Most professional and recreational athletes perform pre-conditioning exercises, often collectively termed a ‘warm-up’ to prepare for a competitive task. The main objective of warming-up is to induce both temperature and non-temperature related responses to optimize performance. These responses include increasing muscle temperature, initiating metabolic and circulatory adjustments, and preparing psychologically for the upcoming task. However, warming-up in hot and/or humid ambient conditions increases thermal and circulatory strain. As a result, this may precipitate neuromuscular and cardiovascular impairments limiting endurance capacity. Preparations for competing in the heat should include an acclimatization regimen. Athletes should also consider cooling interventions to curtail heat gain during the warm-up and minimize dehydration. Indeed, although it forms an important part of the pre-competition preparation in all environmental conditions, the rise in whole-body temperature should be limited in hot environments. This review provides recommendations on how to build an effective warm-up following a 3 stage RAMP model (Raise, Activate and Mobilize, Potentiate), including general and context specific exercises, along with dynamic flexibility work. In addition, this review provides suggestion to manipulate the warm-up to suit the demands of competition in hot environments, along with other strategies to avoid heating-up.
KEYWORDS: cooling, exercise, fatigue, heat illness, hyperthermia, muscle temperature, post-activation potentiation
Body temperature has always been considered an indicator of health status. 1 However, only during the 20th century has thermoregulation of the healthy and active human become a major area of research. This interest was mainly driven by the requirements of the mining industry and the military. Lavoisier (1743–1794) showed that humans generated heat by a combustion process resulting in the production of carbon dioxide. Claude Bernard (1813–1878) then showed that the blood entering the lungs was warmer than that exiting, and that venous blood was warmer than arterial blood in several other organs, suggesting that these tissues were the site of heat production. Muscle heat production and dissipation during exercise and their role in increasing core temperature (Tcore) was described in detail during the 1960s. 2 Since then, several researchers and practitioners have discussed the potential benefit for performance of increasing muscle temperature (Tm) through warming-up, 3,4 or the potential impairment in performance and increased risk to athlete health of increasing Tcore. 5 Interestingly however, this dichotomy is generally considered independently.
From the minimal heat production associated with basal metabolic rate, heat production dramatically increases at the onset of a muscle contraction, doubling over the first minutes of intense dynamic exercise. 6 During the first 45 s, heat production mainly induces a large increase in Tm, 6 thereafter driving an increase in Tcore. 7 Although exact absolute values of Tm are dependent of the depth of measurement, muscle measured, environmental conditions, and intensity of contraction, Tm is ∼35°C at rest and will exceed Tcore within 3–5 min of exercise, remaining 0.65–0.95°C higher than Tcore. 7 As detailed in the first section of this manuscript, the initial increase in Tm has several benefits for athletic performance. Although the benefits of increasing Tm in-vivo might not be as important as originally estimated in-vitro, warming-up also offers non temperature-dependent effects.
Yet, depending on both exercise intensity and climatic conditions, the compensability of the environment will vary. 8 Maintaining thermal allostasis requires transferring metabolic heat from the core to the skin and then on to the environment. This involves an increase in cutaneous circulation 9 and sweating. 10 However, the increase in sweat rate necessary for heat dissipation can lead to progressive dehydration if fluid losses are not offset by adequate fluid consumption. 11-13 Progressive dehydration precipitates a cascade of events including a decrease in plasma volume and an increase in plasma osmolality, 5 a decrease in sweat rate and evaporative heat loss 14 and a decrease in cardiac filling. 15 As detailed in the second section of this manuscript, the blood flow redistribution and other thermoregulatory demands of exercising in hot and/or humid environments represents a significant stress to the cardiovascular system 16 limiting performance, 17 as maintaining a similar relative intensity requires the reduction of absolute intensity (i.e. work load). 18 Moreover, as detailed below, hyperthermia may also affect various levels of the neural system.
Lastly, the final sections of this manuscript will present practical sporting applications for (pre)competition in the heat. Despite a long history of research on thermoregulation, the incidence of heat stroke has increased over the past decades and heat is responsible for more deaths than all other natural disasters combined. 19 This manuscript will present the current state of the literature to inform creation of a warm-up specific to the requirements of competition. This will be achieved by extracting the principles of a 3-stage systematic approach (raise, activate and mobilise, potentiate; RAMP). Also, it will be discussed how to amend the athlete's warm-up to account for environmental conditions and reduce the risk of encountering heat illness. While the most important countermeasure to protect the health and performance of athletes in hot and/or humid environments is to heat acclimatize, 20 there are other countermeasures that can be implemented during the warm-up and throughout exercise that contribute to minimize the increase in Tcore, all the while maintaining optimal locomotor Tm and promoting non-thermal warm-up benefits.
As mentioned above, muscle contractions produce heat. This heat production will increase Tm within seconds, before any visible changes in Tcore. While muscle contractions produce heat, muscle contractility itself is also affected by temperature and thus warming-up.
Muscle temperature effects contraction velocity. 30 While a decrease in Tm can slow-down chemical reactions, 31 delay the cross-bridge cycle 32 and decrease actomyosin sensibility to calcium 33 ; an increase in Tm increases the rate of force development of a muscle twitch, 34,35 probably in relation to an increase in myosin adenosinetriphosphatase (ATPase) activity 36 and calcium sequestration by the sarcoplasmic reticulum. 37 In addition, maximum tetanic force can also be improved by increasing Tm, 34,38,39 possibly by improving contractile protein binding. 39 Of note, slow muscles (eg. soleus) seem to be more sensitive to temperature than fast muscles (e.g. extensor digitorum longus), especially at lower temperatures (i.e., 20°C to 10°C). 35,40 However, despite the inverse relationship between Tm and time to peak twitch tension and half relaxation time in vitro, 38 the effect of temperature is less marked toward physiological temperatures in vivo. 41 Indeed, an increase in Tm across the standard range experienced in vivo (i.e., from 37 to 43°C) has not been observed to modify the absolute force of the muscle fiber. 42 As a consequence, an increase in Tm does not necessary modify peak twitch amplitude in human skeletal muscle ( Fig. 1 ). 43-45 Consequently, increasing Tm through warming-up might have less benefit for muscle contractility in vivo than suggested by in vitro studies, especially in hot environments.
Muscle twitch at resting basal (plain line, blue) and elevated (dashed line, red) muscle temperature. An increase in muscle temperature generally increases the rate of force development and relaxation without modifying the peak tension. Data extracted with permission from Racinais et al. 45
However, in situ muscle responses cannot be limited to the muscle fiber as they also involve non-contractile tissue (e.g., ligaments). Indeed, increasing temperature decreases the viscous resistance of muscle and joints. 46,47 In addition, increasing temperature will affect the muscle environment by increasing local vasodilatation 48 and increasing both nerve and sarcolemmal action potentials. 49 Lastly, as detailed in the next paragraph, warming-up also has non-thermal benefits on the muscle.
Independently of the increase in Tm, a warm-up can potentially increase performance by ‘pre-conditioning’ the muscle. This phenomena called post-activation potentiation (PAP) is generally obtain by performing a maximal or near maximal contraction, 50,51 and has been suggested to have additional benefits relative to a traditional warm-up (i.e., without such contraction) to improve performance in explosive activities. 52 The first purported mechanism explaining PAP is a phosphorylation of the myosin regulatory light chains. 50,53 However, this phosphorylation is not consistently observed in humans. 54 The second mechanism proposed is an increase in spinal synaptic transmission that could last for several minutes following a contraction. 52 Synaptic transmission can be indirectly assessed using H-reflex, a monosynaptic spinal reflex representing an electrically evoked variant of the stretch reflex. While homosynaptic post-activation depression initially decreases the H-reflex during the first minute following a contraction, independently of Tm, 55 the H-reflex can thereafter be potentiated for up to 10 min following maximal contractions. 52,56 However, the efficacy of PAP on real-world athletic performance may still remain inconclusive, when considering the trade-off between, or even coexistence of both fatigue and potentiation actions on the muscle. 51,57 Indeed, neural drive following a maximal contraction is a balance between PAP and fatigue, 51 with the latter likely being the dominant factor. 58 On a separate note, muscles develop actin-myosin cross-bridges at rest to maintain muscle tone and posture. 59 These cross-bridges increase muscle rigidity, but muscle contractions during warm-up breakdown those cross-bridges, 60 potentially increasing the rate of force development and power. However, muscle rigidity re-increases rapidly once the warm-up is completed. 61
In addition to influencing muscle function, temperature and warming-up can affect the neural drive reaching the muscle.
It has consistently been demonstrated that cold exposure reduces nerve 62 and muscle 63 conduction velocity. In addition, cold exposure can increase antagonist muscle co-contractions, likely as a protective mechanism for cold muscles and joints. 64 Shivering can also affect agonist and antagonist (co-)activation. 65 A warm-up increasing body temperatures will therefore counteract these effects and increase performance in cold environments, especially during fast movements. 30
However, the benefits of increasing temperature on neural drive decrease as temperature increases, and are overlaid by other negative factors in hot environmental conditions. Indeed, the amplitude of electrically evoked M-waves and H-reflexes decreases at high temperatures, suggesting an alteration in peripheral neural drive transmission. 66 This decrease is likely due to a reduction in the opening time of the voltage-gated sodium channels, leading in turn to a decrease in the amplitude, duration and area of the axon potential. 67 This is in line with a negative correlation between skin temperature (Tskin) and the amplitude, duration, area and latency of a compound action potential, 68 with a Q10 effect on nerve conduction velocity between 1.1 and 2.4. 69 As a consequence, there is likely no benefit for neural drive transmission of increasing Tm to elevated levels. Even if defining an optimal temperature is contentious, as it depends on several intrinsic and extrinsic factors, it is generally accepted that a Tm slightly above resting should be aimed for when warming-up in temperate environments.
Warming-up has psychological effects potentially improving mental preparedness. For example, warming-up provides the athlete a dedicated time to focus on the event 70 and practice mental imagery, 71 thus offering important psychological effects, beside peripheral thermal and metabolic changes.
Cold exposure can increase muscle glycolysis and lactate accumulation suggesting a lower muscle efficiency and/or an effect of a lower perfusion in cold muscle. 72 Conversely, the increase in local vasodilation due to a temperature increase might benefit substrate delivery and metabolite removal. 48 This suggests that warming-up may have metabolic advantages, at least in cold conditions. Moreover, increasing temperature improves oxygen release from hemoglobin 73 and myoglobin. 74 However, increasing Tm increases ATP utilization with an increase in creatine phosphate degradation and anaerobic glycolysis. 75 This might be viewed as a positive pre-conditioning adjustment for short explosive activities, but might have negative consequences for prolonged exercise as this represents an increase in energy demand.
Abnormal electrocardiographic (ECG) responses suggestive of cardiac ischemia have been reported in 70% of participants running at a high intensity for 10–15 s without warming-up. 76,77 This very high prevalence was observed in asymptomatic males (age 21 to 52 y old) having otherwise normal ECG at heart rates of 170 bpm or higher when the load was progressively increased. 76,77 This phenomenon is likely due to an incapacity of the coronary blood flow to adapt fast enough. However, this abnormal ECG response is minimized or even suppressed by warming-up.
Warming-up is commonly considered as one of the basic tools to reduce injury risk. 3 For example, several studies have reported a decrease in injury prevalence in professional athletes after incorporating preventive physiotherapy programs including supervised warm-ups. 78,79 However, the specific role of the warm-up in these studies cannot be discerned as it was accompanied by other interventions such as taping, recovery, rehabilitation or core stability exercises. 78,79
In cold environments, there is an increase in antagonist/agonist muscle co-activation slowing movement velocity. 64 This slowing impairs performance but could also act as a protective mechanism for muscle injury. 31,64 A warm-up increasing body temperatures will counteract these effects and therefore increase performance in cold environments, especially during fast movements. 30 In addition, warming-up has also been reported to increase flexibility in winter sports performed in cold environments such as downhill skiing. 80 Indeed, increasing temperature increases extensibility in tendon 81 and other connective tissues. 82 As such, increasing peripheral tissue temperature with a warm-up could reduce injury risk. 3,81,82
Animal studies have shown that preconditioning the muscle by electrically evoked contractions increased its stretch length and the force required to tear the fibers. 83 While a part of this effect might be related to the minor (i.e., 1°C) rise in Tm reported by the authors, this study showed that preconditioning contractions reduced injury-risk. 83 An active warm-up also often includes stretching activities. 84 Stretching during warm-up was traditionally passive but it has shifted toward more dynamic exercises in the last decades. 84 While there is not enough data available to conclude on the effect of including stretching in the warm-up routine on injury prevention, some authors have suggested that this practice might reduce injury risk. 3,84 Indeed, both passively stretching or electrically contracting a muscle decreases the passive tension of the muscle-tendon unit. 85 Moreover, warming-up has been reported to reduce the magnitude of delayed onset muscle soreness (DOMS) 48 h after exercise involving a high eccentric component. 86
A rise in whole-body temperature and in particular Tm enhances explosive skeletal muscle performance (e.g., sprinting and jumping) by improving metabolic and contractile function, nerve conduction, and conformational changes associated with muscle contraction. 30,87,88 Conversely, the development of thermal strain, an elevation in Tcore, Tskin and Tm, is associated with increased fatigue development during sustained maximal voluntary isometric contractions (MVCs) 66,89-91 and impairs aerobic performance. 92,93-96 Moreover, while warming-up has health benefit to prevent cardiac ischemia, 76,77 and reduce the risk of injury, 79 heating-up carries a health risk. Indeed, the development of hyperthermia increases the risk of exertional heat illness (EHI), which is a serious health hazard.
In contrast to the beneficial effects of warming-up, the development of whole-body hyperthermia impairs neuromuscular function with alterations occurring at both the central and peripheral level. From a central perspective, elevated heat stress can lead to a reduction in voluntary muscle activation and the loss of force production capacity. 66,89,97 At the skeletal muscle level, a rise in temperature (e.g., 2–3°C) increases contractile speed (i.e., twitch contraction and relaxation time decrease) and alters the force/frequency relationship. 44,98
Brück & Olschewski 99 were among the first to postulate that heat stress might affect brain function and influence exercise performance. The authors identified 3 factors of discomfort that might counteract motivation and progressively reduce the drive to exercise during hyperthermia. They suggested that the interaction of circulatory, thermal, and muscular discomfort determined endurance time and work rate. Nielsen et al. 100,101 subsequently proposed that hyperthermia per se, rather than circulatory failure, was the critical factor causing exhaustion during exercise under heat stress. It was further purported that the attainment of a high Tcore (39.2–39.7°C) might influence the CNS by reducing mental drive (i.e., motivation) for motor performance. 100,101 Interestingly however, the capacity to generate force during a brief (3–5 s) MVC of the knee extensors and elbow flexors was unaltered after exhaustive cycling under heat stress. 101 This capacity to maintain force production was also preserved during 40 repeated MVCs. 89 Notwithstanding, force production was progressively impaired during a sustained (120 s) MVC relative to a contraction performed after exercise in cool conditions. The impairment was attributed to a hyperthermia-induced reduction in voluntary activation. 89 Others have also reported that the progressive increase in Tcore via passive heating is paralleled by a decrease in voluntary activation and force production during 3–5 s MVCs. 97,102 The authors further suggested that Tcore was the primary thermal input mediating hyperthermia-induced fatigue, as rapid cooling of the skin and muscle failed to improve voluntary drive, despite large reductions in cardiovascular and psychophysical strain. Taken together, these observations in isolated muscle contractions led to the suggestion that reaching a core temperature of ∼40°C may not only influence performance in an MVC due to the development of central fatigue, by may also account for the hyperthermia-induced fatigue that develops during prolonged dynamic exercise in the heat. 89,103 However, the development of fatigue during exercise in the heat is multi-factorial and associated with the interaction of several physiologic and psychological processes, and not caused by one single factor. 43,93,104 As such, use of the term “critical core temperature” in a reductionist manner is misleading when characterizing the influence of hyperthermia on the development of fatigue during exercise under heat stress. 105
Indeed, the development of exercise-induced hyperthermia has been shown to impact on performance at both the central and peripheral levels. In a recent study, Lloyd et al. 106 examined the impact of a range of Tm (22 to 38.5°C) on voluntary drive during brief (3 s) and sustained (120 s) MVCs. The authors reported that with Tcore remaining relatively stable, voluntary activation and hence force production, was inversely related to Tm during sustained contractions, but unaffected during brief MVCs. The observed reduction in voluntary drive was assigned to altered peripheral fatigue rates and/or sensitivity to peripheral fatigue occurring during the sustained contraction. It was estimated that a ratio of 5.5 to 1 represented the impact of Tcore and Tm on voluntary muscle activation, respectively. 106 Périard et al. 107 have also demonstrated that voluntary activation and force production are similarly reduced during a 20 s MVC following self-paced exercise in hot and cool conditions. The authors reported that the post-exercise decline in voluntary activation accounted for ∼20% of the decrease in total force production. It was thus suggested that the 0.8°C higher Tcore (39.0 vs. 39.8°C) at time trial completion in the heat did not exacerbate central fatigue and that the loss of force was mainly of peripheral origin and a consequence of the prolonged contractile activity associated with exercise. 107 It has also been shown that a similar increase in Tcore (39.5–39.8°C) either via active or passive heating elicits a similar reduction in voluntary activation during a sustained (45 s) MVC, but that a faster rate of decline in force production capacity occurs following exercise. 90 Together, these studies indicate that the loss of force production capacity originates from both central and peripheral fatigue factors, with the combination of heat stress and prior contractile activity (i.e., exercise) exacerbating the rate of decline.
To separate the effect of hyperthermia from the effect of exercise, several studies have used a passive hyperthermia approach. In the absence of exercise, passive hyperthermia has been shown to affect the peripheral nervous system, but also to induce a supraspinal failure when a contraction is prolonged. 66 Consequently, hyperthermia reduces voluntary activation 66,97,102 ( Fig. 2 ). To identify the mechanism(s) and localize the site of failure in voluntary activation during hyperthermia, Todd et al. 108 induced passive hyperthermia (38.5°C) and evaluated brief (2–3 s) and sustained (2 min) MVC performance in the elbow flexors with transcranial magnetic stimulation (TMS). They observed that hyperthermia induced decrements in voluntary torque and cortical activation during both contractions, with decreases being greater in the sustained MVC. Interestingly, the authors noted that peak muscle relaxation rate (measured during the silent period following TMS) during the sustained contraction was ∼20% faster in hyperthermia. This observation of an increase in contractile speed within heated muscle corroborated previous data, 98,109,110 and led to the suggestion that the greater central fatigue observed during longer contractions may be indicative of a failure in voluntary drive to account for temperature-related adjustments in muscle contractile speed. Hence, while high motor unit firing rates may be transiently attained during brief MVCs, these may not be sustained during prolonged contractions. 108 To further investigate the potential influence of a temperature-induced increase in motor unit firing rate in mediating the additional central fatigue observed during sustained contractions, Périard et al 91 actively and passively heated participants from 37.1 to 38.5, and on to 39.4°C. The authors demonstrated that both active and passive hyperthermia increased peak muscle relaxation rate when performing brief (5 s) and sustained (30 s) MVCs. Moreover, an increase from moderate (38.5°C) to severe (39.5°C) passive hyperthermia further increased relaxation rate, but without exacerbating force loss or voluntary muscle and cortical activation. It was thus concluded that centrally mediated rates of activation (i.e., motor unit firing) are sufficient to overcome active and passive hyperthermia-induced increases in peak muscle relaxation within physiologically relevant ranges (i.e., 10–30 Hz). 91 As such, the reduction in voluntary muscle activation noted during hyperthermia, whether induced actively or passively, does not appear to originate from a failure in voluntary drive to account for temperature-related adjustments in muscle contractile speed. Rather, voluntary activation failure is partly link to alterations in the peripheral transmission of the neural drive and the supraspinal generation of neural drive when contractions are prolonged. 66 Of note, peripheral alterations are not protected by heat acclimation 111 and voluntary activation remains depressed. 45 However, the supraspinal failure is reverted by acclimation, thus protecting from the additional hyperthermia-induced decrease in force when contractions are prolonged in acclimated humans. 111
Hyperthermia reduces the ability to sustain force/torque production (upper panel) and neural drive to the muscle (lower panel) during a 120-s maximal voluntary contraction. Data represent mean and 95% confidence-intervals from 14 participants in control or hyperthermic (rectal temperature 39°C) state. Reproduced with permission from Racinais et al. 111
High Tcore and Tm have been shown to influence muscle function and cellular metabolism in humans. Indeed, exercise in the heat leads to a greater reliance on muscle glycogen and anaerobic metabolism, 112,113 and causes a greater post-exercise accumulation of ammonia as well as muscle and blood lactate. 75,112,114 This elevated muscle lactate production is linked with muscle fatigue, and the decline in force observed during work at high glycolytic rates. 87 It is also highly correlated with the release of force-depressing free hydrogen ions (H + ). 115,116 Temperature-induced impairments in sarcoplasmic reticulum function or structural damage compromising sarcoplasmic reticulum calcium ion regulatory capacity may also influence skeletal muscle force production. 87,117
Moreover, it is well established that isometric exercise involves partial to complete occlusion of blood flow, 118,119 further increasing Tm and stimulating chemoreflexes and mechanoreflexes. 120,121 The afferent limb of these reflexes (i.e., group III and IV polymodal fibers) responds to chemical, mechanical and thermal stimulation, 122,123 which increases muscle sympathetic nervous activity. 124 Depending on the intensity of contraction, the rise in muscle sympathetic nervous activity can alter motor unit excitability, modifying the relationship between central neural drive, motor unit recruitment, and firing rate coding. 125,126 Impairment in neuromuscular function may thus relate to failure in the peripheral transmission of neural drive at any level from cortical activity to sarcolemma depolarization. 66 Although hyperthermia influences neuromuscular performance, it has been demonstrated recently that chronic exposure to heat stress (i.e., heat acclimation) improves skeletal muscle contractile function. 45 This occurs via increases in evoked peak twitch amplitude, torque production at a given voluntary activation as well as improvement in the relative torque/EMG linear relationship ( Fig. 3 ).
Heat acclimation increases peak twitch amplitude in both normothermic (COOL) and hyperthermic (HOT) state (left panel). Heat acclimation also improves the torque/EMG relationship (right panel). Reproduced with permission from Racinais et al. 45
The reduction in voluntary activation observed under heat stress (i.e., hyperthermia-induced central fatigue) may well represent a psychophysiological phenomenon whereby central neural drive is reduced via alterations in neuromuscular function and motivation. Indeed, considerable effort is required to sustain a maximal contraction, along with a willingness to withstand discomfort and pain. Mild sensations of discomfort are generally sensed at the onset of a contraction, which eventually develop into severe pain that alters the perception of sensations in the contracting musculature. 127 As a result, mental fatigue, which involves tiredness, limited attention span and an aversion or decreased commitment to continuing a task or activity, 128 may contribute to decrements in voluntary activation. Conscious signals originating from both central and peripheral afferent pathways could mediate behavior and reduce motivation in order to minimize discomfort 129 and lead to the abandonment of a task in which the energetic demands (i.e., effort) outweigh the perceived benefits of continued performance. 130 Essentially, a lack of motivation can cause central neural drive and motoneurone firing to decline, leading to a loss of force production. 131
During dynamic exercise, it has recently been demonstrated that endurance exercise capacity at 80% VO2max in a hot environment (30°C) is impaired by both a passive increase in Tcore prior to exercise, and a 90 min mentally fatiguing task. 132 It was further demonstrated that the performance impairment was exacerbated by the combination of these interventions, which acted synergistically to influence the exercise task. In contrast, a mentally fatiguing task undertaken prior to 45 min of moderate cycling and a ∼15 min self-paced cycling effort in 30°C did not influence time trial performance. 133 This was likely due to mental faculties already being strained by the combination of high intensity exercise and hot environmental conditions, and the mentally fatiguing task failing to increase negative valence and perceived exertion. A similar mechanism (i.e., failure in down-regulating perceived exertion) was purported to modulate the inability of carbohydrate mouth rinsing to improve 60-min cycling time trial performance in hot-humid conditions, which appears to have been influenced more significantly by the elevated levels of thermal and cardiovascular strain. 134 Notwithstanding, Flouris and Schlader 135 have suggested that thermal perception influences the rating of perceived exertion and concomitantly work rate at the onset of exercise when only Tskin is elevated. However, as thermal strain increases, factors associated with cardiovascular strain 94,95,136 more likely mediate the rating of perceived exertion and the voluntary reduction in work rate.
A moderate increase in core temperature can initially improve cognitive function. 137 Conversely, the development of hyperthermia can impair cognitive function, 138,139 with the impairments being task and complexity dependent. 140-144 It has been suggested that the performance of cognitive tasks under heat stress deteriorates when the total cognitive resources are insufficient to support both the adequate completion of the task and processing of the thermal stress. 139 As such complex tasks are more sensitive to hyperthermia than simple tasks. 140,141,143,144 Importantly, variations in temperature have been shown to induce pleasure or displeasure if they favor or perturb homeostasis, respectively. 145 Thus, a model was developed linking the decrement in complex task performance to the alliesthesial change accompanying compensatory physiological responses to hot environmental conditions. 144 More specifically, increases in temperature during heat exposure generated unpleasant stimuli, as measured by the Positive and Negative Affect Schedule (PANAS), which could be considered as a ‘cognitive load’. It was proposed that this load might reduce the available resources for concurrent cognitive tasks. Interestingly, this model could explain why reducing thermal discomfort, by cooling the head for example, can restore some complex cognitive functions in a hot environment. 66,142 Lastly, based on recent data showing that passive hyperthermia increased the rate of false alarms during a sustained attention task, 142 and led to faster but false responses during a complex planning task, 143 it has been suggested that hyperthermia may increase impulsivity. 144
The circulatory requirements associated with aerobic exercise under heat stress include an increase in skin blood flow and the maintenance of cerebral and exercising muscle perfusion. Although a transient vasoconstrictor-mediated reduction in skin blood flow occurs at the onset of exercise, cutaneous blood vessels eventually dilate to aid in the dissipation of accumulating metabolic heat. The Tcore threshold at which skin blood flow begins to rise is directly related to exercise intensity, and a delay in active vasodilation shifts this threshold to the right relative to rest. 146–149 During prolonged exercise in the heat, the rate of rise in skin blood flow markedly decreases after 20–30 min when Tcore nears 38°C, reaching a virtual plateau at ∼50% of maximum flow capacity. 150,151 At this point, the perfusion requirements of exercising muscles take precedence over thermoregulatory control. Despite this attenuation and the potential for splanchnic and renal vasoconstriction to redistribute 600–800 ml.min −1 of blood to the periphery, the large displacement of blood (6–8 l.min −1 ) to cutaneous vascular beds mediates a progressive decline in arterial pressure, central venous pressure and stroke volume that is accompanied by an increase in heart rate. 152,153 Interestingly, the relationship between Tskin and skin blood flow is minimally influenced by Tcore. 151,154 However, a strong link exists between the core-to-skin temperature gradient and skin blood flow. For example, a 10°C increment in ambient temperature is associated with a 4.5°C decrease in the core-to-skin temperature gradient. 155 This narrowing of the gradient leads to a reflexive rise in skin blood flow, 154,156,157 enhancing non-evaporative heat loss to the environment in compensable conditions.
In exercising muscles, blood flow requirements relate to a rise in relative exercise intensity whereby the increase in oxygen demand is matched by an increase in systemic and muscle oxygen delivery, as well as perfusion pressure. 158 Interestingly, recent studies show that elevated tissue/blood temperatures also induce an increase in skeletal muscle blood flow at rest and during exercise. 24,159,160 The mechanism(s) mediating this increase may include an interaction of metabolic and thermal stimuli inducing the release of erythrocyte-derived ATP, a potent vasodilator. 160 In absolute terms, muscle blood flow can increase from ∼0.3 l·min −1 at rest, to 10 l·min −1 during maximal exercise in less than 10 s. 161 If work rate is stable, a steady-state is reached within 30–90 s and blood flow rises only slightly when exercise intensity increases. 162 As such, muscle blood flow and oxygen uptake are quite stable during prolonged exercise at fixed intensities in thermoneutral conditions. 163 Under conditions of heat stress however, a rise in thermal strain exacerbates the cardiovascular response as metabolic and thermoregulatory processes compete for cardiac output. 152,164,165 The concept of competition or conflict between regulatory systems has recently been suggested to rather represent commensalism, which is an integrated balance of regulatory control where one circulation benefits without substantially affecting the other. 166
The classic hypothesis of circulatory/cardiovascular limitations to exercise in the heat proposed by Rowell 152 lies with the redistribution and peripheral pooling of blood, which reduces central blood volume and concomitantly ventricular filling pressure, end-diastolic volume, and stroke volume. A more contemporary hypothesis suggests that the reduction in stroke volume is primarily due to an increase in intrinsic heart rate, 167-169 mediated by the direct effects of temperature on the sinoatrial node, and/or baroreflex modulation of sympathetic and parasympathetic activity. 170 In effect, the decline in stroke volume during moderate intensity prolonged exercise in the heat likely originates from both a reduction in central blood volume reducing cardiac filling pressure, and a shorter diastolic filling time reducing ventricular end-diastolic volume. Indeed, when exercise is sustained in highly motivated individuals, the attainment of maximum or near maximum heart rate is a well-documented response. 92 Concurrently, maximum cardiac output is decreased, 171172 and the cardiovascular system is forced toward a functional limit at submaximal workloads and oxygen uptake. 173-175 It is suggested that this reduction in cardiovascular reserve is the primary factor limiting constant rate aerobic exercise, and manifested as an increase in relative exercise intensity and perceived exertion for a given workload. 43,129,171,172,176
Cheuvront et al. 93 have previously highlighted that the Tcore tolerated at exhaustion is inversely related to whole-body skin blood flow requirements, suggesting that fatigue during exercise in the heat may correspond with adjustments in muscle and cerebral perfusion related to increases in cardiovascular strain. During short but intense cycling at 80% of peak power output, Gonzalez-Alonso 177 noted that to exhaustion was associated with a reduction in systemic and exercising muscle blood flow, oxygen delivery and uptake. These reductions were exacerbated by heat stress, which accelerated the decline in mean arterial pressure and cardiac output, reducing VO2max. It has also been shown that during maximal incremental and constant rate exercise, systemic oxygen delivery is blunted by a plateau or decrease in cardiac output at intensities below VO2max. 178 From 50–90% VO2max, systemic and exercising muscle blood flow, along with oxygen delivery, match the rise in VO2. However, beyond 90% VO2max a levelling off occurs that attenuates the rate of rise in VO2, despite maximum increases in arteriovenous oxygen difference and heart rate. This impairment indicates an inability of the cardiovascular system to sustain a linear increase in oxygen delivery to exercising muscles. Aerobic power and capacity are therefore impaired by reductions in cardiac output and oxygen delivery to the exercising musculature, partly due to an enhanced muscle sympathetic nervous activity which attenuates leg blood flow. 178-180 These findings have been corroborated during maximal and supramaximal intensity cycling 181 and although metabolic energy requirements are greater in supramaximal exercise, a plateau in cardiac output and exercising muscle vascular conductance was noted at similar levels of oxygen delivery at both intensities. Taken together, these observations challenge the postulate that muscle oxygen delivery increases linearly from rest to VO2max. 158,182,183 During prolonged submaximal exercise in the heat, a similar compromise in oxygen delivery appears to occur, especially as heart rate nears maximum.
The impairment in prolonged self-paced exercise occurring in the heat ( Fig. 4 ) has also been attributed to this detrimental increase in circulatory/cardiovascular strain. 93-95,136,184,185 It has been shown that a thermoregulatory-mediated rise in cardiovascular strain is associated with reductions in VO2max and power output during prolonged (60 min) intense self-paced cycling in the heat ( Fig. 4 ). 94 Although exercise in both hot and cool conditions leads to a progressive decrease in VO2max, the extent of the decrement is greater in the heat. 95 Despite the larger decrease in aerobic capacity and concomitantly work rate (e.g., power output), relative exercise intensity (i.e., %VO2max) in the heat is maintained within a fairly narrow range (i.e., 2–5%), similar to that of cooler conditions. This range widens under heat stress however, as exercise becomes protracted and a disassociation develops between relative exercise intensity and heart rate and RPE. 95
Power output and cardiovascular response during a 40-km cycling time trial in Hot (35°C) and Cool (20°C) conditions. Values are means ± SD for 8 subjects. ∗Significantly different from Cool (P < 0.05). §Significantly higher than previous (P<0.01). †Significantly lower than 10 min (P < 0.05). Reproduced with permission from Périard et al. 17
