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A Novel Model of Integrative Central Neural Regulation of Effort And 120 Br J Sports Med: first published as 10.1136/bjsm.2003.010330 on 21 January 2005. Downloaded from EDUCATION From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions T D Noakes, A St Clair Gibson, E V Lambert ............................................................................................................................... Br J Sports Med 2005;39:120–124. doi: 10.1136/bjsm.2003.010330 It is hypothesised that physical activity is controlled by a maintained. The decisive studies of Kayser,2 Nybo and Nielsen,4 and Gonzalez-Alonso et al6 central governor in the brain and that the human body would now appear to confirm this interpretation, functions as a complex system during exercise. Using feed at least for exercise at altitude and in the heat. forward control in response to afferent feedback from Even during maximal exercise of short dura- tion, which, according to the Hill cardiovascular/ different physiological systems, the extent of skeletal muscle anaerobic/catastrophic model, is limited by a recruitment is controlled as part of a continuously altering severe uncompensated metabolic acidosis, arter- pacing strategy, with the sensation of fatigue being the ial blood pH seldom falls below about 7.1 and muscle pH below 6.6.11 12 However, when isolated conscious interpretation of these homoeostatic, central perfused skeletal muscle was tetanically stimu- governor control mechanisms. lated to similar pH levels (,6.8) in vitro in the ........................................................................... absence of an intact CNS, mechanical failure of the skeletal muscle only occurred at low tem- peratures (,12˚C).13 14 In contrast, at normal he first conclusion of this symposium is that physiological temperatures (,32˚C), force output the peripheral ‘‘limitations’’ or ‘‘catastrophe’’ was not affected by reduction of pH to this Tmodels of exercise physiology are unlikely to level.13 14 These findings led the authors to be correct as they are unable to explain a number suggest that direct reduction in force production of common observations in the exercise sciences. by pH was not a significant factor in muscle The most compelling of these are reviewed. fatigue at normal or raised physiological tem- peratures.13 14 More probably, a developing meta- FATIGUE AND WHOLE BODY bolic acidosis may induce a progressively HOMOEOSTASIS increasing homoeostatic respiratory compensa- Firstly, fatigue during any form of exercise tion, which increases the perception of discom- occurs without evidence of any related failure fort, at the same time producing a compensatory 16 of whole body homoeostasis as predicted by the alkalosis. This escalating discomfort ultimately http://bjsm.bmj.com/ ‘‘limitations’’ or ‘‘catastrophe’’1 models. Perhaps causes the conscious decision to terminate the the clearest examples are the fatigue that exercise bout.15 develops in extreme hypoxia at high altitudes23 Furthermore, skeletal muscle ATP concentra- and during exercise in conditions of severe tions are never reduced to less than 50% of the heat.4–6 In both cases, exercise terminates before resting value under all conditions of exercise, there is any evidence of a catastrophic failure including maximal exercise in persons with a of either metabolic35 or thermoregulatory4–6 reduced capacity to generate ATP either oxida- regulation. tively or glycolytically, or in muscles rendered on October 2, 2021 by guest. Protected copyright. For example, at extreme altitude, exercise ischaemic by the application of a tourniquet and terminates when symptoms of dyspnoea are forced to contract until exhaustion by external severe; yet it is precisely the very high rates of stimulation.9 This is especially remarkable, given ventilation causing that dyspnoea that maintain the small size of the total muscle ATP stores. life by ensuring that the arterial PO2 remains Thus muscle ATP concentrations are as tightly above about 30 mm Hg necessary to sustain regulated during exercise as they are at rest. 7 See end of article for consciousness. There is no published evidence Yet a core teaching of the peripheral ‘‘limita- authors’ affiliations showing that homoeostasis in any other organ tions’’ or ‘‘catastrophe’’1 models is that physical ....................... system is threatened during exercise at altitude; exhaustion occurs as a direct consequence of a Correspondence to: cardiovascular function in particular is entirely failure of homoeostasis—the linear model Professor Noakes, appropriate for the levels of exercise that are described by St Clair Gibson and Noakes.17 University of Cape Town, achieved,8 whereas the low muscle lactate con- Thus the presence of homoeostasis in all organ Research Unit for Exercise centrations and submaximal cardiac output systems at the point of exhaustion is perhaps the Science and Sports Medicine, Sports Science indicate that muscle hypoxia cannot be pre- most robust evidence supporting the hypothesis of South Africa, PO Box sent.910In contrast, the prediction of the central that exercise performance is regulated centrally 115, Newlands 7725, governor model is that the central nervous in the brain as part of a complex dynamic South Africa; tdnoakes@ system (CNS)89 determines the work rate that system, the principal function of which is speci- sports.uct.ac.za can be sustained for the anticipated duration of fically to ensure that homoeostasis is maintained Accepted 4 May 2004 exercise, as well as the moment at which exercise under all conditions of exercise. Accordingly, we ....................... terminates, all to ensure that homoeostasis is have postulated that the ultimate determinant of www.bjsportmed.com Regulation of effort and fatigue 121 Br J Sports Med: first published as 10.1136/bjsm.2003.010330 on 21 January 2005. Downloaded from this homoeostatic regulation is the CNS, which continuously and lactate production, thereby proving that those respective alters the number of motor units that are recruited during rates, previously considered to be maximal, were indeed exercise, thereby setting the total metabolic demand. Hence submaximal and were consequent only on incomplete physical exhaustion develops and exercise terminates as part recruitment of the total number of motor units in the of this homoeostatic regulation rather then as a catastro- exercising limbs. phic, system-limiting event as originally hypothesised by Noakes and St Clair Gibson9 present the evidence support- Edwards.1 ing their argument that skeletal muscle motor unit recruit- This new interpretation is the first to allow a more ment is never 100% even in supposedly maximal isometric reasonable description of a number of phenomena that defy contractions.21 28 Neurophysiologists have long accepted that rational explanation according to the traditional ‘‘limita- the progressive reduction in force production during sus- tions’’ models of fatigue.18 These include, among many tained isometric contractions or during prolonged exercise is others, the chronic fatigue syndrome, in which affected due principally to a progressive reduction in central neural individuals experience evident fatigue at rest,19 and the role command.28 Thus a number of recent studies reviewed by of psychological and motivational factors,20 centrally (brain) Noakes and St Clair Gibson9 confirm Gandevia’s28 telling acting pharmaceutical agents,15 21 22 hypnosis, shouting or conclusion that ‘‘human muscle fatigue does not simply sudden unexpected gunshots,21 or other forms of distraction reside in the muscle.’’ including music or premeditated deception on human Why is it that exercise physiologists seem to have assumed exercise performance.23 24 that skeletal muscle recruitment must always be maximal during exhaustive exercise? One logical explanation could RECRUITMENT OF MOTOR UNITS quite simply be that that is exactly how it feels; that the sensations that develop during exhausting exercise make it The second relevant conclusion of this symposium is that the validity of the peripheral ‘‘limitations’’ or ‘‘catastrophe’’ feel as if not a single additional muscle fibre could possibly be models requires that all available motor units in the activated for exercise to continue at the same intensity. exercising limbs must be recruited at exhaustion, regardless Another possibility is that few exercise scientists other than neurophysiologists routinely consider electromyographic eva- of the duration or intensity of the activity.9 For peripheral factors alone cannot cause the termination of exercise when a luation to be of special value, and few use it as an indirect majority of the available motor units are inactive at the point estimate of the extent of skeletal muscle recruitment during of exhaustion. This question is especially relevant in the case exercise. of prolonged exercise when less than ,30% of the available Thus one of the most important intellectual advances motor units may be active at exhaustion in recreational resulting from this symposium is that the presence or 25 26 absence of skeletal muscle anaerobiosis is not, as is usually athletes. Although elite athletes are likely to recruit a 29 30 31 32 greater proportion of their available motor unit reserve, there argued, even by ourselves, the definitive test of the is no reason to believe that this would be by more than a original cardiovascular/anaerobic/catastrophic model. Rather maximum of 10–20% greater than that achieved by recrea-
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