. C.F. Revising it critically for important intellectual content and language revising. E.V. Conception and design of the work, interpretation of data for the work, drafting the work and revising it critically for important intellectual content.

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Mirizio, G.G., Nunes, R.S.M., Vargas, D.A. et al. Time-of-Day Effects on Short-Duration Maximal Exercise Performance. Sci Rep 10, 9485 (2020). https://doi.org/10.1038/s41598-020-66342-w

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