Why Is Neuromechanical Modeling of Balance and Locomotion So Hard

A goal and challenge in neuromechanical modeling is to develop validated simulations to predict the effects of neuromotor deficits and therapies on movements. This has been particularly challenging in balance and locomotion because they are inherently unstable, making it difficult to explore model parameters in a way that still coordinates the body in a functional way. Integrating realistic and validated musculoskeletal models with neural control mechanisms is critical to our ability to predict how human robustly move in the environment. Here we briefly review both human locomotion models, which generally focus on modeling the physical dynamics of movement with simplified models of neural control, as well as balance models, which model sensorimotor dynamics and processing with simplified biomechanical models. Combining complex neural and musculoskeletal models increases the redundancy in a model and allows us to study how motor variability and robustness are exploited to produce movements in both healthy and impaired individuals. To advance, the integration of neuromechanical modeling and experimental approaches will be critical in testing specific hypotheses concerning how and why neuromechanical flexibility is both exploited and constrained under various movement contexts. We give a few examples of how the close interplay between models and experiments can reveal neuromechanical principles of movement.

[1]  Lena H Ting,et al.  Sensorimotor feedback based on task-relevant error robustly predicts temporal recruitment and multidirectional tuning of muscle synergies. , 2013, Journal of neurophysiology.

[2]  Lena H Ting,et al.  Defining feasible bounds on muscle activation in a redundant biomechanical task: practical implications of redundancy. , 2013, Journal of biomechanics.

[3]  Nobutoshi Yamazaki,et al.  Generation of human bipedal locomotion by a bio-mimetic neuro-musculo-skeletal model , 2001, Biological Cybernetics.

[4]  Andy Ruina,et al.  A Bipedal Walking Robot with Efficient and Human-Like Gait , 2005, Proceedings of the 2005 IEEE International Conference on Robotics and Automation.

[5]  Jeffrey A. Reinbolt,et al.  Biarticular muscles influence postural responses: implications for treatment of stiff-knee gait , 2011 .

[6]  R J Full,et al.  Templates and anchors: neuromechanical hypotheses of legged locomotion on land. , 1999, The Journal of experimental biology.

[7]  Gentaro Taga,et al.  A model of the neuro-musculo-skeletal system for human locomotion , 1995, Biological Cybernetics.

[8]  G. Cavagna,et al.  Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. , 1977, The American journal of physiology.

[9]  Gerald E. Loeb,et al.  Optimal isn’t good enough , 2012, Biological Cybernetics.

[10]  Jonathan P. Walter,et al.  Muscle synergies may improve optimization prediction of knee contact forces during walking. , 2014, Journal of biomechanical engineering.

[11]  R Nataraj,et al.  Comprehensive Joint Feedback Control for Standing by Functional Neuromuscular Stimulation—A Simulation Study , 2010, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[12]  Dario Farina,et al.  EMG-Driven Forward-Dynamic Estimation of Muscle Force and Joint Moment about Multiple Degrees of Freedom in the Human Lower Extremity , 2012, PloS one.

[13]  S. Park,et al.  Feedback equilibrium control during human standing , 2005, Biological Cybernetics.

[14]  Scott L Delp,et al.  Generating dynamic simulations of movement using computed muscle control. , 2003, Journal of biomechanics.

[15]  M. Hoy,et al.  The role of intersegmental dynamics during rapid limb oscillations. , 1986, Journal of biomechanics.

[16]  S. McLean,et al.  Development and validation of a 3-D model to predict knee joint loading during dynamic movement. , 2003, Journal of biomechanical engineering.

[17]  R R Neptune,et al.  Relationships between muscle contributions to walking subtasks and functional walking status in persons with post-stroke hemiparesis. , 2011, Clinical biomechanics.

[18]  Michael Damsgaard,et al.  Analysis of musculoskeletal systems in the AnyBody Modeling System , 2006, Simul. Model. Pract. Theory.

[19]  P. Morasso,et al.  Can muscle stiffness alone stabilize upright standing? , 1999, Journal of neurophysiology.

[20]  L. Ting,et al.  Automatic Postural Responses Are Delayed by Pyridoxine-Induced Somatosensory Loss , 2002, The Journal of Neuroscience.

[21]  Alfred D. Grant Gait Analysis: Normal and Pathological Function , 2010 .

[22]  F. Zajac,et al.  Muscle contributions to support during gait in an individual with post-stroke hemiparesis. , 2006, Journal of biomechanics.

[23]  Katherine M Steele,et al.  How much muscle strength is required to walk in a crouch gait? , 2012, Journal of biomechanics.

[24]  Seyed A Safavynia,et al.  Long-latency muscle activity reflects continuous, delayed sensorimotor feedback of task-level and not joint-level error. , 2013, Journal of neurophysiology.

[25]  Shree Pandya Gait Disorders in Childhood and Adolescence , 1985 .

[26]  Stacie A. Chvatal,et al.  Common muscle synergies for balance and walking , 2013, Front. Comput. Neurosci..

[27]  Stacie A. Chvatal,et al.  Voluntary and Reactive Recruitment of Locomotor Muscle Synergies during Perturbed Walking , 2012, The Journal of Neuroscience.

[28]  Tad McGeer,et al.  Passive Dynamic Walking , 1990, Int. J. Robotics Res..

[29]  Marko Ackermann,et al.  Optimality principles for model-based prediction of human gait. , 2010, Journal of biomechanics.

[30]  D. Lloyd,et al.  An EMG-driven musculoskeletal model to estimate muscle forces and knee joint moments in vivo. , 2003, Journal of biomechanics.

[31]  B. Prilutsky,et al.  A Neuromechanical Model of Spinal Control of Locomotion , 2016 .

[32]  Torrence D. J. Welch,et al.  A feedback model reproduces muscle activity during human postural responses to support-surface translations. , 2008, Journal of neurophysiology.

[33]  F. Horak,et al.  Effect of stance width on multidirectional postural responses. , 2001, Journal of neurophysiology.

[34]  Andrea d'Avella,et al.  Differences in Adaptation Rates after Virtual Surgeries Provide Direct Evidence for Modularity , 2013, The Journal of Neuroscience.

[35]  Michael I. Jordan,et al.  A Minimal Intervention Principle for Coordinated Movement , 2002, NIPS.

[36]  D. Sternad,et al.  Decomposition of variability in the execution of goal-oriented tasks: three components of skill improvement. , 2004, Journal of experimental psychology. Human perception and performance.

[37]  Ying Zhu,et al.  AnimatLab: A 3D graphics environment for neuromechanical simulations , 2010, Journal of Neuroscience Methods.

[38]  Lena H. Ting,et al.  Stability Radius as a Method for Comparing the Dynamics of Neuromechanical Systems , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[39]  D. Winter,et al.  Stiffness control of balance in quiet standing. , 1998, Journal of neurophysiology.

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

[41]  Lena H Ting,et al.  Neuromechanic: a computational platform for simulation and analysis of the neural control of movement. , 2012, International journal for numerical methods in biomedical engineering.

[42]  Manoj Srinivasan,et al.  Computer optimization of a minimal biped model discovers walking and running , 2006, Nature.

[43]  Russ Tedrake,et al.  Efficient Bipedal Robots Based on Passive-Dynamic Walkers , 2005, Science.

[44]  F. Zajac,et al.  Locomotor strategy for pedaling: muscle groups and biomechanical functions. , 1999, Journal of neurophysiology.

[45]  D. B. Lockhart,et al.  Optimal sensorimotor transformations for balance , 2007, Nature Neuroscience.

[46]  F. Horak,et al.  Influence of stimulus parameters on human postural responses. , 1988, Journal of neurophysiology.

[47]  Shinya Aoi,et al.  Evaluating functional roles of phase resetting in generation of adaptive human bipedal walking with a physiologically based model of the spinal pattern generator , 2010, Biological Cybernetics.

[48]  R. Stein,et al.  The relation between the surface electromyogram and muscular force. , 1975, The Journal of physiology.

[49]  Jeffrey A. Reinbolt,et al.  The use of a platform for dynamic simulation of movement: application to balance recovery , 2012 .

[50]  Dario Farina,et al.  A musculoskeletal model of human locomotion driven by a low dimensional set of impulsive excitation primitives , 2013, Front. Comput. Neurosci..

[51]  A. Kuo An optimal state estimation model of sensory integration in human postural balance , 2005, Journal of neural engineering.

[52]  Katherine M Steele,et al.  Muscle contributions to vertical and fore-aft accelerations are altered in subjects with crouch gait. , 2013, Gait & posture.

[53]  Sungho Jo,et al.  A model of cerebellum stabilized and scheduled hybrid long-loop control of upright balance , 2004, Biological Cybernetics.

[54]  Shinya Aoi,et al.  Neuromusculoskeletal Modeling for the Adaptive Control of Posture During Locomotion , 2016 .

[55]  Robert J. Peterka,et al.  Model-Based Interpretations of Experimental Data Related to the Control of Balance During Stance and Gait in Humans , 2016 .

[56]  Gregor Schöner,et al.  The uncontrolled manifold concept: identifying control variables for a functional task , 1999, Experimental Brain Research.

[57]  Richard R Neptune,et al.  Muscle work is increased in pre-swing during hemiparetic walking. , 2011, Clinical biomechanics.

[58]  F. Horak,et al.  Postural feedback responses scale with biomechanical constraints in human standing , 2004, Experimental Brain Research.

[59]  David G Lloyd,et al.  Neuromusculoskeletal modeling: estimation of muscle forces and joint moments and movements from measurements of neural command. , 2004, Journal of applied biomechanics.

[60]  J. A. Pruszynski,et al.  Primate upper limb muscles exhibit activity patterns that differ from their anatomical action during a postural task. , 2006, Journal of neurophysiology.

[61]  J. Collins,et al.  Open-loop and closed-loop control of posture: A random-walk analysis of center-of-pressure trajectories , 2004, Experimental Brain Research.

[62]  Robert J. Peterka,et al.  Postural control model interpretation of stabilogram diffusion analysis , 2000, Biological Cybernetics.

[63]  Torrence D. J. Welch,et al.  A feedback model explains the differential scaling of human postural responses to perturbation acceleration and velocity. , 2009, Journal of neurophysiology.

[64]  L.H. Ting,et al.  Effects of stance width on control gain in standing balance , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[65]  R. Blickhan The spring-mass model for running and hopping. , 1989, Journal of biomechanics.

[66]  E Roth,et al.  A comparative approach to closed-loop computation , 2014, Current Opinion in Neurobiology.

[67]  Stacie A. Chvatal,et al.  Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. , 2011, Journal of neurophysiology.

[68]  Gentaro Taga,et al.  A model of the neuro-musculo-skeletal system for human locomotion , 1995, Biological Cybernetics.

[69]  Lena H Ting,et al.  A limited set of muscle synergies for force control during a postural task. , 2005, Journal of neurophysiology.

[70]  Lena H Ting,et al.  Stability in a frontal plane model of balance requires coupled changes to postural configuration and neural feedback control. , 2011, Journal of neurophysiology.

[71]  Marco Viceconti,et al.  Computational tools for calculating alternative muscle force patterns during motion: a comparison of possible solutions. , 2013, Journal of biomechanics.

[72]  Emilio Bizzi,et al.  Combinations of muscle synergies in the construction of a natural motor behavior , 2003, Nature Neuroscience.

[73]  E. Bizzi,et al.  Article history: , 2005 .

[74]  A.D. Kuo,et al.  An optimal control model for analyzing human postural balance , 1995, IEEE Transactions on Biomedical Engineering.

[75]  Richard R Neptune,et al.  Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. , 2010, Journal of neurophysiology.

[76]  Richard R Neptune,et al.  Biomechanics and muscle coordination of human walking. Part I: introduction to concepts, power transfer, dynamics and simulations. , 2002, Gait & posture.

[77]  Richard R Neptune,et al.  Modular control of human walking: a simulation study. , 2009, Journal of biomechanics.

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

[79]  T. Sinkjaer,et al.  Spastic movement disorder: impaired reflex function and altered muscle mechanics , 2007, The Lancet Neurology.

[80]  Richard R Neptune,et al.  Muscle and prosthesis contributions to amputee walking mechanics: a modeling study. , 2012, Journal of biomechanics.

[81]  Daniel Vélez Día,et al.  Biomechanics and Motor Control of Human Movement , 2013 .

[82]  Sungho Jo,et al.  A model of cerebrocerebello-spinomuscular interaction in the sagittal control of human walking , 2007, Biological Cybernetics.

[83]  V. Zatsiorsky,et al.  Instant equilibrium point and its migration in standing tasks: rambling and trembling components of the stabilogram. , 1999, Motor control.

[84]  Herman van der Kooij,et al.  A multisensory integration model of human stance control , 1999, Biological Cybernetics.

[85]  Martijn Wisse,et al.  Passive-Based Walking Robot , 2007, IEEE Robotics & Automation Magazine.

[86]  T. Brown On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system , 1914, The Journal of physiology.

[87]  F E Zajac,et al.  Human standing posture: multi-joint movement strategies based on biomechanical constraints. , 1993, Progress in brain research.

[88]  Cole S. Simpson,et al.  Feasible muscle activation ranges based on inverse dynamics analyses of human walking. , 2015, Journal of biomechanics.

[89]  Tad McGeer,et al.  Passive walking with knees , 1990, Proceedings., IEEE International Conference on Robotics and Automation.

[90]  Daniele Borzelli,et al.  Effort minimization and synergistic muscle recruitment for three-dimensional force generation , 2013, Front. Comput. Neurosci..

[91]  L. Ting,et al.  Functional muscle synergies constrain force production during postural tasks. , 2008, Journal of biomechanics.

[92]  Reinhard Blickhan,et al.  Compliant leg behaviour explains basic dynamics of walking and running , 2006, Proceedings of the Royal Society B: Biological Sciences.

[93]  G. Cavagna,et al.  MECHANICAL WORK IN RUNNING. , 1964, Journal of applied physiology.

[94]  Stacie A. Chvatal,et al.  Decomposing Muscle Activity in Motor TasksMethods and Interpretation , 2010 .

[95]  Jason J Kutch,et al.  Muscle redundancy does not imply robustness to muscle dysfunction. , 2011, Journal of biomechanics.

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

[97]  Chandana Paul,et al.  Development of a human neuro-musculo-skeletal model for investigation of spinal cord injury , 2005, Biological Cybernetics.

[98]  Stacie A. Chvatal,et al.  Review and perspective: neuromechanical considerations for predicting muscle activation patterns for movement , 2012, International journal for numerical methods in biomedical engineering.

[99]  R J Full,et al.  How animals move: an integrative view. , 2000, Science.

[100]  Richard R Neptune,et al.  Three-dimensional modular control of human walking. , 2012, Journal of biomechanics.

[101]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

[102]  Qi Shao,et al.  An EMG-driven model to estimate muscle forces and joint moments in stroke patients , 2009, Comput. Biol. Medicine.

[103]  Nathan E. Bunderson,et al.  Better Science Through Predictive Modeling: Numerical Tools for Understanding Neuromechanical Interactions , 2016 .

[104]  J J Collins,et al.  The redundant nature of locomotor optimization laws. , 1995, Journal of biomechanics.

[105]  Frans C. T. van der Helm,et al.  Comparison of different methods to identify and quantify balance control , 2005, Journal of Neuroscience Methods.

[106]  T. McMahon,et al.  The mechanics of running: how does stiffness couple with speed? , 1990, Journal of biomechanics.

[107]  Lena H Ting,et al.  Neuromechanical tuning of nonlinear postural control dynamics. , 2009, Chaos.

[108]  Richard R Neptune,et al.  The influence of merged muscle excitation modules on post-stroke hemiparetic walking performance. , 2013, Clinical biomechanics.

[109]  E. Marder,et al.  Similar network activity from disparate circuit parameters , 2004, Nature Neuroscience.

[110]  Raviraj Nataraj,et al.  Center of mass acceleration feedback control for standing by functional neuromuscular stimulation: a simulation study. , 2012, Journal of rehabilitation research and development.

[111]  F. Zajac,et al.  Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. , 2001, Journal of biomechanics.

[112]  Raviraj Nataraj,et al.  Comparing joint kinematics and center of mass acceleration as feedback for control of standing balance by functional neuromuscular stimulation , 2012, Journal of NeuroEngineering and Rehabilitation.

[113]  Lena H. Ting,et al.  Optimization of Muscle Activity for Task-Level Goals Predicts Complex Changes in Limb Forces across Biomechanical Contexts , 2012, PLoS Comput. Biol..

[114]  R. Peterka,et al.  A new interpretation of spontaneous sway measures based on a simple model of human postural control. , 2005, Journal of neurophysiology.

[115]  Torrence D. J. Welch,et al.  Statistically significant contrasts between EMG waveforms revealed using wavelet-based functional ANOVA. , 2013, Journal of neurophysiology.

[116]  T. McMahon,et al.  Ballistic walking. , 1980, Journal of biomechanics.

[117]  Peter J. Gawthrop,et al.  Predictive feedback in human simulated pendulum balancing , 2009, Biological Cybernetics.

[118]  Lena H Ting,et al.  Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. , 2010, Journal of neurophysiology.

[119]  L. Ting,et al.  Biomechanical capabilities influence postural control strategies in the cat hindlimb. , 2007, Journal of biomechanics.

[120]  R. Peterka Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[121]  Gábor Stépán,et al.  Acceleration feedback improves balancing against reflex delay , 2013, Journal of The Royal Society Interface.

[122]  L. Ting,et al.  Muscle synergies characterizing human postural responses. , 2007, Journal of neurophysiology.

[123]  Aymar de Rugy,et al.  Muscle Coordination Is Habitual Rather than Optimal , 2012, The Journal of Neuroscience.

[124]  Ian David Loram,et al.  Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius , 2005, The Journal of physiology.

[125]  Martijn Wisse,et al.  A Three-Dimensional Passive-Dynamic Walking Robot with Two Legs and Knees , 2001, Int. J. Robotics Res..