Muscular strategy shift in human running: dependence of running speed on hip and ankle muscle performance

SUMMARY Humans run faster by increasing a combination of stride length and stride frequency. In slow and medium-paced running, stride length is increased by exerting larger support forces during ground contact, whereas in fast running and sprinting, stride frequency is increased by swinging the legs more rapidly through the air. Many studies have investigated the mechanics of human running, yet little is known about how the individual leg muscles accelerate the joints and centre of mass during this task. The aim of this study was to describe and explain the synergistic actions of the individual leg muscles over a wide range of running speeds, from slow running to maximal sprinting. Experimental gait data from nine subjects were combined with a detailed computer model of the musculoskeletal system to determine the forces developed by the leg muscles at different running speeds. For speeds up to 7 m s–1, the ankle plantarflexors, soleus and gastrocnemius, contributed most significantly to vertical support forces and hence increases in stride length. At speeds greater than 7 m s–1, these muscles shortened at relatively high velocities and had less time to generate the forces needed for support. Thus, above 7 m s–1, the strategy used to increase running speed shifted to the goal of increasing stride frequency. The hip muscles, primarily the iliopsoas, gluteus maximus and hamstrings, achieved this goal by accelerating the hip and knee joints more vigorously during swing. These findings provide insight into the strategies used by the leg muscles to maximise running performance and have implications for the design of athletic training programs.

[1]  T Fukunaga,et al.  In vivo dynamics of human medial gastrocnemius muscle-tendon complex during stretch-shortening cycle exercise. , 2000, Acta physiologica Scandinavica.

[2]  V. Edgerton,et al.  Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. , 1984, Journal of applied physiology: respiratory, environmental and exercise physiology.

[3]  H Kunz,et al.  Biomechanical analysis of sprinting: decathletes versus champions. , 1981, British journal of sports medicine.

[4]  Marcus G Pandy,et al.  Muscle coordination of mediolateral balance in normal walking. , 2010, Journal of biomechanics.

[5]  Andrew A Biewener,et al.  Muscle mechanical advantage of human walking and running: implications for energy cost. , 2004, Journal of applied physiology.

[6]  T Abe,et al.  Fascicle length of leg muscles is greater in sprinters than distance runners. , 2000, Medicine and science in sports and exercise.

[7]  P. Komi,et al.  Moment and power of lower limb joints in running. , 2002, International journal of sports medicine.

[8]  R. C. Nelson,et al.  Biomechanics of overground versus treadmill running. , 1972, Medicine and science in sports.

[9]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[10]  Anthony G Schache,et al.  Non-invasive assessment of soft-tissue artifact and its effect on knee joint kinematics during functional activity. , 2010, Journal of biomechanics.

[11]  D. Kerwin,et al.  Elite sprinting: are athletes individually step-frequency or step-length reliant? , 2011, Medicine & Science in Sports & Exercise.

[12]  Alan M. Wilson,et al.  The anatomical arrangement of muscle and tendon enhances limb versatility and locomotor performance , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  B C Elliott,et al.  A cinematographic analysis of overground and treadmill running by males and females. , 1976, Medicine and science in sports.

[14]  N I Volkov,et al.  Analysis of the velocity curve in sprint running. , 1979, Medicine and science in sports.

[15]  Alan M. Wilson,et al.  Is Achilles tendon compliance optimised for maximum muscle efficiency during locomotion? , 2007, Journal of biomechanics.

[16]  B. Freriks,et al.  Development of recommendations for SEMG sensors and sensor placement procedures. , 2000, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[17]  G. Caldwell,et al.  Energy absorption of impacts during running at various stride lengths. , 1998, Medicine and science in sports and exercise.

[18]  Jonas Rubenson,et al.  Adaptations for economical bipedal running: the effect of limb structure on three-dimensional joint mechanics , 2011, Journal of The Royal Society Interface.

[19]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[20]  Giovanni A. Cavagna,et al.  The two asymmetries of the bouncing step , 2009, European Journal of Applied Physiology.

[21]  S. Piazza,et al.  Built for speed: musculoskeletal structure and sprinting ability , 2009, Journal of Experimental Biology.

[22]  G. Caldwell,et al.  Limitations to maximum sprinting speed imposed by muscle mechanical properties. , 2012, Journal of biomechanics.

[23]  M G Pandy,et al.  Computer modeling and simulation of human movement. , 2001, Annual review of biomedical engineering.

[24]  M. Pandy,et al.  Dynamic optimization of human walking. , 2001, Journal of biomechanical engineering.

[25]  Walter Herzog,et al.  Model-based estimation of muscle forces exerted during movements. , 2007, Clinical biomechanics.

[26]  A Leardini,et al.  Position and orientation in space of bones during movement: experimental artefacts. , 1996, Clinical biomechanics.

[27]  P V Komi,et al.  Physiological and Biomechanical Correlates of Muscle Function: Effects of Muscle Structure and Stretch—Shortening Cycle on Force and Speed , 1984, Exercise and sport sciences reviews.

[28]  B. Katz The relation between force and speed in muscular contraction , 1939, The Journal of physiology.

[29]  J. Hamill,et al.  Relationship between shock attenuation and stride length during running at different velocities , 2002, European Journal of Applied Physiology.

[30]  G. Cavagna,et al.  The determinants of the step frequency in running, trotting and hopping in man and other vertebrates. , 1988, The Journal of physiology.

[31]  D. Thelen Adjustment of muscle mechanics model parameters to simulate dynamic contractions in older adults. , 2003, Journal of biomechanical engineering.

[32]  G. Cavagna,et al.  The mechanics of sprint running , 1971, The Journal of physiology.

[33]  P V Komi,et al.  The role of the stretch reflex in the gastrocnemius muscle during human locomotion at various speeds. , 2007, Journal of applied physiology.

[34]  R. Close Dynamic properties of mammalian skeletal muscles. , 1972, Physiological reviews.

[35]  A E Chapman,et al.  Kinetic limitations of maximal sprinting speed. , 1983, Journal of biomechanics.

[36]  E. Frederick,et al.  Factors Affecting Peak Vertical Ground Reaction Forces in Running , 1986 .

[37]  LIAM HENNESSY,et al.  Relationship of the Stretch‐Shortening Cycle to Sprint Performance in Trained Female Athletes , 2001, Journal of strength and conditioning research.

[38]  R. R. Neptune,et al.  Muscle Activation and Deactivation Dynamics: The Governing Properties in Fast Cyclical Human Movement Performance? , 2001, Exercise and sport sciences reviews.

[39]  T. Hortobágyi,et al.  Teager–Kaiser energy operator signal conditioning improves EMG onset detection , 2010, European Journal of Applied Physiology.

[40]  Thomas J Roberts,et al.  Mechanical power output during running accelerations in wild turkeys. , 2002, The Journal of experimental biology.

[41]  Richard R Neptune,et al.  Differences in muscle function during walking and running at the same speed. , 2006, Journal of biomechanics.

[42]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.

[43]  M Kaneko,et al.  Mechanics and energetics in running with special reference to efficiency. , 1990, Journal of biomechanics.

[44]  Daniel P Ferris,et al.  It Pays to Have a Spring in Your Step , 2009, Exercise and sport sciences reviews.

[45]  J. Mercer,et al.  Kinetic consequences of constraining running behavior. , 2005, Journal of sports science & medicine.

[46]  Sofia Heintz,et al.  Static optimization of muscle forces during gait in comparison to EMG-to-force processing approach. , 2007, Gait & posture.

[47]  Marcus G Pandy,et al.  Muscle and joint function in human locomotion. , 2010, Annual review of biomedical engineering.

[48]  G. Cavagna,et al.  Old men running: mechanical work and elastic bounce , 2008, Proceedings of the Royal Society B: Biological Sciences.

[49]  Volkov Ni,et al.  Analysis of the velocity curve in sprint running. , 1979 .

[50]  L C Rome,et al.  Maximum velocity of shortening of three fibre types from horse soleus muscle: implications for scaling with body size. , 1990, The Journal of physiology.

[51]  P. Weyand,et al.  Faster top running speeds are achieved with greater ground forces not more rapid leg movements. , 2000, Journal of applied physiology.

[52]  B. Nigg,et al.  A kinematic comparison of overground and treadmill running. , 1995, Medicine and science in sports and exercise.

[53]  B. C. Abbott,et al.  The relation between velocity of shortening and the tension‐length curve of skeletal muscle , 1953, The Journal of physiology.

[54]  Marcus G Pandy,et al.  A neuromusculoskeletal tracking method for estimating individual muscle forces in human movement. , 2007, Journal of biomechanics.

[55]  Elliott Bc,et al.  A cinematographic analysis of overground and treadmill running by males and females. , 1976 .

[56]  W. Kibler,et al.  Functional biomechanical deficits in running athletes with plantar fasciitis , 1991, The American journal of sports medicine.

[57]  Ajay Seth,et al.  Muscle contributions to propulsion and support during running. , 2010, Journal of biomechanics.

[58]  Marcus G. Pandy,et al.  A computationally efficient method for assessing muscle function during human locomotion , 2011 .

[59]  J J O'Connor,et al.  Bone position estimation from skin marker co-ordinates using global optimisation with joint constraints. , 1999, Journal of biomechanics.

[60]  Tim W. Dorn,et al.  Estimates of muscle function in human gait depend on how foot-ground contact is modelled , 2012, Computer methods in biomechanics and biomedical engineering.

[61]  Tim W Dorn,et al.  Effect of running speed on lower limb joint kinetics. , 2011, Medicine and science in sports and exercise.

[62]  D. Kerrigan,et al.  A kinematics and kinetic comparison of overground and treadmill running. , 2008, Medicine and science in sports and exercise.

[63]  R. Marshall,et al.  Interaction of step length and step rate during sprint running. , 2004, Medicine and science in sports and exercise.

[64]  W Baumann,et al.  The three-dimensional determination of internal loads in the lower extremity. , 1997, Journal of biomechanics.

[65]  T. Hortobágyi,et al.  Muscles do more positive than negative work in human locomotion , 2007, Journal of Experimental Biology.

[66]  M. Pandy,et al.  Individual muscle contributions to support in normal walking. , 2003, Gait & posture.

[67]  B. Prilutsky,et al.  Sensitivity of predicted muscle forces to parameters of the optimization-based human leg model revealed by analytical and numerical analyses. , 2001, Journal of biomechanics.

[68]  G. Lichtwark,et al.  The influence of tendon compliance on muscle power output and efficiency during cyclic contractions , 2010, Journal of Experimental Biology.

[69]  Timothy R. Konold,et al.  Sagittal plane knee joint moments following anterior cruciate ligament injury and reconstruction: a systematic review. , 2010, Clinical biomechanics.

[70]  Tim W Dorn,et al.  Comparison of different methods for estimating muscle forces in human movement , 2012, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[71]  A. Bahler,et al.  The Dynamic Properties of Mammalian Skeletal Muscle , 1968, The Journal of general physiology.

[72]  F. Zajac Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. , 1989, Critical reviews in biomedical engineering.

[73]  Novacheck,et al.  The biomechanics of running. , 1998, Gait & posture.

[74]  B. Frishberg,et al.  An analysis of overground and treadmill sprinting. , 1983, Medicine and science in sports and exercise.

[75]  T Abe,et al.  Sprint performance is related to muscle fascicle length in male 100-m sprinters. , 1999, Journal of applied physiology.

[76]  R. Crowninshield,et al.  A physiologically based criterion of muscle force prediction in locomotion. , 1981, Journal of biomechanics.

[77]  G. Caldwell,et al.  An integrated biomechanical analysis of high speed incline and level treadmill running. , 2000, Medicine and science in sports and exercise.

[78]  R V Mann,et al.  A kinetic analysis of sprinting. , 1981, Medicine and science in sports and exercise.

[79]  Thomas M Best,et al.  Simulation of biceps femoris musculotendon mechanics during the swing phase of sprinting. , 2005, Medicine and science in sports and exercise.

[80]  D. Thelen,et al.  Hamstring musculotendon dynamics during stance and swing phases of high-speed running. , 2011, Medicine and science in sports and exercise.

[81]  G. Lichtwark,et al.  Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. , 2007, Journal of biomechanics.

[82]  P Webb,et al.  The work of walking: a calorimetric study. , 1988, Medicine and science in sports and exercise.

[83]  Justin W. Fernandez,et al.  Evaluation of predicted knee‐joint muscle forces during gait using an instrumented knee implant , 2008, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[84]  Laura H. Smallwood,et al.  Are Current Measurements of Lower Extremity Muscle Architecture Accurate? , 2009, Clinical orthopaedics and related research.

[85]  Ajay Seth,et al.  Minimal formulation of joint motion for biomechanisms , 2010, Nonlinear dynamics.

[86]  Ping Zhou,et al.  Teager–Kaiser Energy Operation of Surface EMG Improves Muscle Activity Onset Detection , 2007, Annals of Biomedical Engineering.

[87]  T. Roberts The integrated function of muscles and tendons during locomotion. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[88]  Benjamin J. Fregly,et al.  Evaluation of Predicted Knee Joint Muscle Forces During Gait Using an Instrumented Knee Implant , 2008 .

[89]  A. McIntosh,et al.  Gait dynamics on an inclined walkway. , 2006, Journal of biomechanics.

[90]  Elizabeth S Chumanov,et al.  The effect of speed and influence of individual muscles on hamstring mechanics during the swing phase of sprinting. , 2007, Journal of biomechanics.

[91]  R. Marshall,et al.  Relationships between ground reaction force impulse and kinematics of sprint-running acceleration. , 2005, Journal of applied biomechanics.

[92]  May Q. Liu,et al.  Muscle contributions to support and progression over a range of walking speeds. , 2008, Journal of biomechanics.

[93]  G. Cavagna,et al.  The two power limits conditioning step frequency in human running. , 1991, The Journal of physiology.

[94]  Ralph Mann,et al.  Kinematic Analysis of Olympic Sprint Performance: Men's 200 Meters , 1985 .

[95]  F. Zajac,et al.  Determining Muscle's Force and Action in Multi‐Articular Movement , 1989, Exercise and sport sciences reviews.

[96]  Timothy E Higham,et al.  How muscles define maximum running performance in lizards: an analysis using swing- and stance-phase muscles , 2011, Journal of Experimental Biology.

[97]  P. Komi Stretch-shortening cycle: a powerful model to study normal and fatigued muscle. , 2000, Journal of biomechanics.

[98]  N. Curtin,et al.  Energetic aspects of muscle contraction. , 1985, Monographs of the Physiological Society.

[99]  A J Ward-Smith,et al.  A mathematical theory of running, based on the first law of thermodynamics, and its application to the performance of world-class athletes. , 1985, Journal of biomechanics.