Corresponding author J. H. Coote: School of Clinical and Experimental Medicine, College of Medical and Dental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK. Email: firstname.lastname@example.org
The Olympic biathlon is a very demanding physical event that requires high oxygen delivery, good cross-country skiing skills and skilful use of a rifle. Like all high-performance endurance athletes, high cardiac vagal tone is a characteristic and extends the range over which cardiac output can increase. In the biathlete, however, the enhanced vagal control of the heart also allows a strategy for better control of stability needed for accurately firing a rifle at the end of each lap of the race. The role of endurance training, central command, reflexes from muscle, and of the carotid–cardiac baroreceptor reflex in changing vagal tone during intense exercise and recovery is discussed.
The mechanisms contributing to the heart rate changes at the start and during exercise have been well explored (Coote & Bothams, 2001; Raven et al. 2006). Less attention has been given to the events underlying the fall in heart rate at the cessation of exercise. In recent years, however, clinicians have become aware of the prognostic value of the decline in heart rate following exercise as a predictor of mortality in patients at risk of cardiac disease (Cole et al. 1999; Buch et al. 2002). In addition, its value in assessment of the beneficial effects of different training regimens has been realized by athletic coaches (Borresen & Lambert, 2008). During some endurance events, the speed of recovery of heart rate following exercise is of particular importance. One such event is the biathlon, which is an event that combines cross-country skiing for up to 20 km with the ability to aim a rifle accurately and hit a target at 50 m distance in subzero temperatures (Fig. 1). Competitors in biathlon are elite endurance athletes, who need stamina in abundance and great skill not only to ski fast but also to control a rifle. Skiers set off at regular intervals and race against the clock over laps of 5 km. At the end of each lap, they stop at a shooting range to take five shots using a small-bore rifle without magnifying sites. Time or distance penalties are added for each target missed. The skier must come to a complete stop before they start firing from two different positions, prone and standing. In the prone position they must fire five shots at each of five targets of 4.5 cm diameter. In the standing position they fire a further five shots at 15.5 cm targets. The heart is racing and breathing is hard from the exertion of racing on skis, but since it is vital to hit the targets, it is said that in order to allow their heart and breathing to slow, athletes often slow their skiing speed down on approaching the shooting station. Understandably, this is difficult; therefore, biathletes train to control their breathing and heart rate and learn to relax between periods of extreme effort.
It is therefore not surprising that these winter Olympians are elite athletes who have high maximal oxygen uptake values (>65 ml min kg−1) and low resting heart rates, around 50 beats min−1 (Mognoni et al. 2001), suggesting high vagal tone and high baroreflex gain.
Endurance exercise and the cardiovascular system
Elite athletes undertaking events such as the biathlon need to provide a sustained high oxygen delivery to the working muscles, including the respiratory muscles. This is achieved to a large extent by the ability to increase cardiac output from resting levels of around 4–5 l min−1 to 40 l min−1 or more, together with adaptations in the trained muscles. As a consequence, can be as high as 70–80 ml kg−1 min−1 (Astrand & Rodahl, 1977), and competitors usually maintain their skiing activity at 70–90% of (Hoffman & Street, 1992; Mognoni et al. 2001).
Owing to the focus of this review, in the following account I will consider only cardiac output further. Cardiac output is the product of stroke volume and heart rate, and the significance of these is dealt with in turn.
Around 50% of the high during exercise of elite athletes can be attributed to an increase in maximal stroke volume. This is enabled by having an enlarged left ventricle as a result of prolonged periods of endurance training (Ehsani et al. 1978). Such a change is partly due to stress-induced growth of myocardial cells (Moore & Korzick, 1995) as a consequence of the volume loading (higher venous return) experienced by the heart during exercise, but may also be a consequence of an increase in filling time associated with a lower resting heart rate for a given workload induced by training (Rowell, 1993). These effects are supported by an increase in systemic vascular conductance and a training (exercise)-induced expansion of plasma volume of approximately 200–300 ml.
Heart rate makes little contribution to maximal oxygen uptake because maximal heart rate remains the same, since it is not altered by endurance training. Resting heart rate, however, is decreased (Al-Ani et al. 1996b), and the importance of this is that it allows a larger range over which it can increase during exercise. This, combined with a larger stroke volume, enables the same cardiac output (oxygen delivery) to be achieved at a lower heart rate, thus enabling the very high values of cardiac output to be reached without compromising filling time by much higher heart rates. An added benefit is that oxygen delivery to the heart muscle is greater because the longer diastole increases cardiac perfusion for a given workload. A lower resting heart rate may have other benefits, such as reducing adverse events due to coronary artery disease or heart failure, but discussion of these is outside the scope of this article (see Buch et al. 2002).
All parameters of cardiac function, including heart rate, conduction, force of contraction and relaxation, reflect the net balance between an inhibitory parasympathetic influence and an excitatory sympathetic influence (Levy, 1998). Whilst the general contribution of cardiac sympathetic nerves to all chambers of the heart is well accepted (Armour, 1996), there is a degree of ignorance surrounding the influence of the cardiac vagal efferent fibres. However, both anatomical studies (Johnson et al. 2004) and functional studies (Xenopoulos & Applegate, 1994; Gatti et al. 1997; Lewis et al. 2001; Brack et al. 2009) show that cardiac vagal postganglionic fibres project to all chambers of the heart and can have a significant influence on ventricular rhythm, conduction and force of contraction. In addition, vagal nerves inhibit sympathetic nerve activity via pre- and postsynaptic interactions (Paterson, 2001; Casadei, 2006). Although these effects should be borne in mind, they are not the main focus of the present review, which is to discuss the changes in the vagal inhibitory effect on cardiac pacemaker activity which, together with cardiac sympathetic changes, is especially pertinent to exercise performance in the elite biathlete.
Resting cardiac vagal tone
Since there are no parallels in man to the direct neuronal recording in experimental animals from cardiac nerves, a variety of linear and non-linear mathematical measures of the variability in heart rhythms (heart rate variability) have been used. Humans at rest show a degree of sinus arrhythmia, in which heart rate increases during inspiration and decreases during expiration, which is more pronounced in younger people. This beat-to-beat variation during each respiratory cycle is mainly dependent on cardiac vagal activity, since it disappears following peripheral cholinergic blockade with atropine (Eckberg, 1983). Thus, to gain insight into changes in autonomic balance, a much favoured approach is analysis of the frequency and magnitude of the oscillations of heart rate variability from a spectrum of the sum of the sine waves that approximate the original signal using fast Fourier transform or an autoregressive method (Karemaker, 1993). Providing both respiratory rate and depth are controlled for, the high-frequency peak in the spectrum corresponds to vagal activity (Karemaker, 1993; Sandercock et al. 2008). Other measures of vagal tone, such as the root mean square of successive differences (RMSSD) between R–R intervals, have been validated (Task Force, 1996; Buch et al. 2002). These methods have confirmed that in humans at rest, heart rate is a function predominantly of the amount of cardiac vagal nerve activity (Eckberg, 1983; Al-Ani et al. 1997; Buch et al. 2002). Cardiac vagal tone is determined by the integration of several different synaptic inputs to the cardiac preganglionic neurones (Daly, 1997), located in the nucleus ambiguus and vagal motor nucleus in the brainstem (Spyer, 1981). The main excitatory inputs are from arterial baroreceptors and chemoreceptors (McAllen & Spyer, 1978; Potter, 1981) and the trigeminal receptors situated on the face and in the upper airways (Daly, 1997). A major inhibitory influence is from medullary inspiratory neurones (Daly, 1997). The vagal preganglionic neurones project axons to the various ganglionated plexuses throughout the heart (Armour, 2008), from where the peripheral neuronal circuits mediate postganglionic vagal effects via acetylcholine and other neuromodulators, such as nitric oxide (Armour, 2008; Herring & Paterson, 2009; Brack et al. 2009).
Effect of endurance training on resting cardiac vagal tone
Repeated long periods of aerobic exercise normally result in a significant drop in resting heart rate (Barney et al. 1988; Reiling & Seals, 1988). This is accompanied by an increased respiratory sinus arrhythmia and an increased high-frequency peak in the R–R interval power spectrum (Al-Ani et al. 1996b). Therefore, the lower heart rate after training was interpreted as due to an increase in resting cardiac vagal tone. Further support for this conclusion came from the demonstration that following endurance training, there is a greater degree of shortening of the R–R interval immediately after an isometric voluntary or involuntary contraction of the arm flexors, an effect entirely due to vagal withdrawal (Al-Ani et al. 1996b). It is therefore reasonable to conclude that the low resting heart rates of biathletes are mainly a result of a high vagal tone.
The question of what mechanisms underlie the training-induced increase in cardiac vagal tone has been addressed over many years with little success, but recently more promising results have been reported (Mohan et al. 2000; Danson & Paterson, 2003). It was shown that isolated atria from endurance exercise-trained mice had a small but significant enhancement of the slowing induced by vagus nerve stimulation. Associated with this change, there was also an upregulation of the nitric oxide pathway (Mohan et al. 2000), an effect that would have led to facilitation of vagal cholinergic transmission and accentuated antagonism of cardiac sympathetic activity (Conlon et al. 1996; Paterson, 2001). A tantalizing possibility that there are changes in the central neuronal pathways controlling vagal tone is more difficult to study. Intriguingly, however, the arterial baroreceptor synapses in the cardiac vagal neurone pathway in the medulla are positively modulated by an intrinsic NO mechanism (Fletcher et al. 2006), whereas presympathetic neurones are negatively affected (Zanzinger et al. 1995). Therefore, similar effects to those in the peripheral organ (Danson & Paterson, 2003), occurring also in the NO synthesis pathways in the brain, both activated by chronic exercise, could more fully explain why the heart rate becomes much slower.
Cardiac autonomic balance during exercise
Exercise causes a marked alteration in cardiac autonomic balance, which is illustrated schematically in Fig. 2. Using a variety of time domain and frequency domain methods, various studies have confirmed that at the start of exercise there is an immediate decrease in cardiac vagal tone that contributes entirely to the initial increase in heart rate (Al-Ani et al. 1996b; Gladwell & Coote, 2002; Gladwell et al. 2005). This is followed by a more gradual vagal withdrawal (O’Leary & Seamans, 1993) and, as heart rate reaches about 100 beats min−1, an increasing effect of cardiac sympathetic acceleratory fibre activation predominates (Fig. 2; O’Leary & Seamans, 1993; Tulpo et al. 1998; Ogoh et al. 2005; Raven et al. 2006). Significant for performance, the exercise intensity at which cardiac vagal influence disappears is higher in those who habitually undertake aerobic exercise (Tulpo et al. 1998), in accordance with the increase in resting vagal tone associated with endurance training. Subsequently, heart rate continues to increase to maximal heart rate under the influence of increasing sympathetic nerve activity and, to some extent, circulating hormones, but it remains constrained by the arterial baroreceptors (Raven et al. 2006). The baroreceptor reflex is, however, reset to a higher operating point (Bevegard & Shepherd, 1966; Coote & Dodds, 1976; Raven et al. 2006).
Initiators of the cardiac events during exercise
There is convincing evidence that the cardiovascular changes associated with exercise are set in motion by central command, in which cerebral regions concerned with volition induce parallel activation of motor and cardiovascular centres (Coote, 1995; Secher, 1999). Whilst central command is clearly important, numerous studies in experimental animals and man show that afferent feedback from exercising muscles exerts a considerable additional influence (Coote, 1995; Coote & Bothams, 2001; Fisher & White, 2004). Especially relevant are studies showing that cardiac acceleration is linked in a graded fashion with involuntary muscle contraction where central command is absent (Bull et al. 1989; McMahon & McWilliam, 1992; Al-Ani et al. 1997). Recent evidence shows that these involuntary muscle contraction-induced heart rate increases are elicited by small muscle afferents that are sensitive to distortion or stretch of muscles, so allowing their effects to be examined experimentally in humans and experimental animals (Potts & Mitchell, 1998; Gladwell & Coote, 2002; Fisher et al. 2005). The primary effect of these muscle mechanoreceptors, named tentanoreceptors by Gladwell et al. (2005), is an inhibition of cardiac vagal tone. Muscles also contain metabolically sensitive afferents that are excited during muscle contraction and throughout exercise and provide a major driving force to sympathetic activity (Coote et al. 1971; McCloskey & Mitchell, 1972; Fisher & White, 2004).
The combined action of the central and peripheral arms of the exercise control system is to increase heart rate (Fig. 2) and arterial blood pressure simultaneously. Since increases of this kind would normally be sensed by arterial baroreceptors and buffered in part by decreases in heart rate, the question arises of how well these receptors are functioning during exercise and particularly during prolonged endurance events, such as the biathlon.
Baroreceptor control of heart rate in exercise
During exercise, the baroreceptor reflex is reset to a higher operating point (Bevegard & Shepherd, 1966; Coote & Dodds, 1976; Raven et al. 2006). In a beautifully designed series of studies, Peter Raven and colleagues tested the entire carotid baroreceptor stimulus–response curve by measuring the heart rate changes following increases and decreases in pressure in a neck cuff, which induce decreases and increases, respectively, in carotid baroreceptor input. In accord with resetting, it was revealed that the carotid–heart rate response curve during exercise was shifted to the right and upwards but was similar to rest, except that the reflex was now operating at a higher heart rate and arterial blood pressure (Fig. 3; Raven et al. 2006). The relocation of the function curve occurs in direct relation to the intensity of exercise, and the operating point is similarly shifted to a higher point on the function curve, hence to a position of reduced gain (Fig. 3; Ogoh et al. 2005). The extent of this change in position of the operating point and reduction in gain of the baroreceptor–heart rate response reflects the decrease in cardiac vagal tone that is induced by exercise. As a consequence, there is a progressive operational reduction in the baroreceptor reflex control of the heart rate from rest to maximal exercise, although a degree of control is still maintained via the cardiac sympathetic supply. The importance of the resetting is that it provides a sufficient buffer of the cardiovascular changes to control them adequately in a physiologically beneficial manner relevant to exercise intensity. Thus, if the influence of the baroreceptors is reduced by maintaining blood pressure at resting values when humans or animals are exercising, the heart rate changes are much increased (Scherrer et al. 1990; DiCarlo & Bishop, 1992). Although not directly pertinent to this review, it is important to understand that the influence of the baroreflex on arterial blood pressure is also reset and that this occurs despite the increase in vascular conductance in the exercising muscles, which is partly offset by opposite changes in other vascular beds (Keller et al. 2003).
How exercise brings about these changes in the baroreceptor influence has been explored in numerous studies (Raven et al. 2006). There is a consensus that central command is associated with a rightwards and upwards shift of the carotid–cardiac response curve and a relocation of the operating point away from maximal gain (Gallagher et al. 2001a; Raven et al. 2006). In contrast, studies of the exercise pressor reflex, which was selectively tested by postexercise muscle circulation occlusion, when only muscle metaboreceptors remain active, showed that the carotid–cardiac function curve was relocated rightwards to a higher carotid pressure without any upward movement, so that the gain around the operating point was unchanged (Gallagher et al. 2001b; Fisher et al. 2008). However, these excellent and ingenious studies on human subjects deliberately excluded a tentanoreceptor input from active muscles, so the full reflex effect from exercising muscles on the carotid–cardiac function curve remained obscure. This is important because recent animal model and human studies have established that the muscle tetanoreceptors can bring about an immediate and sustained withdrawal of cardiac vagal tone (McMahon & McWilliam, 1992; Gladwell & Coote, 2002; Gladwell et al. 2005; Fisher et al. 2005). In accord with this, electrically induced involuntary isometric contraction of limb muscles, where central command is absent, can induce similar heart rate (and blood pressure) increases to voluntary isometric contractions (Bull et al. 1989). Therefore, it follows logically that input from muscle receptors during exercise must shift the carotid–cardiac response curve both rightwards and upwards.
Thus, the concerted actions of both central command and muscle reflexes are likely to contribute to resetting of the carotid–cardiac response curve. To some extent, this is at variance with the arguments put forward by Raven et al. (2006), based on several studies in which it was concluded that central command is 100% responsible for the upwards resetting of the carotid–cardiac response curve. The studies surveyed by these authors have used imaginative and robust methods in an attempt to manipulate either the level of central command or the metaboreceptor input from exercising muscle, but a contribution from muscle tetanoreceptor activation was not considered. It is important to realize that reference to an exercise pressor reflex is historically associated with the influence of the muscle metaboreceptors, and experimental manipulation of these has a more limited effect on the cardiac response curve (Ogoh et al. 2002).
Heart rate recovery after exercise
This brief summary of the changes accompanying exercise and some of the underlying mechanisms enables a better insight into the cardiac events following exercise. On the cessation of high physical activity, heart rate decreases rapidly (Fig. 2) and more quickly than arterial blood pressure. Studies of heart rate following heavy exercise in subjects before and after a period of endurance training show that recovery becomes significantly faster after training (Goldberger et al. 2006; Seiler et al. 2007; Martinmäki & Rusko, 2008). Furthermore, comparisons between highly trained endurance athletes and untrained control subjects show that heart rate falls more quickly after a bout of high-intensity exercise in the athletes (Brown & Brown, 2007; Borresen & Lambert, 2008). The immediate rapid reduction in heart rate is largely eliminated by cholinergic blockade with intravenous atropine (Savin et al. 1982; Imai et al. 1994; Fisher et al. 2006; Borresen & Lambert, 2008). Therefore, cardiac parasympathetic reactivation is the principal determinant of the immediate fall in heart rate when exercise ceases or intensity drops. Following moderate and longer periods of dynamic exercise, however, the sharp fall in heart rate does not reach the previous resting value but continues to decrease slowly in an exponential manner (Savin et al. 1982) over many minutes, and longer depending on the duration and intensity of the exercise (Hautala et al. 2001; Murrell et al. 2007). During this period, there is a co-ordinated cardiac vagal–sympathetic interaction, which ensures that there is sufficient cardiac output to prevent circulatory collapse whilst the dilated muscle vascular beds recover. This is probably enabled by slow reduction of sympathetic nerve activity, which is still being reflexly enhanced by muscle metaboreceptors as the muscles recover, and by the slow clearance of circulating catecholamines (Hart et al. 2006).
The pattern of parasympathetic reactivation after exercise has been confirmed by studies using a variety of indices of heart rate variability, both in the time domain and in the frequency domain (Savin et al. 1982; Hautala et al. 2001; Goldberger et al. 2006; Brown & Brown, 2007; Kaikkonen et al. 2007; Murrell et al. 2007; Martinmäki & Rusko, 2008; Sztajzel et al. 2008). In summary, the rapid heart rate decrease that occurs promptly when exercise ceases is entirely due to increase in cardiac vagal activity, and the subsequent slow exponential decay in heart rate results from algebraic summation of an increasing vagal inhibitory effect and a gradually subsiding excitatory sympatho-adrenal action. An important question is what is driving the increase in cardiac vagal activity at the termination of exercise when it appears as though there is a freeing of constraint of cardiac vagal neurones. This is most dramatically observed at the end of isometric contractions of arm or leg muscles if the blood flow to the muscle is occluded with a cuff (Fig. 4). In these circumstances, the effect of central command and muscle mechanoreceptor input is removed, and there is little central respiratory inhibitory input to the cardiac vagal neurones, leaving only the muscle metaboreceptor influence. In these circumstances, blood pressure remains increased and the heart rate descends very rapidly to pre-exercise control levels or less (Fig. 4; Bull et al. 1989; Fisher et al. 2008; Ogoh et al. 2009). This results in the carotid–cardiac response curve moving down and to the left, and the operating point moving down the slope to a point of maximal gain, so the full excitatory effect of the arterial baroreceptors on cardiac vagal outflow is strongly manifest. In the period following the initial rapid recovery, the sensitivity/gain of the carotid–cardiac baroreceptor reflex remains increased even up to 24 h following a single bout of exercise in the laboratory (Convertino & Adams, 1991). Convertino & Adams (1991) evaluated the carotid–cardiac baroreflex with graded pressure changes applied around the carotid sinuses in the neck using a neck cuff. Following exercise to exhaustion in healthy normotensive young men, measurements of the baroreflex response curve for nine periods spanning 24 h showed that it was shifted downwards and to the left with an increase in slope, indicating an increase in gain. Therefore, the evidence supports the idea that the arterial baroreceptors are a major driving force to increase cardiac vagal activity immediately after a bout of exercise. However, the duration and type of exercise have a major influence on the time course of the changes in autonomic balance and baroreflex sensitivity. For example, measurements made in more real-life situations, such as a 75 km cross-country ski race (Hautala et al. 2001) or a mountain marathon fell race (Murrell et al. 2007), showed that for 24 h following the race, heart rate remained higher than the control pre-race level, sympathetic activity and vagal activity had not returned to pre-race values and baroreflex sensitivity was attenuated. These values had returned or exceeded pre-race values by 48 h.
In the long term, repeated periods of exercise induce changes in the influence of the vagus nerves on cardiac excitability (Danson & Paterson, 2003). This may to help explain why there are many reports that regularly repeated exercise, in both young and elderly subjects and in hypertensives, increases the baroreflex sensitivity (Barney et al. 1988; Sommers et al. 1991; Shi et al. 2008).
The change in resting cardiac vagal tone may be of great significance to the type of endurance competition that is practised by the biathlete. Elite biathletes have high values (>60 ml min kg−1) and low resting heart rates (around 50 beats min−1; Mognoni et al. 2001), suggesting high vagal tone and high baroreflex gain. Hence, during a race as soon as these athletes reduce exercise intensity and eventually come to a brief stop (<1 min), heart rate might be expected to drop rapidly and thus enable more precise control of the rifle position. This will be affected by ventilation depth and frequency (Al-Ani et al. 1996a) and by how much physical activity is reduced. Perhaps also of importance is the demonstration that the speed of parasympathetic reactivation is affected by posture. Buchheit et al. (2009) estimated vagal activity from time domain and frequency domain analysis of heart rate variability with subjects resting in four positions following a bout of exercise. It was shown that heart rate slowing and the measured indices of vagal reactivation were greater when the subjects were lying down compared with sitting or standing. This would suggest that biathletes should first fire at the targets in the prone position before doing so from the standing position. The start–stop nature of the intense periods of exercise is unique to biathlon and, whilst heart rate has been measured, little else of the physiological events in athletes participating in or following a race is known.
A further factor that might have a significant influence on cardiac parasympathetic activity and its reactivation after exercise is the effect of cold air on the face. The biathlon events take place in temperatures around zero or subzero, so that the trigeminal afferent nerve endings in the facial regions around the cheeks and nasal areas are likely to be substantially stimulated. Experimental animal studies have shown that some of these afferents provide a strong excitatory input to cardiac vagal neurones (Daly, 1997), resulting in a profound bradycardia. Cooling of the face in areas supplied by the trigeminal nerve also produces a vagal bradycardia in humans (Finley et al. 1979; Al-Ani et al. 1995). Furthermore, in a study of the interaction between exercise and facial cooling, Al-Ani et al. (1995) found that as the exercise effect declines, the influence of the trigeminal input predominates; this should be especially beneficial to the biathlete. No studies of the influence of cold on the performance of biathletes have been reported, although a laboratory study of elite skiers indicated that oxygen uptake was higher in a cold compared with warm temperature for the same degree of submaximal exercise (Sandsund et al. 1998).
Taking account of the physiological factors, it is not surprising to learn that during a race, as the firing station is approached, the heart rate of a biathlete decreases by about 5% or more from the race level of 90% maximal heart rate. This is reduced further, to 60–70% of maximal heart rate at the firing line and drops even lower in the prone position (Hoffman & Street, 1992). This may be learned during training, and an interesting speculation is whether there is also a conscious attempt by the athlete to slow heart rate, since time spent at the firing range has to be very short, <1 min, so there is a strong advantage in willing heart rate to fall rapidly. A cerebral influence may not be too far fetched, since there is good evidence from studies on experimental animals and humans (Oppenheimer et al. 1992a,b) that neurones in the left insular cortex can selectively induce vagal bradycardia and may be part of an exercise central command network (Williamson et al. 2006).
The Olympic biathlon is a very demanding physical event that requires high oxygen delivery, good cross-country skiing skills and skilful use of a rifle. Like all high-performance endurance athletes, high cardiac vagal tone is characteristic and extends the range over which cardiac output can increase. In the biathlete, however, the enhanced vagal control of the heart also allows a strategy for better control of stability needed for accurately firing a rifle at the end of each lap of the race.
It is with regret that because of editorial restrictions, many relevant outstanding papers on this subject could not be cited.