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J Physiol 587.11 (2009) pp 2425–2426 2425 JOURNAL CLUB Go rinse your mouth: a novel way to improve endurance performance? Nicolas Place Institut des Sciences du Mouvement et de la edecine du Sport, Universit´ e de Gen` eve, Geneva, Switzerland Email: [email protected] Who would have ever believed that just rinsing one’s mouth with a sports energy drink and not swallowing but spitting it out would improve endurance performance? Not me, at least not until reading the exciting study of Chambers et al. (2009), which considerably challenges our current under- standing of exercise physiology. And the evidence of the mechanisms underlying this unexpected finding is puzzling. Peak performances in endurance sports are realized by individuals who are able to limit the decrease in speed or power output (i.e. fatigue) while competing. The factors limiting endurance performance of prolonged exercise, i.e. the causes of fatigue, remain incompletely understood. Generally, fatigue is explained in terms of limits to oxygen transport capacity and/or muscle metabolic capacity and/or the development of central and peri- pheral fatigue. Numerous experiments have established that intramuscular processes are impaired during repeated muscle activation. For example, intact single fibres repeatedly stimulated show a decreased force production intimately related to alterations in Ca 2+ handling, which can explain the reduction in muscle force production associated with prolonged exercise in humans under certain conditions (Allen et al. 2008). Although fatigue can develop within muscle fibres, motor unit activity is centrally modulated. Indeed, the descending neural drive from the brain to the exercising muscles determines the strategy in terms of motor unit recruitment and de-recruitment during prolonged exercise, and therefore the force-generating capacity of the muscle (Kayser, 2003). Thus, the development of central fatigue would be set above a safe level via integration of multiple neural and humoral inputs to maintain body homeostasis during repeated or sustained muscle contractions. If the safety margin is threatened, the functional outcome would be a reduced neural drive, leading to decreased muscle activity and thus a lowering of exercise intensity or task failure depending on the details of the task. In a recent issue of The Journal of Physio- logy , Chambers et al. (2009) assessed the effect of mouth rinsing with carbohydrate solutions on a cycle time trial of 1h duration. Chambers et al. (2009) used functional magnetic resonance imaging in a second set of experiments to identify brain areas eventually activated by oral carbohydrates. Trained cyclists performed time trials simulated on a cycle ergometer (separated by at least 3 days) in a fasted (> 6 h) state, where they had to complete a fixed workload (corresponding to 1h at 75% maximal work) when complemented with glucose, maltodextrin or placebo (saccharin) solutions. An artificial sweetener was used to reduce sensory clues between solutions. Sub- jects were asked every 12.5% of the time trial to rinse the solution in the mouth for 10 s but not to swallow anything. Intriguingly, the results showed that a 6.4% carbohydrate solution produced an astonishing improvement of 2–3% as indicated by the average power output, when compared to the placebo solution. This could equate to more than 1 min difference in the longer time trials in the Tour de France. The rate of perceived exertion (RPE) was not different between conditions, which led the authors to suggest that oral exposure to carbohydrate reduces the perception of exertion for a given workload allowing them to increase power output during the time trial. The authors hypothesized that the caloric content detected by ‘unidentified receptors’ might mediate a neural response. Neuroimaging measurements then were performed while the subjects at rest rinsed their mouth in the same manner as they did while cycling, showing that oral carbohydrates acted via supraspinal pathways during exercise. Brain activation was similar with glucose and maltodextrin solutions, and brain regions were activated, including the anterior cingulated cortex (ACC), that were not activated with placebo. Previous reports using hypnosis during cycling exercise have shown that ACC activity is closely related to RPE; ACC blood flow decreased when subjects cycled on a cycle ergometer under hypnosis while perceiving a down- hill descent compared to a flat, level grade (Williamson et al. 2001). Furthermore, results from Marcora et al. (2009) show that mental fatigue induced by a cognitive task prior to exercise significantly reduces the time to exhaustion when cycling at a workload corresponding to 80% of peak power output. The alteration in endurance performance was attributed to the higher RPE during exercise performed after induction of mental fatigue: a possible implication of the ACC, although this was not quantified, was suspected (Marcora et al. 2009). The novel findings of Chambers et al. (2009) move us forward. They show, for the first time, that central fatigue development during prolonged exercise may be post- poned or attenuated by activating brain regions that were possibly inactive or inhibited. Nevertheless, these results raise several new questions: what are the receptors that convey sensory information from the mouth to the brain? Would the same results have been observed in a competition situation, i.e. in a fed state? Would it be possible to observe improvements in performance in highly trained athletes? Indeed, one can calculate that performance over a half-marathon (1 h duration) not realized in the heat would be improved if the athlete does not swallow the solution by preventing (i) any, even minor, weight gain and (ii) risks of gastrointestinal problems, frequently observed in running. Thus, it appears important to attempt to address some of these questions with the use of oral carbohydrates combined with non-invasive methods such as surface electromyography and transcranial magnetic stimulation of the motor cortex. In summary, Chambers et al. (2009) show an unexpected pathway exists to counter- act central fatigue development. Although central fatigue is difficult to quantify, this pioneer study again underlines the fact that the brain must always be considered when studying fatigue. Further studies are needed to extend these data and identify the underlying mechanisms explaining the non-metabolic, central positive impact of oral carbohydrates in order to optimize endurance performance. Puzzled I may be, C 2009 The Author. Journal compilation C 2009 The Physiological Society DOI: 10.1113/jphysiol.2009.172874

Go rinse your mouth: a novel way to improve endurance performance?

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J Physiol 587.11 (2009) pp 2425–2426 2425

JOURNAL CLUB

Go rinse your mouth: a novelway to improve enduranceperformance?

Nicolas PlaceInstitut des Sciences du Mouvement et de laMedecine du Sport, Universite de Geneve,Geneva, Switzerland

Email: [email protected]

Who would have ever believed that justrinsing one’s mouth with a sports energydrink and not swallowing but spitting it outwould improve endurance performance?Not me, at least not until reading the excitingstudy of Chambers et al. (2009), whichconsiderably challenges our current under-standing of exercise physiology. And theevidence of the mechanisms underlying thisunexpected finding is puzzling.

Peak performances in endurance sportsare realized by individuals who are ableto limit the decrease in speed or poweroutput (i.e. fatigue) while competing. Thefactors limiting endurance performanceof prolonged exercise, i.e. the causes offatigue, remain incompletely understood.Generally, fatigue is explained in termsof limits to oxygen transport capacityand/or muscle metabolic capacity and/orthe development of central and peri-pheral fatigue. Numerous experiments haveestablished that intramuscular processesare impaired during repeated muscleactivation. For example, intact single fibresrepeatedly stimulated show a decreasedforce production intimately related toalterations in Ca2+ handling, which canexplain the reduction in muscle forceproduction associated with prolongedexercise in humans under certain conditions(Allen et al. 2008). Although fatigue candevelop within muscle fibres, motor unitactivity is centrally modulated. Indeed, thedescending neural drive from the brainto the exercising muscles determines thestrategy in terms of motor unit recruitmentand de-recruitment during prolongedexercise, and therefore the force-generatingcapacity of the muscle (Kayser, 2003). Thus,the development of central fatigue wouldbe set above a safe level via integrationof multiple neural and humoral inputs to

maintain body homeostasis during repeatedor sustained muscle contractions. If thesafety margin is threatened, the functionaloutcome would be a reduced neural drive,leading to decreased muscle activity andthus a lowering of exercise intensity or taskfailure depending on the details of the task.

In a recent issue of The Journal of Physio-logy, Chambers et al. (2009) assessed theeffect of mouth rinsing with carbohydratesolutions on a cycle time trial of ∼1 hduration. Chambers et al. (2009) usedfunctional magnetic resonance imaging ina second set of experiments to identifybrain areas eventually activated by oralcarbohydrates. Trained cyclists performedtime trials simulated on a cycle ergometer(separated by at least 3 days) in afasted (> 6 h) state, where they had tocomplete a fixed workload (correspondingto 1 h at 75% maximal work) whencomplemented with glucose, maltodextrinor placebo (saccharin) solutions. Anartificial sweetener was used to reducesensory clues between solutions. Sub-jects were asked every 12.5% of thetime trial to rinse the solution in themouth for ∼10 s but not to swallowanything. Intriguingly, the results showedthat a 6.4% carbohydrate solution producedan astonishing improvement of 2–3% asindicated by the average power output,when compared to the placebo solution.This could equate to more than 1 mindifference in the longer time trials in theTour de France. The rate of perceivedexertion (RPE) was not different betweenconditions, which led the authors to suggestthat oral exposure to carbohydrate reducesthe perception of exertion for a givenworkload allowing them to increase poweroutput during the time trial. The authorshypothesized that the caloric contentdetected by ‘unidentified receptors’ mightmediate a neural response. Neuroimagingmeasurements then were performed whilethe subjects at rest rinsed their mouthin the same manner as they did whilecycling, showing that oral carbohydratesacted via supraspinal pathways duringexercise. Brain activation was similar withglucose and maltodextrin solutions, andbrain regions were activated, including theanterior cingulated cortex (ACC), that werenot activated with placebo. Previous reportsusing hypnosis during cycling exercise

have shown that ACC activity is closelyrelated to RPE; ACC blood flow decreasedwhen subjects cycled on a cycle ergometerunder hypnosis while perceiving a down-hill descent compared to a flat, level grade(Williamson et al. 2001). Furthermore,results from Marcora et al. (2009) showthat mental fatigue induced by a cognitivetask prior to exercise significantly reducesthe time to exhaustion when cycling at aworkload corresponding to 80% of peakpower output. The alteration in enduranceperformance was attributed to the higherRPE during exercise performed afterinduction of mental fatigue: a possibleimplication of the ACC, although this wasnot quantified, was suspected (Marcora et al.2009). The novel findings of Chambers et al.(2009) move us forward. They show, for thefirst time, that central fatigue developmentduring prolonged exercise may be post-poned or attenuated by activating brainregions that were possibly inactive orinhibited. Nevertheless, these results raiseseveral new questions: what are the receptorsthat convey sensory information from themouth to the brain? Would the sameresults have been observed in a competitionsituation, i.e. in a fed state? Would itbe possible to observe improvements inperformance in highly trained athletes?Indeed, one can calculate that performanceover a half-marathon (∼1 h duration) notrealized in the heat would be improved ifthe athlete does not swallow the solution bypreventing (i) any, even minor, weight gainand (ii) risks of gastrointestinal problems,frequently observed in running. Thus, itappears important to attempt to addresssome of these questions with the use of oralcarbohydrates combined with non-invasivemethods such as surface electromyographyand transcranial magnetic stimulation ofthe motor cortex.

In summary, Chambers et al. (2009) showan unexpected pathway exists to counter-act central fatigue development. Althoughcentral fatigue is difficult to quantify, thispioneer study again underlines the factthat the brain must always be consideredwhen studying fatigue. Further studies areneeded to extend these data and identifythe underlying mechanisms explaining thenon-metabolic, central positive impact oforal carbohydrates in order to optimizeendurance performance. Puzzled I may be,

C© 2009 The Author. Journal compilation C© 2009 The Physiological Society DOI: 10.1113/jphysiol.2009.172874

2426 Journal Club J Physiol 587.11

but I am also excited about the prospect offuture findings.

References

Allen DG, Lamb GD & Westerblad H (2008).Skeletal muscle fatigue: cellular mechanisms.Physiol Rev 88, 287–332.

Chambers ES, Bridge MW & Jones DA (2009).Carbohydrate sensing in the human mouth:effects on exercise performance and brainactivity. J Physiol 587, 1779–1794.

Kayser B (2003). Exercise starts and ends in thebrain. Eur J Appl Physiol 90, 411–419.

Marcora SM, Staiano W & Manning V (2009).Mental fatigue impairs physical performancein humans. J Appl Physiol 106, 857–864.

Williamson JW, McColl R, Mathews D, MitchellJH, Raven PB & Morgan WP (2001). Hypnoticmanipulation of effort sense during dynamicexercise: cardiovascular responses and brainactivation. J Appl Physiol 90, 1392–1399.

Acknowledgements

I would like to thank Professor B. Kayser andDr J. D. Bruton for reading this manuscript andtheir constructive comments.

C© 2009 The Author. Journal compilation C© 2009 The Physiological Society