Ultrasound imaging links soleus muscle neuromechanics and energetics during human walking with elastic ankle exoskeletons

Unpowered exoskeletons with springs in parallel to human plantar flexor muscle-tendons can reduce the metabolic cost of walking. We used ultrasound imaging to look ‘under the skin’ and measure how exoskeleton stiffness alters soleus muscle contractile dynamics and shapes the user’s metabolic rate during walking. Eleven participants (4F, 7M; age: 27.7 ± 3.3 years) walked on a treadmill at 1.25 m s −1 and 0% grade with elastic ankle exoskeletons (rotational stiffness: 0–250 Nm rad −1 ) in one training and two testing days. Metabolic savings were maximized (4.2%) at a stiffness of 50 Nm rad −1 . As exoskeleton stiffness increased, the soleus muscle operated at longer lengths and improved economy (force/activation) during early stance, but this benefit was offset by faster shortening velocity and poorer economy in late stance. Changes in soleus activation rate correlated with changes in users’ metabolic rate ( p  = 0.038, R 2  = 0.44), highlighting a crucial link between muscle neuromechanics and exoskeleton performance; perhaps informing future ‘muscle-in-the loop’ exoskeleton controllers designed to steer contractile dynamics toward more economical force production.

[1]  T. Finni,et al.  Age-related differences in Achilles tendon properties and triceps surae muscle architecture in vivo. , 2012, Journal of applied physiology.

[2]  R. Enoka Neuromechanics of Human Movement , 2001 .

[3]  D. Thelen,et al.  The effects of Achilles tendon compliance on triceps surae mechanics and energetics in walking. , 2017, Journal of biomechanics.

[4]  T. Cr Relating mechanics and energetics during exercise. , 1994 .

[5]  Natalie C Holt,et al.  What drives activation-dependent shifts in the force–length curve? , 2014, Biology Letters.

[6]  Dominic J Farris,et al.  More is not always better: modeling the effects of elastic exoskeleton compliance on underlying ankle muscle–tendon dynamics , 2014, Bioinspiration & biomimetics.

[7]  Neil J Cronin,et al.  Automatic tracking of medial gastrocnemius fascicle length during human locomotion. , 2011, Journal of applied physiology.

[8]  Philip E. Martin,et al.  A Model of Human Muscle Energy Expenditure , 2003, Computer methods in biomechanics and biomedical engineering.

[9]  Rachel W Jackson,et al.  Muscle–tendon mechanics explain unexpected effects of exoskeleton assistance on metabolic rate during walking , 2017, Journal of Experimental Biology.

[10]  C. R. Taylor,et al.  Relating mechanics and energetics during exercise. , 1994, Advances in veterinary science and comparative medicine.

[11]  H. Pontzer A unified theory for the energy cost of legged locomotion , 2016, Biology Letters.

[12]  J. Houk,et al.  Reflex Compensation for Variations in the Mechanical Properties of a Muscle , 1973, Science.

[13]  D. Farris,et al.  Linking the mechanics and energetics of hopping with elastic ankle exoskeletons. , 2012, Journal of applied physiology.

[14]  Gregory S. Sawicki,et al.  A Simple Model to Estimate Plantarflexor Muscle–Tendon Mechanics and Energetics During Walking With Elastic Ankle Exoskeletons , 2016, IEEE Transactions on Biomedical Engineering.

[15]  Conor J. Walsh,et al.  Assistance magnitude versus metabolic cost reductions for a tethered multiarticular soft exosuit , 2017, Science Robotics.

[16]  K. Kamibayashi Motor Control and Learning: A Behavioral Emphasis, 6th Edition , 2019, Medicine & Science in Sports & Exercise.

[17]  Daniel P. Ferris,et al.  Mechanics and energetics of level walking with powered ankle exoskeletons , 2008, Journal of Experimental Biology.

[18]  Daniel P. Ferris,et al.  Learning to walk with a robotic ankle exoskeleton. , 2007, Journal of biomechanics.

[19]  C. Maganaris,et al.  Adaptive response of human tendon to paralysis , 2006, Muscle & nerve.

[20]  W. O. Fenn,et al.  Muscular force at different speeds of shortening , 1935, The Journal of physiology.

[21]  R. Kram,et al.  Metabolic cost of generating muscular force in human walking: insights from load-carrying and speed experiments. , 2003, Journal of applied physiology.

[22]  Shriya S Srinivasan,et al.  Closed-loop functional optogenetic stimulation , 2018, Nature Communications.

[23]  R. Kram,et al.  Energetics of bipedal running. I. Metabolic cost of generating force. , 1998, The Journal of experimental biology.

[24]  G. Sawicki,et al.  Impact of elastic ankle exoskeleton stiffness on neuromechanics and energetics of human walking across multiple speeds , 2020, Journal of NeuroEngineering and Rehabilitation.

[25]  A V Hill,et al.  Length of muscle, and the heat and tension developed in an isometric contraction , 1925, The Journal of physiology.

[26]  Dominic James Farris,et al.  UltraTrack: Software for semi-automated tracking of muscle fascicles in sequences of B-mode ultrasound images , 2016, Comput. Methods Programs Biomed..

[27]  D. De Clercq,et al.  Exoskeleton plantarflexion assistance for elderly. , 2017, Gait & posture.

[28]  C. R. Taylor,et al.  Energetics of bipedal running. II. Limb design and running mechanics. , 1998, The Journal of experimental biology.

[29]  D. Morgan New insights into the behavior of muscle during active lengthening. , 1990, Biophysical journal.

[30]  E. Azizi,et al.  The effect of activation level on muscle function during locomotion: are optimal lengths and velocities always used? , 2016, Proceedings of the Royal Society B: Biological Sciences.

[31]  M. Mon-Williams,et al.  Motor Control and Learning , 2006 .

[32]  Rachel W Jackson,et al.  Human-in-the-loop optimization of exoskeleton assistance during walking , 2017, Science.

[33]  J. Brockway Derivation of formulae used to calculate energy expenditure in man. , 1987, Human nutrition. Clinical nutrition.

[34]  S. Verschueren,et al.  Altered Achilles tendon function during walking in people with diabetic neuropathy: implications for metabolic energy saving. , 2018, Journal of applied physiology.

[35]  D. De Clercq,et al.  Bi-articular Knee-Ankle-Foot Exoskeleton Produces Higher Metabolic Cost Reduction than Weight-Matched Mono-articular Exoskeleton , 2018, Front. Neurosci..

[36]  D. C. Lin,et al.  Experimental determination of sarcomere force-length relationship in type-I human skeletal muscle fibers. , 2009, Journal of biomechanics.

[37]  Scott Kuindersma,et al.  Human-in-the-loop Bayesian optimization of wearable device parameters , 2017, PloS one.

[38]  J C Houk,et al.  Regulation of stiffness by skeletomotor reflexes. , 1979, Annual review of physiology.

[39]  C. Maganaris,et al.  Changes in Achilles tendon moment arm from rest to maximum isometric plantarflexion: in vivo observations in man , 1998, The Journal of physiology.

[40]  D. De Clercq,et al.  Adaptation to walking with an exoskeleton that assists ankle extension. , 2013, Gait & posture.

[41]  Emanuel Azizi,et al.  Flexible mechanisms: the diverse roles of biological springs in vertebrate movement , 2011, Journal of Experimental Biology.

[42]  Jonas Rubenson,et al.  A Soft-Exosuit Enables Multi-Scale Analysis of Wearable Robotics in a Bipedal Animal Model , 2018, 2018 IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS).

[43]  C. Walsh,et al.  A soft robotic exosuit improves walking in patients after stroke , 2017, Science Translational Medicine.

[44]  Hugh M. Herr,et al.  Biomechanical walking mechanisms underlying the metabolic reduction caused by an autonomous exoskeleton , 2016, Journal of NeuroEngineering and Rehabilitation.

[45]  D. Farris,et al.  Human medial gastrocnemius force–velocity behavior shifts with locomotion speed and gait , 2012, Proceedings of the National Academy of Sciences.

[46]  B. R. Umberger,et al.  Understanding Muscle Energetics in Locomotion: New Modeling and Experimental Approaches , 2011, Exercise and sport sciences reviews.

[47]  A A Biewener,et al.  Muscle and Tendon Contributions to Force, Work, and Elastic Energy Savings: A Comparative Perspective , 2000, Exercise and sport sciences reviews.

[48]  Ian Loram,et al.  The Application of Deep Convolutional Neural Networks to Ultrasound for Modelling of Dynamic States within Human Skeletal Muscle , 2017, bioRxiv.

[49]  A. Hill The heat of shortening and the dynamic constants of muscle , 1938 .

[50]  D. De Clercq,et al.  A Simple Exoskeleton That Assists Plantarflexion Can Reduce the Metabolic Cost of Human Walking , 2013, PloS one.

[51]  M. Hull,et al.  A method for determining lower extremity muscle-tendon lengths during flexion/extension movements. , 1990, Journal of biomechanics.

[52]  Ignacio Galiana,et al.  Reducing the metabolic rate of walking and running with a versatile, portable exosuit , 2019, Science.

[53]  Dario Farina,et al.  Robust Real-Time Musculoskeletal Modeling Driven by Electromyograms , 2018, IEEE Transactions on Biomedical Engineering.

[54]  Rodger Kram,et al.  Energetics of running: a new perspective , 1990, Nature.

[55]  Yin-Biao Sun,et al.  Effects of sarcomere length and temperature on the rate of ATP utilisation by rabbit psoas muscle fibres , 2001, The Journal of physiology.

[56]  Jusuk Lee,et al.  Autonomous hip exoskeleton saves metabolic cost of walking uphill , 2017, 2017 International Conference on Rehabilitation Robotics (ICORR).

[57]  Scott L. Delp,et al.  A Model of the Lower Limb for Analysis of Human Movement , 2010, Annals of Biomedical Engineering.

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

[59]  Soha Pouya,et al.  Simulating Ideal Assistive Devices to Reduce the Metabolic Cost of Running , 2016, PloS one.

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

[61]  R L Lieber,et al.  Muscle damage is not a function of muscle force but active muscle strain. , 1993, Journal of applied physiology.

[62]  Hugh M Herr,et al.  Autonomous exoskeleton reduces metabolic cost of human walking during load carriage , 2014, Journal of NeuroEngineering and Rehabilitation.

[63]  Katherine M Steele,et al.  Impact of ankle foot orthosis stiffness on Achilles tendon and gastrocnemius function during unimpaired gait. , 2017, Journal of biomechanics.

[64]  R. Kram,et al.  Muscular Force or Work: What Determines the Metabolic Energy Cost of Running? , 2000, Exercise and sport sciences reviews.

[65]  Constantinos N. Maganaris,et al.  Imaging-based estimates of moment arm length in intact human muscle-tendons , 2004, European Journal of Applied Physiology.

[66]  Massimo Sartori,et al.  In Vivo Neuromechanics: Decoding Causal Motor Neuron Behavior with Resulting Musculoskeletal Function , 2017, Scientific Reports.

[67]  G. Zahalak,et al.  A distribution-moment model of energetics in skeletal muscle. , 1991, Journal of biomechanics.

[68]  Gregory S. Sawicki,et al.  Reducing the energy cost of human walking using an unpowered exoskeleton , 2015, Nature.

[69]  Daniel P Ferris,et al.  Invariant ankle moment patterns when walking with and without a robotic ankle exoskeleton. , 2010, Journal of biomechanics.

[70]  S. Delp,et al.  Musculoskeletal modelling deconstructs the paradoxical effects of elastic ankle exoskeletons on plantar-flexor mechanics and energetics during hopping , 2014, Journal of Experimental Biology.

[71]  R. Alexander Optimum Muscle Design for Oscillatory Movements. , 1997, Journal of theoretical biology.

[72]  Scott L Delp,et al.  Simulating ideal assistive devices to reduce the metabolic cost of walking with heavy loads , 2017, PloS one.

[73]  Daniel P. Ferris,et al.  Learning to walk with an adaptive gain proportional myoelectric controller for a robotic ankle exoskeleton , 2015, Journal of NeuroEngineering and Rehabilitation.

[74]  M. Pandy,et al.  In vivo behavior of the human soleus muscle with increasing walking and running speeds. , 2015, Journal of applied physiology.

[75]  Daniel P Ferris,et al.  Mechanics and energetics of incline walking with robotic ankle exoskeletons , 2009, Journal of Experimental Biology.

[76]  Youngbo Shim,et al.  A Wearable Hip Assist Robot Can Improve Gait Function and Cardiopulmonary Metabolic Efficiency in Elderly Adults , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[77]  Christoph Anders,et al.  The musculoskeletal system of humans is not tuned to maximize the economy of locomotion , 2011, Proceedings of the National Academy of Sciences.

[78]  Rachel W Jackson,et al.  An experimental comparison of the relative benefits of work and torque assistance in ankle exoskeletons. , 2015, Journal of applied physiology.

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

[80]  Gregory S Sawicki,et al.  A benchtop biorobotic platform for in vitro observation of muscle-tendon dynamics with parallel mechanical assistance from an elastic exoskeleton. , 2017, Journal of biomechanics.

[81]  Richard R Neptune,et al.  The effect of walking speed on muscle function and mechanical energetics. , 2008, Gait & posture.

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

[83]  J. Houk,et al.  Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. , 1976, Journal of neurophysiology.

[84]  Thomas A. McMahon,et al.  Muscles, Reflexes, and Locomotion , 1984 .

[85]  Alena M. Grabowski,et al.  What determines the metabolic cost of human running across a wide range of velocities? , 2018, Journal of Experimental Biology.

[86]  Richard W Nuckols,et al.  Exoskeletons Improve Locomotion Economy by Reducing Active Muscle Volume , 2019, Exercise and sport sciences reviews.

[87]  J. Maxwell Donelan,et al.  "Body-In-The-Loop": Optimizing Device Parameters Using Measures of Instantaneous Energetic Cost , 2015, PloS one.

[88]  P. Komi,et al.  Muscle-tendon interaction and elastic energy usage in human walking. , 2005, Journal of applied physiology.

[89]  T. Finni,et al.  Slower Walking Speed in Older Men Improves Triceps Surae Force Generation Ability , 2017, Medicine and science in sports and exercise.

[90]  Dirk De Clercq,et al.  Reducing the metabolic cost of walking with an ankle exoskeleton: interaction between actuation timing and power , 2017, Journal of NeuroEngineering and Rehabilitation.

[91]  Jusuk Lee,et al.  Fully autonomous hip exoskeleton saves metabolic cost of walking , 2016, 2016 IEEE International Conference on Robotics and Automation (ICRA).

[92]  Kota Z. Takahashi,et al.  Adding Stiffness to the Foot Modulates Soleus Force-Velocity Behaviour during Human Walking , 2016, Scientific Reports.

[93]  Li-Qun Zhang,et al.  Ultrasonic evaluations of Achilles tendon mechanical properties poststroke. , 2009, Journal of applied physiology.

[94]  T. Fukunaga,et al.  In vivo behaviour of human muscle tendon during walking , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[95]  Benjamin D. Robertson,et al.  Elastic ankle exoskeletons reduce soleus muscle force but not work in human hopping. , 2013, Journal of applied physiology.

[96]  D. Morgan,et al.  Early events in stretch-induced muscle damage. , 1999, Journal of applied physiology.

[97]  V. Edgerton,et al.  Physiological cross‐sectional area of human leg muscles based on magnetic resonance imaging , 1992, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[98]  W Herzog,et al.  Stability of muscle fibers on the descending limb of the force-length relation. A theoretical consideration. , 1996, Journal of biomechanics.

[99]  H. Pontzer A new model predicting locomotor cost from limb length via force production , 2005, Journal of Experimental Biology.

[100]  Andy Ruina,et al.  Energetic Consequences of Walking Like an Inverted Pendulum: Step-to-Step Transitions , 2005, Exercise and sport sciences reviews.

[101]  Hugh M Herr,et al.  Autonomous exoskeleton reduces metabolic cost of human walking , 2014, Journal of NeuroEngineering and Rehabilitation.

[102]  Karl E Zelik,et al.  Six degree-of-freedom analysis of hip, knee, ankle and foot provides updated understanding of biomechanical work during human walking , 2015, The Journal of Experimental Biology.

[103]  Dominic James Farris,et al.  Erratum: More is not always better: modeling the effects of elastic exoskeleton compliance on underlying ankle muscle–tendon dynamics (2014 Bioinspir. Biomim. 9 046018) , 2015 .

[104]  Jarred G Gillett,et al.  Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound , 2013, Computer methods in biomechanics and biomedical engineering.

[105]  J. Rubenson,et al.  On the ascent: the soleus operating length is conserved to the ascending limb of the force–length curve across gait mechanics in humans , 2012, Journal of Experimental Biology.