AN ADVANCEMENT IN THE CONCEPT OF EXERCISE FATIGUE
Noakes, T. D. (2012). Fatigue is a brain-derived emotion that regulates the exercise behavior to ensure the protection of whole-body homeostasis. Frontiers in Physiology, 3, article 82, pp. 10.
[Editor's note: Although this article is not directly on swimming, it is very important for swimming science. Essentially, it explains that the physiology of exercise model upon which traditional swimming physiology is based is wrong and incomplete. A new approach to understanding the physical limits placed on a swimming exercise needs to be developed. This is further grist for the mill of swimming science as it adds to the flaws in the structures of several incomplete exercise physiology models that have been adopted by the sport's scientists and coaches (see An Argument That Modern Exercise Physiology Needs Revising and Physiological Training Principles Are often Inaccurate.]
This article unites past, present, and diverse literature sources to provide a very useful concept of fatigue and how the body guards against the potential destructive effects of fatiguing exercise. The work of Italian physiologist A. Mosso, written a century ago is cited as explaining two central concepts of muscular fatigue. The first is central and neural in origin then described as "the will" which alluded to how much work an individual would do. The second factor is peripheral and is the chemical force that is transformed into mechanical work. Fatigue involves a diminution in muscular force and sensations that develop as it accrues. The central ("psychic") mechanism influences peripheral or muscular work. Even if no muscular work is being performed, the brain and the muscles are irrigated with blood. In work, fatigue increases more rapidly than the amount of work accomplished which saves the organs from injury. Mosso noted that the brain is the only organ protected from the effects of starvation. The brain continues to function as the rest of the body is ravaged and damaged by many influences. Because the brain moderates the fatigue phenomenon in exercise, fatigue is mostly an exhaustion of the nervous system.
"It has taken studies of “fatigue” more than a century to rediscover what Mosso believed to be obvious - that both the brain and the skeletal muscles alter their function during exercise; that the change in skeletal muscle function is characterized by a slowing of the force and speed of contraction; and that fatigue is principally an emotion, part of a complex regulation, the goal of which is to protect the body from harm part. So fatigue is indeed one of the human body’s “most marvelous perfections" (p. 2; references redacted).
Mosso's ideas were not immediately embraced and were supplanted by a different and more simplistic interpretation by English Nobel Laureate A. V. Hill. Hill's personal beliefs greatly influenced the results of his research and the path that physiology would follow in the many years to come. His personal beliefs were fashioned by three factors: his being a muscle physiologist, an unsatisfactory method of evaluating lactate concentrations post-exercise, and the belief that muscular work was limited by the supply of oxygen to the muscles and brain rather than by the function of the skeletal muscles (i.e., the supply of oxygen is the limiting factor in exercise. The doctrinaire of Hill's concepts led to the long-enduring beliefs that i) lactic acid is produced only under conditions of muscle anaerobiosis, and ii) muscle fatigue is caused by increased muscle lactate accumulations. The supply of oxygen to the body is the decisive factor in setting the limit to exercise.
"Hill’s model predicts that shortly before the termination of maximal exercise the oxygen demands of the exercising muscles exceed the (limiting) capacity of the heart to supply that oxygen. This causes skeletal muscle anaerobiosis with the accumulation of “poisonous” lactate (lacticacid) in the muscles. So Hill believed that the heart’s capacity to pump a large volume of blood to the active skeletal muscles was the single factor determining the human’s ability to perform maximal exercise since the higher the blood supply to muscle, the greater the exercise intensity that could be achieved before the onset of anaerobiosis and fatigue" (p.2).
The anachronism of Hill's model has been ignored for 90 years. If the heart's output limits exercise, then what limits the heart's output?
"So Hill’s complete model theorized that maximal exercise is limited by the development of myocardial failure consequent to the development of myocardial ischemia. This model is “catastrophic” since it predicts that exercise is limited by a failure of homeostasis, in this case in the regulation of cardiac function" (p. 3).
Despite occasional mention of Mosso's work and theory, the idea that peripheral fatigue was situated exclusively in the skeletal muscles and explained all forms of fatigue became the benchmark explanation.
Hill did add one final feature to his fatigue model, the protection of the ischemic heart from damage. He proposed a "governor" in either the heart or brain that reduced pumping capacity once ischemia set in. "This governor would protect the ischemic myocardium form damage in the critical period before exercise terminated" (p. 3). Unfortunately, sometime after WWII, the "governor" concept disappeared in the then next generation of exercise physiology books. With increasing electrical technology, it was established that a healthy heart does not become ischemic even in maximal exercise. Ischemia became an important diagnostic phenomenon for coronary heart disease. Instead of asserting that the failure of Hill's explanation of myocardial ischemia was sufficient to disprove his theory, exercise physiologists simply removed it from the still popular model. The original Hill pre-governor hypothesis was reborn as the sole regulator of exercise performance.
The current physiological explanation of fatigue and its moderators (a failure first of the heart and then skeletal muscle function) is subject to several problems.
Despite the above problems, the simple physiological model for fatigue is still popular. In its simplest form, it is training volume and intensity that is mainly accepted as the coaching determinant of athletes' performances.
Further problems associated with the "Hill-model" of athletic performance are i) athletes initiate and maintain different exercise intensities depending upon the expected duration of an event, and ii) competitive performances usually are of higher quality than training performances. Muscles do not have the capacity to make such judgments or adjustments and so a mental factor must be involved in producing those performance variations. "The second inexplicable observation is that humans also speed up near the end of exercise, the so-called end spurt. This finding significantly disproves the popular belief that fatigue increases progressively and inexorably during prolonged exercise so that athletes reach their most fatigued state immediately prior to the termination of exercise" (p. 4).
"In addition to these two rather obvious logical limitations to the predictions of the Hill model, are also a number of significant problems with certain physiological predictions of this model. These include: an absence of evidence that muscles become “anaerobic” during exercise; the absence of a “plateau” in oxygen consumption or cardiac output at exhaustion during maximal exercise; the failure to identify metabolites that explain why muscles “fatigue” during exercise so that “Metabolic causes for these changes (in fatigued skeletal muscle) are hard to identify”; and the absence of evidence for any catastrophic failure of organ function at exhaustion. Rather exercise always terminates with the maintenance of cellular homeostasis" (p. 4; references redacted).
Professor Noakes cites the most compelling evidence against the Hill-model as being the fact that skeletal muscle is never fully recruited during any form of exercise. Some selective recruitment of muscle fibers during exercise must occur so that fatigued fibers are replaced by fresher fibers in muscle contractions. As the fatigue states of fibers increase performance deteriorates, the most obvious feature being the degradation of skill-level (the first stage of detrimental fatigue). It is now established that fatigue in all exercise forms develops before complete muscle recruitment. Between 35 and 50% of active muscle mass is recruited during prolonged exercise and up to about 60% in maximal exercise.
The failure of the Hill-model of fatigue to accommodate the above concerns shows that it is too simple and in that simplicity would misguide individuals attempting to understand fatigue or train appropriately in sport.
"Inspired by Hill’s concept of a governor regulating human exercise performance, my colleagues and I have proposed a complex model of human exercise regulation in which human exercise performance is not limited by a failure of homeostasis in key organs like the skeletal muscles but is rather regulated in anticipation specifically to insure that no such biological failure can ever occur, at least in healthy humans. This complex regulation originates within the central nervous system; hence we have termed it the Central Governor Model to honor A.V. Hill’s original concept that a “governor” ultimately protects the body from damage during maximal exercise. This model finally re-integrates a body of evidence provided by the neuroscientists that has largely been ignored by those, principally cardio-respiratory physiologists, who have been responsible for sustaining [most of] the Hill-model for the past 90 years" (p. 4).
"Neuroscientists have shown that “. . . muscle fatigue . . . may arise not only because of peripheral changes at the level of the muscle but also because the central nervous system fails to drive the motoneurons adequately.” As a result “human muscle fatigue does not simply reside in the muscle” (p. 5). The brain is the central modifier responsible for governing exercise responses. The brain's exercise-modifying role is influenced by many factors, some are listed below:
"Exercise then begins at an intensity that the brain has determined can be sustained for the expected duration of the exercise bout. As a result all forms of exercise are submaximal since there is always a reserve of motor units in the exercising limbs that is never fully utilized even during maximal exercise especially when undertaken at altitude. Indeed recent studies show that the conventional testing of the maximum oxygen consumption produce submaximal values for oxygen consumption, a finding which seriously challenges the foundation finding on which Hill based his [original] model" (p. 6; references redacted).
"Once exercise begins, the pace is continuously modified contraction-by-contraction by continuous feedback from conscious sources including accurate information of the distance covered and of the end-point. Allowing the pace to change during exercise reduces the physiological effort required to perform a constant amount of work. Conscious deceptions that improve performance include using the Ramachandran mirror to observe the non-fatigued arm when working with the opposite arm, listening to music, the provision of inaccurate information provided by a clock that runs slowly or of the actual distance to be covered, or of the pace of a prior performance that had been deceptively increased by 2%, or of the true environmental conditions in which the exercise is being performed and the athlete’s real core body temperature response. Factors that influence performance and which are likely sensed subconsciously include the degree of arterial or cerebral oxygenation, the size of the muscle glycogen stores, the extent of fluid loss or thirst, and variables relating to the rate of heat accumulation. A variety of cooling techniques including the lower body, the neck or palms, all improve performance presumably by altering the nature of the sensory feedback to the control regions in the brain. Rinsing the mouth with carbohydrate improves performance perhaps by acting on specific brain areas. Running downhill and the presence of muscle damage or muscle soreness are all associated with reduced performance further suggesting the presence of specific sensory pathways subserving these functions. The exercise intensity may also be regulated to insure that a critical level of fatigue is not reached. If true, this requires a muscle sensor able to detect the level of fatigue in individual motor units" (p. 6; references redacted).
"A key component of the CGM [Central Governor Model] is its proposal that fatigue is not a physical event but rather an emotion that is used by the brain to regulate the exercise performance. This occurs through changes in the RPE [Rating of Perceived Exertion] which rises as a linear function of the percentage of the planned exercise bout that has been completed or which remains and which always reaches a maximum value at the termination of any truly maximal physical effort. Since the RPE rises as a linear function of the exercise duration, then it must be pre-set either before the exercise bout begins or shortly after its initiation.
. . . proposed a model of exercise regulation which “incorporates anticipatory/feedforward as well as feedback components using an expectation of exercise duration to set an initial work rate and to generate what has been termed a subconscious ‘template’ for the rate of increase in the RPE. During exercise, afferent feedback from numerous physiological systems is responsible for the generation of the conscious RPE, which is continuously matched with the subconscious template by means of adjustment in power output. The subjective rating is biologically linked, allowing the pacing strategy to be adjusted to prevent catastrophic changes in the monitored physiological variables (homeostats)”.
More recently, . . . advanced our understanding of the manner in which two separate sets of fatigue symptoms interact to determine the exercise performance. These authors wished to distinguish between the symptoms that develop during exercise, specifically the physical sensations produced by exercise as distinct from the sensations produced by the physiological/psychic effort required to continue performing a task at a chosen intensity. They note that in his original description Dr. Gunnar Borg described the RPE as a measure of an 'individual’s total physical and psychic reaction to exertion'” (pp. 6-7, references redacted).
Thus, the onset of fatigue in a performance consists of two sets of inputs: i) the physical symptoms produced by the exercise itself (e.g., the rise in lactate level, and the availability of glycogen) which rise as a linear function of exercise duration to a maximal level at the exercise termination if an optimal pacing strategy is produced, and ii) the self-generated sense of effort or psychic effort associated with a task (e.g., adhering to a pre-determined steady level of effort, and focusing on distracting mental activities). "The brain uses two distinct and separate sets of fatigue symptoms to insure that homeostasis is maintained during all forms of exercise" (p. 7).
When the psychic effort matches the exercise symptoms, performance is likely to be steady and tolerable. However, if the pace is above the capacity of the individual, the conscious perception of effort rises quickly and usually provokes an alteration in exercise intensity. That phenomenon is frequently observed in swimmers who "go out too fast" and suffer a marked reduction in swimming velocity normally for the remainder of the race. The sense of effort is modified by the motivation to perform and the sensations generated in the performance. One often sees individuals plan to execute a performance for which they have neither the adequate preparation nor the capacity to achieve. The performance starts at a desired level and then falls off to a lesser level based on the sensations from the exercise and the inability to sustain the desired level. When the sense of effort and the physical sensations exceed what was expected, performance levels are lowered to avoid harming the athlete's homeostasis. The sense of fatigue is often not an index of working capacity, but rather and index of how well (a comparison to the optimal work level) the exercise was executed.
"Summarizing the current evidence, Tanaka and Watanabe (2012) have proposed that physical fatigue is regulated by the balance between inhibitory and facilitatory influences on the motor cortex. Thus, 'sensory input from the peripheral system to the primary motor cortex (M1) decreases the motor output (supraspinal fatigue), and a neural pathway that interconnects the spinal cord, thalamus (TH), secondary somatosensory cortex, medial insular cortex, posterior insular cortex, ACC, premotor (PM) area, supplementary motor area (SMA), and M1 constitutes the inhibition system. In contrast, a facilitation system . . . that interconnects the limbic system, basal ganglia (BG), TH, orbitofrontal cortex, prefrontal cortex, ACC, PM, SMA, and M1 constitutes the facilitation system and a motivational input to this facilitation system enhances SMA and then M1 to increase the motor output to the peripheral system' (p. 730)" (p. 8).
The article disappointingly includes selected testimonies of individual champions who attest their success to a number of different psychological labels. That is unscientific. There are a considerable number of refereed articles that demonstrate the effectiveness of forms of imagery in different situations, the use of performance strategies that enhance performances as well as leading to more consistent improved performances, and suggested mental skills (e.g., positive and task-relevant self-talk, thought intensification, coping strategies, etc.). The addition of psychological content in competitive performances illustrates the role of the brain in moderating the exercise response mostly in improved manners. Unfortunately, that aspect of sport science is not reported in the article. Its inclusion would vastly improve the conclusions offered. Mental skills training is an important feature of modern coaching and athlete development.
Professor Noakes offers several hypotheses in the closing section of the article. One concerns close finishes.
"My unproven hypothesis is that in the case of a close finish, physiology does not determine who wins. Rather somewhere in the final section of the race, the brains of the second, and lower placed finishers accept their respective finishing positions and no longer choose to challenge for a higher finish. Once each runner consciously accepts his or her finishing position, the outcome of the race is decided. So just as a single athlete must “decide” to win, so too must the rest of the top finishers decide the opposite – specifically that they are not going to win" (p. 8).
"Furthermore the CGM suggests that this outcome will be strongly influenced by the manner in which the brains of the respective runners generate the sensations of fatigue during exercise. Recall that these symptoms of fatigue are entirely self-generated by each athlete’s brain and so are unique to each individual. As such they are illusionary" (p. 9).
To fully understand why performances occur and how to mould winning performances will never be understood by studying only physiological mechanisms and ignoring the role of the brain. The psychological bases of performing currently are incomplete but nevertheless improving as more acceptable research is published. Essentially, it is the pre-performance expectations of competitive levels and competencies that limit athletic achievements. To win or break records first of all has to be "believed" and planned by the athlete. In there is the far-from-understood concept of motivation which determines the seriousness and extent of a competitive performance. Winners want to win and pre-determine the extent that they will exert themselves to achieve that aim.
Implication. The fatigue experiences of performances are composed of two domains. The physical sensations generated by the level of exertion and the expected or pre-determined sensations that the athlete is willing to endure. It usually is the alteration of the second feature that improves finals performances over those exhibited in heats. Some ways of achieving those alterations are known.
Before a contest, athletes should define what they want to achieve, produce detailed descriptions of how that will be achieved, develop task-relevant strategy elements for distracting them from developing physical sensations, and attempt to keep the pre-defined level and pattern of exertion in concert with actual physical sensations of fatigue onset. Leaving such matters to the athlete to formulate without detailed and concerted instruction is unsatisfactory. Preparing thought-patterns and content to ensure the brain functions most efficiently is as important for governing the outcome of a competitive effort as is the physical work of training.
Professor Noakes' contribution to sport science has been extensive over a long period. The quality of his scientific work is impeccable. Consequently, readers are advised to obtain an original copy of this article and place it in the "most important" section of their library. Periodic re-reading of the article and this extensive abstract is warranted.
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