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How does a foundational myth become sacred scientific dogma?

The case of A.V. Hill and the anaerobiosis controversy

Part 5

 by Tim Noakes1

The integrated neuromuscular recruitment model of exercise physiology

In order to offer an alternative physiological model that would explain all these divergent findings, the central governor model has been developed (Noakes 1991, 2000; Noakes et al. 2001). We originally postulated that receptors may exist in the heart, muscles, brain, blood and perhaps respiratory muscles to assess the adequacy of oxygenation of those tissues. Before any of these reach some predetermined limit, the motor cortex in the brain reduces the number of skeletal muscle fibres that are recruited. As a consequence, skeletal muscle recruitments fails to rise further or it falls, limiting the amount of power the exercising muscles can produce. Since the body’s power output is regulated in this way, so the need from blood flow and oxygen use is reduced according to Figure 4.6. Thus the regulated fall in work output by the body reduces tissue oxygen demands and, as a consequence, the threat of hypoxic damage is averted.

Accordingly I have proposed that maximal exercise is limited by a regulated process that terminates exercise before the development of an oxygen deficiency in any of the tissues at risk during such exercise.

The next advance in the development of this ‘central governor’ model came when we found that less than 100 per cent of the muscle fibres in the active limbs are recruited during voluntary exercise (Gandevia 2001); that this amount is less the longer the duration of exercise and may be as little as 30 per cent at exhaustion during more prolonged (1–2 hours) exercise (St Clair Gibson et al. 2001); but that the body has the capacity to increase the number of muscle fibres that it recruits near the end of exercise, the so-called ‘end spurt phenomenon’ (Kay et al. 2001; Tucker et al. 2004). All these findings are compatible only with a model of exercise in which the brain regulates the performance by altering the amount of muscle that it recruits at all times during exercise (Figure 4.6).

We therefore concluded that the regulation of changes in power output during self-paced exercise reflects, principally, changes in the number of motor units that are active, that is, the mass of skeletal muscle that is recruited by the central nervous system (Noakes 2003). As a result, we propose (i) that it is indeed the brain that regulates performance during exercise by determining the total number of motor units that are recruited and alternatively de-recruited during exercise and (ii) that the number of motor units that are active is influenced by afferent sensory feedback to the brain from a host of peripheral receptors, only some of which are currently recognized (Figure 4.7). The goal of this sensory feedback is to ensure that the homeostasis is regulated and that damage to vital organs is prevented (Noakes and St Clair Gibson 2004; St Clair Gibson and Noakes 2004; Lambert et al. 2004).

Figure 4.7

Perhaps the simplest analogy for the central governor model is that of a Formula 1 racing car which will remain stationary until the brain of its driver takes control. The decision on how fast to travel is set by the driver’s subconscious and conscious brain in response to sensory feedback, including feedback from the racing team’s pit crew, the nature of the racing circuit, the driver’s prior experience and his perceived ability. But the control of the speed of the racing car is ultimately set by the pressure the driver’s foot exerts on the accelerator pedal. This is in turn determined by the number of muscle fibres in the driver’s right calf muscles that are recruited by his brain. And unless he has a death wish, the driver’s ultimate consideration will always be his own self preservation (homeostasis) and this will set the ultimate speed that he is prepared to risk.

Conclusion

The central conjecture that I have questioned originates from the statement by Hill and his colleagues in the 1920s, to the effect that: ‘The oxygen intake (during maximal exercise) may attain its maximum and remain constant merely because it cannot go any higher owing to the limitations of the circulatory and respiratory systems’. This conjecture has exerted a profound influence on the teaching of exercise physiology for the past 70 years, for it predicts a physiological model in which exercise performance is determined solely by oxygen delivery to the exercising muscles (Figure 4.2). Thus it is believed that exercise, especially of high intensity, causes the oxygen demand of the active muscles to outstrip the available oxygen supply, requiring the muscles to contract in the face of a developing anaerobiosis. This physiological model also predicts that, since anaerobic conditions in muscle terminate maximal exercise, the principal effect of exercise training and of any other interventions that improve exercise performance must be either to increase oxygen supply to the muscles or to increase the muscles’ capacity to utilize that oxygen (Figure 4.1). The model is also ‘catastrophic’ in that fatigue or exhaustion results only after the limitations of the system have been exceeded, causing system failure (Noakes and St Clair Gibson 2004; St Clair Gibson and Noakes 2004; Lambert et al. 2004).

Yet, as I have shown (Figure 4.3), Hill’s own findings did not adequately support his original conclusions. Hence the original basis for this physiological model is without substance. If the basis for the model is in doubt, then it behoves us vigorously to question the further predictions of that original model. The key assumption made by A.V. Hill, and by three generations of succeeding physiologists, is that there is complete skeletal muscle recruitment during all forms of exercise, not just during progressive maximal exercise to exhaustion but also during prolonged submaximal exercise. For if skeletal muscle recruitment is not total at exhaustion, then there is no known manner by which a peripheral regulator can determine fatigue in any form of exercise. The simple reason is that a peripheral control cannot regulate the contractile function of motor units that have yet to be recruited and in which the concentration of these ‘poisonous’ metabolites must be low if it is the process of contraction that causes the accumulation of such toxic metabolites.

To accommodate this new insight, my colleagues and I have proposed a novel model (Noakes and St Clair Gibson 2004; St Clair Gibson and Noakes 2004; Lambert et al. 2004) in which skeletal muscle recruitment is regulated, not limited, specifically to prevent damage to any of a number of different organs. Severe anaerobiosis is one specific endpoint that must be thwarted so that irreversible rigor and necrosis in the active muscles is prevented. But any number of other regulated processes can be imagined. Thus the function of the brain during exercise is to ensure that homeostasis is maintained in all the organ systems so that bodily damage does not occur. This model further predicts that the sensation of fatigue that is experienced during all forms of exercise is in some way determined by the effort required to maintain that homeostasis (St Clair Gibson and Noakes 2004; St Clair Gibson et al. 2003).

The challenge for the next generation of exercise scientists is to understand how the body anticipates the potential for organ damage and how skeletal muscle recruitment is regulated specifically to preclude any such calamity.

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Note

1 I should like to acknowledge my gratitude for the dedicated financial support of the University of Cape Town, the Medical Research Council of South Africa, Discovery Health, the Founding Donors of the Sports Science Institute of South Africa, and the National Research Foundation through the THRIP initiative, to the work of this Unit.