Bouncing to conclusions: clear evidence for the metabolic cost of generating muscular force
2011; American Physiological Society; Volume: 110; Issue: 4 Linguagem: Inglês
10.1152/japplphysiol.00120.2011
ISSN8750-7587
Autores Tópico(s)Sensor Technology and Measurement Systems
ResumoInvited EditorialsBouncing to conclusions: clear evidence for the metabolic cost of generating muscular forceRodger KramRodger KramDepartment of Integrative Physiology, University of Colorado, Boulder, ColoradoPublished Online:01 Apr 2011https://doi.org/10.1152/japplphysiol.00120.2011This is the final version - click for previous versionMoreSectionsPDF (45 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat to try and understand the biomechanical basis for the metabolic demand of locomotion, scientists have gone to extreme measures. Exercise physiologists have studied Olympic athletes. Comparative physiologists have studied mice running on treadmills with tiny backpacks (12) and even trained elephants to breathe through garbage cans attached to their trunks while they walk behind motorized golf carts (6). Engineers have employed supercomputers to model nearly every muscle in legs (1). Yet, as Dean and Kuo (4) demonstrate in this issue of the Journal of Applied Physiology, sometimes simple is best.Dean and Kuo's paper has its roots in Dawson and Taylor's watershed 1973 paper on the energetics of kangaroo hopping (3). As a young physiologist and runner, I was stunned to learn that red kangaroos (Macropus rufus) could hop along at a jogging pace or rapidly at 6 m/s and yet consume oxygen at the same rate. While I could only dream of running a 4-minute mile, these marvelous marsupials could comfortably cruise at nearly that pace, idling along at just a third of their maximal rate of oxygen consumption. We now know that much of the kangaroo's “secret” resides in their long, slender Achilles tendons that store and return mechanical energy during each hop (2). But even for a kangaroo, locomotion is not free. To operate the tendon springs, the muscles must generate tension forces. Further, the tendon springs are not ideal, and so the muscles must also perform some mechanical work. Work, of course, is equal to the product of force and displacement. Isometric muscle actions involve force but no length change, and hence no mechanical work. Thus there can be no work without force, but there can be force without work.Kangaroos are extreme but they are not unique. Humans and other animals exploit the elastic properties of tendons to varying degrees when they walk, run, hop, trot, or gallop. To quantify the various combinations of mechanical work and force production at the level of the skeletal muscle, Roberts et al. (9) pioneered direct in vivo measurements of tendon force and muscle fiber displacement (using sonomicrometry) in running wild turkeys. They showed that during level running, there was near-isometric force production in the gastrocnemius muscle fibers and thus little work performed. Since sonomicrometry is invasive, Lichtwark and colleagues (7) have used ultrasound to measure muscle fiber excursions in the calf muscles of walking and running humans. But the actions of single muscle tendons cannot be confidently extrapolated to the whole leg or whole body, and ultrasound techniques have only been successful with superficial muscles. In contrast, the metabolic cost of human locomotion can only be readily measured at the whole body level. Thus the field has been stymied in our efforts to better relate locomotion mechanics (i.e., work vs. force) and energetics at the whole body level.Refreshingly, Dean and Kuo (4) present a clever experiment in which human subjects systematically “bounced” in place at prescribed frequencies and amplitudes such that the external mechanical work rate remained nearly constant. The subjects did not hop into the air like kangaroos; rather, they kept their feet on the ground and used only their calf musculature and tendons to cause the movements (the knee joints were splinted). Dean and Kuo calculated metabolic rate of the whole body, using standard expired gas analysis, and focused on the energy used above that at rest. When the net metabolic rates were plotted vs. bounce frequency, a U-shape pattern emerged with a minimum at ∼3 Hz, a resonant frequency that optimized the elastic energy storage and return from tendons while apparently minimizing the work done by the muscle fibers themselves.To noninvasively gain insight into how the muscle fibers and tendons were behaving, Dean and Kuo, both engineers, used a powerful modeling technique called parameter or system identification (8). We physiologists would be wise to collaborate with our engineering colleagues more often. The results of their modeling showed that at slow bouncing frequencies (1 Hz), the forces and thus the Achilles tendon-spring stretching were small so the majority of the mechanical work was performed actively by the muscle fibers. In contrast, at a 3-Hz bounce frequency, the muscle stretch and shortening amplitude were much smaller. As a result, the muscle work and overall metabolic cost was much less. At faster bouncing frequencies, the muscle work was greater as was the metabolic cost. The calculated overall efficiency was ∼25% at both slow and rapid bouncing and peaked at 45% for 3-Hz bouncing. Neither the authors nor I think that the actual efficiency of the muscle itself is changing by that much. Rather, the efficiency appears to be very high at resonance because what appears to be work when viewed externally is due primarily to passive elastic recoil of tendons, not active muscle work. To me, the big take-home message of Dean and Kuo is that under optimal conditions, as much as 60% of the metabolic cost of a whole body movement can be attributed to the cost of generating muscular force. That figure is remarkably similar to the 70% ascribed to the cost of generating force in human running (10).Still, Dean and Kuo's study was deliberately limited to the ankle joint, which has rather prominent tendons. Walking and running are complex movements with many muscle actions across multiple joints. Thus it is unclear how well the actions of a single joint-muscle-tendon complex represent the whole leg. Further, because force and work vary across gait and speed, the energetic cost of each may be apportioned differently.On a related note, human hopping energetics with wearable exoskeletons was the focus of a recent paper by Grabowski and Herr in the Journal of Applied Physiology (5). Their springy carbon-fiber exoskeleton augmented the muscle-powered actions of the legs and reduced the metabolic cost by 24%. Since it was not their intent, that study could not distinguish what fraction of the savings were due to reductions in muscle force vs. muscle work. But perhaps their exoskeleton technique can be synthesized with the fixed work rate approach of Dean and Kuo?For roughly two decades, Dick Taylor and his many colleagues devoted themselves to quantifying how mechanical work and force combine to determine the metabolic demand of locomotion across animal diversity, size, and locomotor speed. In one of his final scientific papers, Taylor outlined what has become known as the “cost of generating force” hypothesis (11). Dean and Kuo provide an innovative set of data that unequivocally add credence to that hypothesis.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the author(s).REFERENCES1. Anderson FC , Pandy MG . Dynamic optimization of human walking. J Biomech Eng 123: 381–391, 2001.Crossref | PubMed | ISI | Google Scholar2. Biewener AA , Baudinette RV . In vivo muscle force and elastic energy storage during steady-speed hopping of tammar wallabies (Macropus eugenii). J Exp Biol 198: 1829–1841, 1998.Google Scholar3. Dawson TJ , Taylor CR . Energetic cost of locomotion in kangaroos. Nature 246: 313–314, 1973.Crossref | ISI | Google Scholar4. Dean JC , Kuo AD . Energetic costs of producing muscle work and force in a cyclical human bouncing task. J Appl Physiol (January 6, 2011). doi:10.1152/japplphysiol.00505.2010.Link | ISI | Google Scholar5. Grabowski AM , Herr HM . Leg exoskeleton reduces the metabolic cost of human hopping. J Appl Physiol 107: 670–678. 2009.Link | ISI | Google Scholar6. Langman VA , Roberts TJ , Black J , Maloiy GMO , Heglund NC , Weber JM , Kram R , Taylor CR . Moving cheaply: energetics of walking in the African elephant. J Exp Biol 198: 629–632, 1995.ISI | Google Scholar7. Lichtwark GA , Bougoulias K , Wilson AM . Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. J Biomech 40: 157–164, 2007.Crossref | PubMed | ISI | Google Scholar8. Ljung L . System Identification: Theory for the User. Upper Saddle River, NJ: Prentice-Hall, 1999.Crossref | Google Scholar9. Roberts TJ , Marsh RL , Weyand PG , Taylor CR . Muscular force in running turkeys: the economy of minimizing work. Science 275: 1113–1115, 1997.Crossref | ISI | Google Scholar10. Roberts TJ , Kram R , Weyand PG , Taylor CR . Energetics of bipedal running I. metabolic cost of generating force. J Exp Biol 201: 2745–2751, 1998.ISI | Google Scholar11. Taylor CR . Relating mechanics and energetics during exercise. Adv Vet Sci Comp Med 38A: 181–215, 1994.PubMed | Google Scholar12. Taylor CR , Heglund NC , McMahon TA , Looney TR . Energetic cost of generating muscular force during running: a comparison of small and large animals. J Exp Biol 86: 9–18, 1980.ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: R. Kram, UCB354, Dept. of Integrative Physiology, Univ. of Colorado, Boulder, Boulder, CO 80309-0354 (e-mail: rodger.kram@colorado.edu). Download PDF Back to Top Next FiguresReferencesRelatedInformation Cited ByReduced prosthetic stiffness lowers the metabolic cost of running for athletes with bilateral transtibial amputationsOwen N. Beck, Paolo Taboga, and Alena M. Grabowski11 April 2017 | Journal of Applied Physiology, Vol. 122, No. 4 More from this issue > Volume 110Issue 4April 2011Pages 865-866 Copyright & PermissionsCopyright © 2011 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.00120.2011PubMed21292841History Published online 1 April 2011 Published in print 1 April 2011 Metrics
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