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.

It is improbable that athletic performances can be reduced to a single variable which allows no role for
psychological factors such as motivation, self-belief, placebo, nocebo, etc. While there often is staunch
resistance against psychological factors, there is an inadequate physiological explanation for any special
"motivation" to reach biological failure (and the health risks that it would pose).
If exercise is limited by catastrophic skeletal muscle failure, then there would be no need for the symptoms
of fatigue whose primary function must be to forestall homeostatic failures. The presence of noxious
symptoms of fatigue demonstrates that fatigue is more complex than a simple organic failure.
The physiological model suggests the best athletes have the largest hearts and the greatest capacity to
transport and consume oxygen. Evidence does not support that. The common measure, VO2max, is not a
good predictor of athletic ability or changes in performances associated with training.
One would expect cardiac output to always be maximal during all forms of exercise. That is untrue.

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.

A Viable Fact-based Alternative

"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:

1. The biological state of the athlete at the start of exercise including the emotional state, the extent of mental
fatigue or sleep deprivation, the state of recovery from a previous exercise bout, the level of motivation
and prior experience, and the degree of self-belief including superstitious beliefs.
2. Factors specific to the event that alter performance include monetary reward, prior knowledge of the
exercise end-point, and the presence of competitors especially if they are of similar ability.
3. A number of chemical agents including the stimulants amphetamine, caffeine, pseudoephedrine, modafinil,
and the dopamine/noradrenaline reuptake inhibitor bupropion - as well as the analgesic, acetaminophen or
the analgesic naloxone , or the cytokines interleukin-6 (IL-6), or brain IL-1?. All have been shown to alter
exercise performance as do placebos.
4. Psychological skills training or pre-exercise whole-body cooling can also improve subsequent exercise
performance.
5. Additionally, this Editor's own psychological research has shown performances to be altered for the better
not only by appropriate mental skills training, but by positive, mood-specific, and task-relevant thought
content, the restructuring of an extensive task into segments, the length of self-controlled and self-centered
task-specific thought content, the intensity of task-relevant thought content, and the preparation of coping
strategy elements if primary task elements fail to produce expected performance elements.

"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).

Sensations and Fatigue

"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.
The Mechanism in the Brain

"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).

Mind over Muscle?

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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