Article - Running On Empty

New Scientist vol 181 issue 2439 - 20 March 2004, page 42

Your lungs are bursting and your muscles are screaming at you to stop. Can it really be possible that fatique is all in the mind? Rick Lovett reports

TIMOTHY NOAKES will never forget the day he encountered the hill from hell. It was 1976 and he was running the gruelling Comrades Marathon, an annual 90-kilometre road race between Durban and Pietermaritzburg in South Africa. About 20 kilometres from home he rounded a bend and saw a steep incline he hadn't known was there. Even before he started climbing, he suddenly began to feel overwhelmingly tired.

At the time it was just a case of gritting his teeth. But Noakes, a professor of exercise physiology at the University of Cape Town, South Africa, soon came to see that hill as an intellectual mountain, too. Why had the very thought of it made him feel so tired?

Conventional wisdom on muscle fatigue can't explain what happened that day. For the better part of a century, scientists and athletes have presumed, not unreasonably, that fatigue originates in the muscles themselves. Precise explanations have varied, but all have been based on the "limitations theory". In other words, muscles tire because they hit a physical limit: they either run out of fuel or oxygen or they drown in toxic by-products.

In the past few years, however, Noakes and his colleague Alan St Clair Gibson have taken a hard look at the standard theory. The deeper they dig, the more convinced they have become that physical fatigue simply isn't the same as a car running out of petrol. Fatigue, they argue, is caused not by distress signals springing from overtaxed muscles, but is an emotional response which begins in the brain.

The essence of their new theory is that the brain, using a mix of physiological, subconscious and conscious cues, paces the muscles to keep them well back from the brink of exhaustion. When the brain decides it's time to quit, it creates the distressing sensations we interpret as unbearable muscle fatigue. This "central governor" theory remains controversial, but it does explain many puzzling aspects of athletic performance, as well as suggesting some revolutionary approaches to training and offering tantalising hints as to the cause and maybe even the cure of chronic fatigue syndrome.

The hill from hell might have set Noakes thinking about fatigue, but it was a more recent discovery that made him start researching it in earnest. He calls this the "lactic acid paradox". Lactic acid is a by-product of exercise, and its build-up is often cited as a cause of fatigue. But when research subjects exercise in a decompression chamber designed to simulate high altitude, they become fatigued even though lactic acid levels remain low. Nor has the oxygen content of their blood fallen too low for them to keep going. Obviously, Noakes deduced, something else was making them tire well before they hit either physiological limit.

Noakes and St Clair Gibson decided to probe further. For their first study, published in 2001 (American Journal of Physiology - Regulatory Integrative and Comparative Physiology, vol 281, p R187), they recruited seven experienced cyclists and asked them to pedal 100-kilometre time trials on stationary exercise bikes. On several occasions during the time trial, they asked the cyclists to sprint for 1000 or 4000 metres. Throughout the experiment, the cyclists wore electrical sensors taped to their legs to measure the nerve impulses travelling to their muscles.

It has long been known that during exercise, the body never uses 100 per cent of the available muscle fibres in a single contraction. The amount used varies with the length of the endeavour, but in endurance tasks such as the cycling test the body calls on about 30 per cent, spreading the load by rotating in fresh ones as needed. And because separate nerve filaments send signals to each fibre, sports scientists can determine what fraction of the muscle is being used by measuring the electrical impulse travelling to it.

Noakes reasoned that if the limitations theory was correct and fatigue was due to muscle fibres hitting some limit, the number of fibres used for each pedal stroke should increase as the fibres tired and the cyclist's body attempted to compensate by recruiting an ever-larger fraction of the total. But his team found exactly the opposite. As fatigue set in, the electrical activity in the cyclists' legs declined - even during the sprints, when they were striving to cycle as fast as they could.

Plenty in the tank

To Noakes, this was strong evidence that the old theory was wrong. The cyclists may have felt completely done in, he says, but their bodies actually had considerable reserves that they could theoretically tap by using a greater fraction of the resting fibres. This, he believes, is proof that the brain is regulating the pace of the workout to hold the cyclists well back from the point of catastrophic exhaustion.

More evidence comes from the fact that fatigued muscles don't actually run out of anything critical. Muscle biopsies have shown that levels of glycogen, which is the muscles' primary fuel, and ATP, the chemical they use for temporary energy storage, decline with exercise but never bottom out. Even at the end of a marathon, ATP levels are 80 to 90 per cent of the resting norm. And while glycogen levels approach zero, they never get there. Post-marathon muscles also still have substantial reserves of other fuels, notably fat.

Still more evidence in favour of the central regulator comes from observations of the closing stages of distance races. Top athletes almost always manage to go their fastest during the last kilometre of a race, even though, theoretically, that's when their muscles should be closest to exhaustion. In particular, Noakes says, the end spurt makes no sense if fatigue is caused by muscles poisoning themselves with lactic acid. If lactic acid build-up is the limiting factor, racers would progressively slow down and would find it impossible to sprint for the finish line.

But with the central governor theory, the explanation is obvious. Knowing the end is near, the brain slightly relaxes its vigil and allows the athlete to tap a bit of the body's carefully hoarded reserves.

But the central governor theory does not mean that what's happening in the muscles is irrelevant. The governor constantly monitors physiological signals from the muscles, along with other information, to set the level of fatigue. A large number of signals are probably involved, but the ones Noakes is most sure about include the body's remaining stores of carbohydrates, the levels of glucose and oxygen in the blood, the rates of heat generation and heat loss, and the rate at which muscles are working. Where the central governor theory differs from the limitations theory is that these physiological factors are not the direct determinants of fatigue - they are just information to take into account.

Conscious factors can also intervene. Noakes believes that the central regulator evaluates the planned workout, and sets a pacing strategy accordingly. Experienced runners know, for example, that if they set out on a 10-kilometre training run, the first kilometre feels mysteriously easier than the first kilometre of a 5-kilometre run, even though there should be no difference. That, Noakes says, is because the central governor knows you have farther to go in the longer run and has programmed itself to dole out fatigue symptoms accordingly.

This can be verified by putting people on treadmills and telling them they're going to run one distance when in fact you have another planned. When the subjects are given the real story midway through the test, their reported levels of fatigue suddenly adjust to account for the new information.

It also explains Noakes's experience on the hill from hell. "The central governor had been pacing me for another 20 kilometres," he says, "but it had presumed it was going to be flat. Now, it suddenly had to take the hill into account, and it forced me to slow down."

St Clair Gibson believes there is a good reason why our bodies are designed to keep something back. That way, there's always something left in the tank for an emergency. In ancient times, an emergency might take the form of a lion or pack of wolves at the end of a long, gruelling hunt. Today, the "wolf" might be a mugger hiding in an alley, or a lightning storm near the end of a long hike. But the same concept applies: life would be too dangerous if our bodies allowed us to become so tired that we couldn't move quickly when faced with an unexpected need.

Drugs and hypnosis

The team also believes the central governor theory helps to explain why hypnosis helps block sensations of fatigue, allowing athletes to work harder. If fatigue were merely the result of hitting the muscles' physiological limits, this shouldn't be possible. But it is. Amphetamines have a similar effect, and again it could be down to the central governor. Blocking the sensation of fatigue with drugs, however, makes it much easier to work yourself to death. Normally, fatigue will force even the most iron-willed competitor to quit before they succumb to heatstroke, but this didn't happen for the British cyclist Tom Simpson, who died after taking amphetamine during the Tour de France in 1967, the year before drug tests started. Ecstasy, Noakes adds, is an amphetamine-like substance that could have the same effect on clubbers.

The theory could also help to unravel the mystery of chronic fatigue syndrome. Perhaps something has interfered with the brain's regulation of fatigue so that you always feel exhausted even though you are not. Successfully puzzling out the workings of the central governor might open the door to a long-awaited cure, Noakes suggests.

St Clair Gibson and Noakes are presently trying to find where the central governor is located in the brain by studying the electroencephalograms (EEGs) of tiring cyclists. "We're finding that a lot of areas of the brain are involved," St Clair Gibson says, "but we haven't yet found the stop switch." However, the mix of such areas is interesting, and includes the frontal lobe (which is involved in decision making), the parietal lobe (which is involved in sensation), and, for some reason, the visual and speech centres.

The central governor theory has found favour with other exercise physiologists. George Brooks at the University of California, Berkeley, for example, recently amended his textbook to include it. But for some it remains controversial.

One critic is Jere Mitchell, a cardiologist at the University of Texas Southwestern Medical Center, Dallas. He points to treadmill tests in which people run up ever-steeper slopes while having their oxygen consumption measured. Shortly before the subjects collapse in exhaustion, their oxygen consumption reaches a plateau beyond which it won't increase, no matter how hard they try to work.

This maximum rate of oxygen consumption, called VO2 max, can be boosted by increasing the number of red blood cells in circulation - for example, by re-injecting blood that was taken several weeks earlier. This proves that fatigue has nothing to do with any central governor, Mitchell argues. Instead, it kicks in at the point at which the body has bumped into a very real physiological limit - the amount of oxygen the blood can transport.

Peter Wagner of the University of California, San Diego, concurs. He has conducted treadmill tests in which athletes are tested under two different conditions: on normal air, and on pure oxygen. That is enough to produce an 8 to 10 per cent increase in the amount of oxygen going to the muscles, he says, producing a measurable increase the VO2 max in well-trained athletes.

Noakes and St Clair Gibson, however, argue that the central governor theory can explain both studies. The brain, they say, senses the elevated amount of oxygen in the blood and then "resets" the pace to allow the athlete to work harder, while still maintaining a reserve. "So there is a ceiling of oxygen use," says St Clair Gibson, "but at a level decided by the brain, with a wide margin of reserve for error."

If the central governor theory does prove to be correct, can coaches use it to improve athletes' performance? Noakes's experience on the Comrades Marathon underscores the importance of knowing the course beforehand - particularly its later stages. Top athletes and coaches figured that one out many years ago. In fact, says Brooks, trainers are often ahead of the science. "Coaches, by experience, have discovered things which scientists take longer to understand," he says. But Noakes argues that the central governor theory helps make sense of interval training, a "sharpening" technique in which athletes do repetitive bouts of high-intensity exercise interspersed with recovery breaks (see Graphic).

In a recent experiment, Noakes took a group of cyclists who had never done intervals before and asked them to add them to their normal training, once or twice a week for six weeks. At the end of this programme the cyclists, who were fast recreational riders but not professional racers, had shaved a startling 15 minutes, or approximately 10 per cent, off their previous times on a 100-kilometre time trial.

Similarly dramatic improvements are often observed when runners are introduced to interval training. Traditional theory says that the improvement is due to physiological changes in the muscle cells that make them better able to use oxygen or tolerate the build-up of metabolic waste products. But Noakes doesn't see how major physiological improvements can occur so quickly. And in any case, he says, interval training seems to induce very little, if any, biochemical change in the muscle. He believes that interval training works largely by teaching the central governor that going faster won't do you any harm.

Perhaps, then, the central governor idea can be used to give athletes an important mental edge. Simply telling them that even when they are feeling completely exhausted their bodies actually have a lot in reserve should provide an incredible psychological boost, says St Clair Gibson. "When athletes know that," he says, "it's going to be exciting."

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