The total limb force production, determined as a peak vertical GRF, reached 3.82 ± 0.51 body weight (BW) during hopping (Table 2). In walking, running, and sprinting, peak vertical GRF values were 2.58, 0.68, and 0.47 BW greater, respectively, compared with hopping (P < 0.001, P < 0.001, and P < 0.01). Ground contact time was 0.17 ± 0.02 s for hopping, which was significantly shorter than that for walking (0.63 ± 0.02 s, P < 0.001) and running (0.21 ± 0.02 s, P < 0.001), but longer than that for sprinting (0.12 ± 0.01, P < 0.001).
To approximate muscle contractile conditions during measured tasks, we analyzed joint angles and angular velocities at the time of peak extensor muscle forces. At the knee level, flexion angles at the time of peak knee extensor force (FKmax) were 32.9°, 12.9°, and 12.0° greater during hopping compared with walking, running, and sprinting, respectively (P < 0.001, P < 0.001, and P < 0.01; Table 1). Furthermore, at the time of peak ankle extensor force (FAmax), the ankle plantarflexion angles were 14.5° and 4.3° greater during hopping than during walking and running, respectively (P < 0.001 and P < 0.05; Table 1). Knee angular velocities at FKmax were relatively low and showed no significant differences between hopping and locomotor tasks. At the ankle level, angular velocities at FAmax in walking showed positive values and differed significantly (P < 0.05) from hopping where negative velocity was present at FAmax (Table 1). An analysis of relative efforts using joint angular velocity matched reference force values had minimal effects on the operating levels of the muscle groups (Table 1).
The present article provides the most comprehensive description available to date of operating muscular efforts of human primary locomotor muscles across walking, running, and sprinting. The results highlight that, regardless of the mode of locomotion, humans operate at a clearly greater proportion of capacity at the ankle than knee extensor muscles. This observation offers a new insight into biomechanical constraints of human locomotor ability and provides the basis for better understanding of the mechanisms that influence the way we locomote and adapt to accommodate compromised neuromuscular system function.
As expected, during walking, the participants operated at a greater proportion of capacity at the ankle than knee extensor muscles. The relative force of the ankle extensors was almost two times greater compared with the knee extensors, which is consistent with previous studies (4,7); however, the relative level at which both muscle groups were operating was remarkably lower in the present study. Our analysis demonstrate 19% and 35% operating force for the knee and ankle extensors, respectively, whereas previous studies (4,7) have reported a relative level approximately two times greater for both muscle groups, when normalization to the maximum isokinetic force reference test was used. Nevertheless, the current and previous observations (4,7) imply that during walking, much lower muscular reserve is available at the ankle than knee extensors to buffer any loss of muscular capacity. Consequently, these findings may explain why muscular weakness, for example, due to aging, typically first challenges the normal function of the ankle extensors during walking, leading to compensatory actions such as shorter steps and shift of the joint kinetics from the ankle toward more proximal joints (4,9,25).
When gait was changed from a walk to a run (4.1 ± 0.2 m·s−1), the peak extensor muscle forces increased more at the knee (3.2-fold) than the ankle level (2.5-fold). This result was expected because of a considerable decrease in knee extensor effective mechanical advantage that occurs during running due to deeper knee flexion (5). As a result, the difference in the relative effort between muscle groups decreased, but still, the ankle extensors operated at a significantly greater proportion of capacity than the knee extensors (84% vs 63%). Consequently, running gait appears to require clearly greater operating effort from the ankle than knee extensors. This suggests that the ankle extensors may be more prone to running-induced muscular fatigue than the knee extensors, which would possibly make declined ankle propulsion ability a key limiting factor of prolonged running performance. Although no direct evidence for this has yet appeared, previous studies (39,42) have reported a significant reduction in the extensor muscle EMG at the ankle but not at the knee during intensive long-distance running, thus supporting the suggestion of a greater level of fatigue in the ankle extensors.
The above findings may also shed new light on understanding why the majority of both recreational and competitive runners favor using a rearfoot rather than forefoot striking pattern (28), if sufficient cushion, provided by the shoe or surface, is available (30). According to a long-standing hypothesis, natural running patterns are believed to be selected because they coincide with the minimum metabolic cost (19). However, this theory is not well supported in human running because the energy expenditure appears to be essentially similar between rearfoot and forefoot striking (41). An alternative explanation for the preference of using rearfoot striking may be the simple fact that it requires clearly lower force production from the ankle extensors than forefoot striking (24), and although this lower demand is achieved at the cost of greater knee extensor muscle force production with rearfoot striking (35), it may be a more advantageous running pattern for most runners because of larger muscular capacity reserve at the knee than at the ankle extensor level. Accordingly, a lower demand of the ankle extensors when using rearfoot striking can be a potential strategy to prevent fatigue of this muscle group. However, despite different lower limb muscle force production patterns in rearfoot and forefoot striking, the total volume of active muscle, which explains the majority of the energy expenditure of running (23), may remain essentially equal, explaining the similar energy cost of the different running patterns.
Our analysis of top speed sprinting (9.3 ± 0.4 m·s−1) showed that the ankle extensors operated at significantly greater relative effort than the knee extensors (96% vs 72%), as was the case in walking and running. This remarkable difference in relative effort may be due to very different functional roles of the ankle and knee extensors in locomotion: while both muscle groups are important contributors to vertical GRF, the ankle extensors also provide the majority of the horizontal propulsive GRF (45). Because sprinting speed has been shown to be related more to the magnitude of propulsion than vertical GRF (38), the maximum effort from the ankle rather than from knee extensors may, therefore, be required to achieve top speed. Accordingly, these results may provide a rationale for understanding age-related alterations in lower limb mechanics observed previously in running and sprinting studies, in which older adults were capable of producing similar amounts of joint moments at their knee but not at their ankle extensors during submaximal (8) and even during maximal speed running (25) when compared with the young adults.
Interestingly, the ankle extensors were able to develop virtually equal peak force during sprinting versus hopping despite clearly shorter ground contact time, suggesting that the peak force production ability of the ankle extensors was not diminished during sprinting. This is contrary to common theory that due to increasingly shorter ground contact time with greater locomotor speeds, the force production of the ankle extensors diminishes (as well as in other limb muscles) because of greater muscle fiber shortening velocity requirement (45,50,51), which, according to the well-known force–velocity relationship (17), severely compromises a maximum force a muscle can produce. Most direct evidence supporting this theory comes from a previous experimental study (50), which demonstrated that approximately 0.6 BW greater peak vertical GRF can be applied by limb muscles over a longer period of ground contact during maximal one-leg forward hopping than sprinting. Furthermore, by comparing extensor muscle forces expressed as a grand mean value over a broad range of speeds of hopping (2.5–7.5 m·s−1) versus running (2.5–10.5 m·s−1), the investigators (50) found that greater vertical GRF values in hopping were achieved by producing greater extensor muscle forces across the ankle, knee, and hip. Unfortunately, however, no comparative data of the extensor muscle forces were provided for the maximal hopping and sprinting, making comparison of the muscle forces with the present study difficult. Like previous investigators (50), we measured greater peak vertical GRF (approximately 0.5 BW) during maximal hopping than sprinting, but as can be expected from the different running speeds, our muscle force results from maximal sprinting differ from the mean values calculated over a wide range of speeds of the previous work (50), which are only roughly half of the values reported here. However, our magnitudes of the knee and ankle extensor forces agree well with other studies with comparable running and sprinting speeds (35,45,46).
We attribute the similar peak force of the ankle extensors measured in maximal sprinting versus hopping to a unique structure and function of the triceps surae MTU, which is known to greatly facilitate elastic energy storage and return during locomotion (21,29). Although no studies have yet measured in vivo muscle function in human sprinting, previous evidence from submaximal running indicates that the springlike behavior of the Achilles tendon enables muscle fibers of the ankle extensors to operate at low shortening velocities and near the plateau of the force–length relationship, up to a speed of 5 m·s−1 (27). Potentially, tendon compliance together with the history-dependent properties of the MTU, such as the stretch-induced force enhancement (16) and viscoelastic resistance to stretching (33), allows the muscle fiber contractile conditions of the ankle extensors to remain favorable at greater running speeds independent of ground contact time, which thus may enable greater force development of the ankle extensors during sprinting than would otherwise be possible.
Although we determined operating efforts of the knee and ankle extensors across different modes of locomotion, our reference test did not allow us to quantify maximal capacity and thus operating efforts of the hip extensors, which also play an important role in locomotion. This leaves open the question of which muscle groups ultimately constrain human locomotor performance. However, some insights into this issue may be sought from the recent modeling study (2), which examined the effects of speed on the limb muscle force production abilities during walking and running, based on the predicted muscle fiber force–length and force–velocity dynamics. Although the walking results supported the previous hypothesis (36) that increased muscle fiber shortening velocity compromises the force production ability of the ankle extensors at greater walking speeds and thus cause the walk-to-run transition, the running results revealed a dramatic decrease in the force production ability at the hip extensors rather than ankle or knee extensors when speed increased from 2 to 5 m·s−1. This phenomenon may be due to disadvantageous function of the hip extensor muscles for producing force because they do not undergo a springlike function during limb support, but rather exhibit active shortening at a substantial rate (14,44). If the same decreasing trend in the hip extensor muscle force production ability continues with greater running speeds, as can be expected because of progressive increases in step frequency and hip movement velocity (45), it is likely that, in addition to ankle extensor capacity, diminished peak force of the hip extensors may constrain sprinting speed.
Practical implications, limitations, and future directions
The muscles operating closest to their functional limits logically produce the weak link for locomotor ability and, therefore, are likely the most efficient therapeutic targets for exercise interventions aimed at improving walking or running performance (4). Consequently, evidence that both walking and running require greater effort from the ankle than knee extensor muscles suggests that exercise interventions designed to enhance locomotor ability should especially focus on improving ankle extensor capacity. This idea is further supported by the previous studies indicating that the loss of ankle extensor strength (48) and a consequent propulsive deficit during gait (4,9,25) are the main contributors to locomotor decline in older age. Future research is warranted to examine the effectiveness of ankle-targeted training interventions on the locomotor ability and movement mechanics across the broad context of human locomotion ranging from sport performance enhancement to prevention and rehabilitation of mobility impairments.
The current approach and findings constitute proof of principle for assessing relative muscle efforts in locomotion, a fundamental issue that deserves further investigation. Specifically, there is a need for future studies to strengthen our understanding of relative muscle efforts during locomotion across different subject groups, as well as to refine the measurement approach used to quantify muscular efforts. For example, given the relatively low angular velocities of both extensor muscle groups at the time of peak force across locomotor modes, it may be worth investigating whether the isometric force test, similar to the study by Hortobágyi et al. (18), can be used to provide a comparable reference force level with the dynamic hopping test. If so, such a reference test may be easier to conduct and, therefore, more suitable when examining relative muscle efforts in older adults and persons with limited functional abilities.
There are several limitations associated with this study. First, because our analysis was limited to males with excellent physical condition, caution must be made in generalizing these results to persons with typical or limited functional capacities. Based on previous studies on relative muscle efforts in older healthy adults (4,18,20) and diabetic patients (7), such persons can be expected to operate clearly closer to their maximal force production capacities during locomotion than the athletic subjects in the current study. Second, our inverse dynamics-based analysis was unable to account the effects of muscle co-contractions and two-joint muscles when calculating forces of the knee and ankle extensors. Consequently, although our magnitudes of peak knee and ankle extensor muscle forces across walking, running, and sprinting are within the range of values reported by others (10,22,45,46), we may underestimate the true muscle forces in the present study. However, because all measured activities are equally affected, it is unlikely that the differences in the operating efforts between the knee and the ankle extensors in this study are due to methodological issues. Third, although the study by Sugisaki et al. (49) suggests that the maximal two-leg hopping task enabled humans to produce the greatest muscle moments from their knee and ankle extensors compared with several other stretch-shortening types of movements, we cannot completely confirm that this movement task enabled both extensor muscle groups to reach their maximum force in our subjects. However, the peak extensor forces of the knee (13.9 BW) and ankle (9.9 BW) in our hopping test are in line with the previously reported peak forces developed by trained athletes during very demanding activities such as squatting, jumping, and sprinting (forces up to 12–13 BW for both muscle groups) (22,37), suggesting that the maximum effort was most likely required from both muscle groups. This postulation is also fairly well supported by reported in vivo values of maximal force capacity normalized to physiological muscle cross-sectional area of the knee (25–30 N·cm−2) (12,34) and ankle extensors (11–15 N·cm−2) (13,32). In the present study, normalized force estimations using magnetic resonance imaging measurements of physiological muscle cross-sectional areas of quadriceps (280 cm2) (34) and triceps surae (326 cm2) (13) muscles from similarly sized subjects yield values of 36 and 22 N·cm−2 for the knee and ankle extensors, respectively. Even though our values for both muscle groups are slightly larger than those reported earlier, we feel that they are still realistic, because the previous analyses (12,13,32,34) were confined to the untrained subjects and to isometric contractions. Possibly, the subjects in our study may have been able to reach greater normalized muscle forces because of their training background and usage of a reference force test that allowed a stretch-shortening type of muscle action. Thus, when viewed in the above light, it seems reasonable to assume that both extensor muscle groups reached their maximum capacity limits in our reference hopping test.
The final limitation is that we did not match the joint angles and angular velocities between locomotor tasks and the reference force test. Therefore, although our reference force test allowed natural springlike limb behavior, the muscle contractile conditions at the time of peak muscle force may have differed between the conditions, which thus may influence the maximal muscle force production capacity. This can lead to underestimation of relative efforts particularly during walking, where elastic limb behavior and its advantage on the muscle force production are less pronounced compared with the springlike hopping reference test. Also, angles and angular velocities at the time of FKmax and FAmax during walking differed the most from hopping. However, running, sprinting, and hopping all demonstrated springlike limb behavior with very similar joint angular velocities at the time of FKmax and FAmax, suggesting an isometric type of muscle contraction at the peak force production. Furthermore, although knee flexion and ankle plantarflexion angles at the time of FKmax and FAmax were greater during hopping than running and sprinting (12°–13° and 2°–4°, respectively), such differences appear to have very limited effects on the peak muscle moment production capability (3,18). In addition, an analysis of relative effort using joint angular velocity matched reference force values for each locomotion mode demonstrates essentially similar operating force levels compared with the normalization using the peak muscle forces from hopping (Table 1). This provides us with confidence that our approach is a reliable tool for assessing the relative efforts of the knee and ankle extensors and that our overall conclusions drawn from the data are not significantly influenced by the issues that limit the accuracy with what we can estimate the operating muscle efforts in this study.
This study provides the most comprehensive description available to date of operating efforts of the knee and ankle extensor muscles during walking, running, and sprinting. The results demonstrate that, regardless of the mode of locomotion, the ankle extensors operate much closer to their capacity limits compared with the knee extensors. This functional feature likely poses a primary biomechanical constraint on the human locomotor ability and, thus, may also influence the way how we locomote and adapt to accommodate compromised neuromuscular system function. These findings have relevance in the broad context of human locomotion from sport performance enhancement to prevention and rehabilitation of locomotor impairments.
This study was financially supported by the Finnish Ministry of Education and Culture, Finnish Academy (grants 250683 and 138574), and the Finnish Cultural Foundation. The funding sources did not have any involvement with the progress of study.
The authors declare no conflict of interest regarding this manuscript.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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Keywords:© 2016 American College of Sports Medicine
WALKING; RUNNING; SPRINTING; RELATIVE EFFORT; MUSCLE FORCE; LOCOMOTOR PERFORMANCE