Defining feasible bounds on muscle activation in a redundant biomechanical task: practical implications of redundancy.

Measured muscle activation patterns often vary significantly from musculoskeletal model predictions that use optimization to resolve redundancy. Although experimental muscle activity exhibits both inter- and intra-subject variability we lack adequate tools to quantify the biomechanical latitude that the nervous system has when selecting muscle activation patterns. Here, we identified feasible ranges of individual muscle activity during force production in a musculoskeletal model to quantify the degree to which biomechanical redundancy allows for variability in muscle activation patterns. In a detailed cat hindlimb model matched to the posture of three cats, we identified the lower and upper bounds on muscle activity in each of 31 muscles during static endpoint force production across different force directions and magnitudes. Feasible ranges of muscle activation were relatively unconstrained across force magnitudes such that only a few (0-13%) muscles were found to be truly "necessary" (e.g. exhibited non-zero lower bounds) at physiological force ranges. Most of the muscles were "optional", having zero lower bounds, and frequently had "maximal" upper bounds as well. Moreover, "optional" muscles were never selected by optimization methods that either minimized muscle stress, or that scaled the pattern required for maximum force generation. Therefore, biomechanical constraints were generally insufficient to restrict or specify muscle activation levels for producing a force in a given direction, and many muscle patterns exist that could deviate substantially from one another but still achieve the task. Our approach could be extended to identify the feasible limits of variability in muscle activation patterns in dynamic tasks such as walking.

[1]  Louise Ada,et al.  Muscle strengthening is not effective in children and adolescents with cerebral palsy: a systematic review. , 2009, The Australian journal of physiotherapy.

[2]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

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

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

[5]  F. Valero-Cuevas,et al.  Releasing the A3 pulley and leaving flexor superficialis intact increases pinch force following the Zancolli lasso procedures to prevent claw deformity in the intrinsic palsied finger , 2002, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[6]  J. Macpherson,et al.  Two functional muscle groupings during postural equilibrium tasks in standing cats. , 1996, Journal of neurophysiology.

[7]  B. Walmsley,et al.  Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats. , 1978, Journal of neurophysiology.

[8]  Rachid Ait-Haddou,et al.  Predictions of co-contraction depend critically on degrees-of-freedom in the musculoskeletal model. , 2006, Journal of biomechanics.

[9]  Nathan E. Bunderson,et al.  Reduction of neuromuscular redundancy for postural force generation using an intrinsic stability criterion. , 2008, Journal of biomechanics.

[10]  M. Tresch,et al.  Flexibility of motor pattern generation across stimulation conditions by the neonatal rat spinal cord. , 2010, Journal of neurophysiology.

[11]  F. Valero-Cuevas Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range. , 2000, Journal of neurophysiology.

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

[13]  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.

[14]  R L Lieber,et al.  Sarcomere length operating range of vertebrate muscles during movement. , 2001, The Journal of experimental biology.

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

[16]  M. Pandy,et al.  Muscular contributions to hip and knee extension during the single limb stance phase of normal gait: a framework for investigating the causes of crouch gait. , 2005, Journal of biomechanics.

[17]  W Herzog,et al.  Validation of optimization models that estimate the forces exerted by synergistic muscles. , 1991, Journal of biomechanics.

[18]  S. Delp,et al.  How robust is human gait to muscle weakness? , 2011, Gait & posture.

[19]  D. F. Hoyt,et al.  Gait and the energetics of locomotion in horses , 1981, Nature.

[20]  Lena H Ting,et al.  Ratio of shear to load ground-reaction force may underlie the directional tuning of the automatic postural response to rotation and translation. , 2004, Journal of neurophysiology.

[21]  Rieko Osu,et al.  The central nervous system stabilizes unstable dynamics by learning optimal impedance , 2001, Nature.

[22]  S. Giszter,et al.  Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors , 2004, The Journal of Neuroscience.

[23]  W Herzog,et al.  Analysis of the force-sharing problem using an optimization model. , 2004, Mathematical biosciences.

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

[25]  V R Edgerton,et al.  Architectural and histochemical properties of cat hip 'cuff' muscles. , 1997, Acta anatomica.

[26]  S. Delp,et al.  Crouched postures reduce the capacity of muscles to extend the hip and knee during the single-limb stance phase of gait. , 2008, Journal of biomechanics.

[27]  Anthony G Schache,et al.  Potential of lower-limb muscles to accelerate the body during cerebral palsy gait. , 2012, Gait & posture.

[28]  R. M. Alexander Models and the scaling of energy costs for locomotion , 2005, Journal of Experimental Biology.

[29]  A. Biewener,et al.  In vivo muscle force-length behavior during steady-speed hopping in tammar wallabies. , 1998, The Journal of experimental biology.

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

[31]  E Burdet,et al.  Motor memory and local minimization of error and effort, not global optimization, determine motor behavior. , 2010, Journal of neurophysiology.

[32]  M G Pandy,et al.  Static and dynamic optimization solutions for gait are practically equivalent. , 2001, Journal of biomechanics.

[33]  P. Rack,et al.  The effects of length and stimulus rate on tension in the isometric cat soleus muscle , 1969, The Journal of physiology.

[34]  Lena H Ting,et al.  Muscle synergy organization is robust across a variety of postural perturbations. , 2006, Journal of neurophysiology.

[35]  M. Pandy,et al.  Sensitivity of model predictions of muscle function to changes in moment arms and muscle-tendon properties: a Monte-Carlo analysis. , 2012, Journal of biomechanics.

[36]  D. A. Shreeve,et al.  An evaluation of optimization techniques for the prediction of muscle activation patterns during isometric tasks. , 1996, Journal of biomechanical engineering.

[37]  F. Horak,et al.  Central programming of postural movements: adaptation to altered support-surface configurations. , 1986, Journal of neurophysiology.

[38]  R. M. Alexander,et al.  Optimization and gaits in the locomotion of vertebrates. , 1989, Physiological reviews.

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

[40]  Rieko Osu,et al.  CNS Learns Stable, Accurate, and Efficient Movements Using a Simple Algorithm , 2008, The Journal of Neuroscience.

[41]  T Richard Nichols,et al.  Three‐dimensional model of the feline hindlimb , 2004, Journal of morphology.

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

[43]  R. Roy,et al.  Architecture of the hind limb muscles of cats: Functional significance , 1982, Journal of morphology.

[44]  Katherine M Steele,et al.  Can Strength Training Predictably Improve Gait Kinematics? A Pilot Study on the Effects of Hip and Knee Extensor Strengthening on Lower-Extremity Alignment in Cerebral Palsy , 2010, Physical Therapy.

[45]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

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

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

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

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

[50]  B. Prilutsky,et al.  Forces of individual cat ankle extensor muscles during locomotion predicted using static optimization. , 1997, Journal of biomechanics.

[51]  G. Loeb,et al.  Spinal-Like Regulator Facilitates Control of a Two-Degree-of-Freedom Wrist , 2010, The Journal of Neuroscience.