Impedance modulation: a means to cope with neuromuscular noise

Impedance modulation has been suggested as a means to suppress the effects of internal ‘noise’ on movement kinematics. We investigated this hypothesis in a neuromusculo-skeletal model. A prerequisite is that the muscle model produces realistic force variability. We found that standard Hill-type models do not predict realistic force variability in response to variability in stimulation. In contrast, a combined motor-unit pool model and a pool of parallel Hill-type motor units did produce realistic force variability as a function of target force, largely independent of how the force was transduced to the tendon. To test the main hypothesis, two versions of the latter model were simulated as an antagonistic muscle pair, controlling the position of a frictionless hinge joint, with a distal segment having realistic inertia relative to the muscle strength. Increasing the impedance through co-activation resulted in less kinematic variability, except for the lowest levels of co-activation. Model behaviour in this region was affected by the noise amplitude and the inertial properties of the model. Our simulations support the idea that muscular co-activation is in principle an effective strategy to meet accuracy demands.

[1]  Robert Sessions Woodworth,et al.  THE ACCURACY OF VOLUNTARY MOVEMENT , 1899 .

[2]  C. E. SHANNON,et al.  A mathematical theory of communication , 1948, MOCO.

[3]  J. Brobeck The Integrative Action of the Nervous System , 1948, The Yale Journal of Biology and Medicine.

[4]  P. Fitts The information capacity of the human motor system in controlling the amplitude of movement. , 1954, Journal of experimental psychology.

[5]  J. Foley The co-ordination and regulation of movements , 1968 .

[6]  H. Zelaznik,et al.  Motor-output variability: a theory for the accuracy of rapid motor acts. , 1979, Psychological review.

[7]  P. Matthews,et al.  Comparison of electromyogram spectra with force spectra during human elbow tremor. , 1980, The Journal of physiology.

[8]  O. Lippold,et al.  The tremor in fatigue. , 1981, Ciba Foundation symposium.

[9]  G. Borg Psychophysical bases of perceived exertion. , 1982, Medicine and science in sports and exercise.

[10]  R. Miall,et al.  Manual tracking of visual targets by trained monkeys , 1986, Behavioural Brain Research.

[11]  R A Abrams,et al.  Optimality in human motor performance: ideal control of rapid aimed movements. , 1988, Psychological review.

[12]  I W Hunter,et al.  System identification of human joint dynamics. , 1990, Critical reviews in biomedical engineering.

[13]  W S Levine,et al.  An optimal control model for maximum-height human jumping. , 1990, Journal of biomechanics.

[14]  T. Milner,et al.  The effect of accuracy constraints on three-dimensional movement kinematics , 1990, Neuroscience.

[15]  E. Saltzman,et al.  Steady-state and perturbed rhythmical movements: a dynamical analysis. , 1991, Journal of experimental psychology. Human perception and performance.

[16]  William L. Goffe,et al.  SIMANN: FORTRAN module to perform Global Optimization of Statistical Functions with Simulated Annealing , 1992 .

[17]  Gilmen Smyth,et al.  Cocontraction changes in muscular fatigue at different levels of isometric contraction , 1992 .

[18]  Lambert Schomaker,et al.  FITTS LAW AS A LOW-PASS FILTER EFFECT OF MUSCLE-STIFFNESS , 1992 .

[19]  D. Winter,et al.  Models of recruitment and rate coding organization in motor-unit pools. , 1993, Journal of neurophysiology.

[20]  E Cafarelli,et al.  Behavior of coactive muscles during fatigue. , 1993, Journal of applied physiology.

[21]  G. Edelman,et al.  Solving Bernstein's problem: a proposal for the development of coordinated movement by selection. , 1993, Child development.

[22]  Karl M. Newell,et al.  On postural stability and variability , 1993 .

[23]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[24]  W. Rymer,et al.  Muscle stiffness during transient and continuous movements of cat muscle: perturbation characteristics and physiological relevance , 1994, IEEE Transactions on Biomedical Engineering.

[25]  D. J. Bennett Stretch reflex responses in the human elbow joint during a voluntary movement. , 1994, The Journal of physiology.

[26]  Gerard P. van Galen,et al.  Fitts' law as the outcome of a dynamic noise filtering model of motor control , 1995 .

[27]  P. Matthews Relationship of firing intervals of human motor units to the trajectory of post‐spike after‐hyperpolarization and synaptic noise. , 1996, The Journal of physiology.

[28]  R. Stein,et al.  Identification of intrinsic and reflex contributions to human ankle stiffness dynamics , 1997, IEEE Transactions on Biomedical Engineering.

[29]  R. Howe,et al.  Identification of the mechanical impedance at the human finger tip. , 1997, Journal of biomechanical engineering.

[30]  Robert E. Kearney,et al.  Identification of time-varying stiffness dynamics of the human ankle joint during an imposed movement , 1997, Experimental Brain Research.

[31]  G P Van Galen,et al.  Stress, neuromotor noise, and human performance: a theoretical perspective. , 1997, Journal of experimental psychology. Human perception and performance.

[32]  C. Marsden,et al.  Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing , 1997, Experimental Brain Research.

[33]  Charles L. Webber,et al.  Lumbar paraspinal muscle fatigability in repetitive isoinertial loading: EMG spectral indices, Borg scale and endurance time , 1997, European Journal of Applied Physiology and Occupational Physiology.

[34]  R Plamondon,et al.  Speed/accuracy trade-offs in target-directed movements , 1997, Behavioral and Brain Sciences.

[35]  Li-Qun Zhang,et al.  Simultaneous and nonlinear identification of mechanical and reflex properties of human elbow joint muscles , 1997, IEEE Transactions on Biomedical Engineering.

[36]  G E Stelmach,et al.  Coactivation to reduce variability in the elderly. , 1998, Motor control.

[37]  H. Teulings,et al.  Axial pen force increases with processing demands in handwriting. , 1998, Acta psychologica.

[38]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[39]  G P Van Galen,et al.  Auditory stress effects on preparation and execution of graphical aiming: a test of the neuromotor noise concept. , 1998, Acta psychologica.

[40]  T. Milner,et al.  Damping of the wrist joint during voluntary movement , 1998, Experimental Brain Research.

[41]  G. Sjøgaard,et al.  Effect of speed and precision demands on human shoulder muscle electromyography during a repetitive task , 1998, European Journal of Applied Physiology and Occupational Physiology.

[42]  Maarten F. Bobbert,et al.  From twitch to tetanus for human muscle: experimental data and model predictions for m. triceps surae , 1998, Biological Cybernetics.

[43]  C J De Luca,et al.  Hand dominance and motor unit firing behavior. , 1998, Journal of neurophysiology.

[44]  Etienne Burdet,et al.  Quantization of human motions and learning of accurate movements , 1998, Biological Cybernetics.

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

[46]  R. Emmerik,et al.  A dynamical systems approach to lower extremity running injuries. , 1999, Clinical biomechanics.

[47]  K. Newell,et al.  Noise, information transmission, and force variability. , 1999, Journal of experimental psychology. Human perception and performance.

[48]  Sybert H. Stroeve,et al.  Impedance characteristics of a neuromusculoskeletal model of the human arm I. Posture control , 1999, Biological Cybernetics.

[49]  H. Gomi,et al.  Multijoint muscle regulation mechanisms examined by measured human arm stiffness and EMG signals. , 1999, Journal of neurophysiology.

[50]  Robert F. Kirsch,et al.  Multiple-input, multiple-output system identification for characterization of limb stiffness dynamics , 1999, Biological Cybernetics.

[51]  The processing of foetal magnetocardiograms , 1999 .

[52]  D J Ostry,et al.  Compensation for interaction torques during single- and multijoint limb movement. , 1999, Journal of neurophysiology.

[53]  J. Cholewicki,et al.  Effects of external trunk loads on lumbar spine stability. , 2000, Journal of biomechanics.

[54]  Gregor Schöner,et al.  Identifying the control structure of multijoint coordination during pistol shooting , 2000, Experimental Brain Research.

[55]  R. Enoka,et al.  Steadiness is reduced and motor unit discharge is more variable in old adults , 2000, Muscle & nerve.

[56]  G. P. van Galen,et al.  Error, stress and the role of neuromotor noise in space oriented behaviour. , 2000, Biological psychology.

[57]  E Burdet,et al.  A method for measuring endpoint stiffness during multi-joint arm movements. , 2000, Journal of biomechanics.

[58]  W Z Rymer,et al.  Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. , 2001, Journal of neurophysiology.

[59]  W. Helsen,et al.  A century later: Woodworth's (1899) two-component model of goal-directed aiming. , 2001, Psychological bulletin.

[60]  A. Gordon,et al.  Contribution of tactile information to accuracy in pointing movements , 2001, Experimental Brain Research.

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

[62]  R. Enoka,et al.  Activation of the arousal response and impairment of performance increase with anxiety and stressor intensity. , 2001, Journal of applied physiology.

[63]  S. Gandevia Spinal and supraspinal factors in human muscle fatigue. , 2001, Physiological reviews.

[64]  Kelvin E. Jones,et al.  Sources of signal-dependent noise during isometric force production. , 2002, Journal of neurophysiology.

[65]  Rieko Osu,et al.  Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. , 2002, Journal of neurophysiology.

[66]  Roger M Enoka,et al.  Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. , 2002, Journal of neurophysiology.

[67]  Michael I. Jordan,et al.  Optimal feedback control as a theory of motor coordination , 2002, Nature Neuroscience.

[68]  Frans C. T. van der Helm,et al.  Identification of intrinsic and reflexive components of human arm dynamics during postural control , 2002, Journal of Neuroscience Methods.

[69]  Les G Carlton,et al.  Modeling Variability of Force During Isometric Contractions of the Quadriceps Femoris , 2002, Journal of motor behavior.

[70]  D. Wolpert,et al.  Controlling the statistics of action: obstacle avoidance. , 2002, Journal of neurophysiology.

[71]  D. Ostry,et al.  Relationship between jaw stiffness and kinematic variability in speech. , 2002, Journal of neurophysiology.

[72]  Maarten F Bobbert,et al.  Initial arm muscle activation in a planar ballistic arm movement with varying external force directions: a simulation study. , 2002, Motor control.

[73]  Arend W A Van Gemmert,et al.  Forearm EMG response activity during motor performance in individuals prone to increased stress reactivity. , 2002, American journal of industrial medicine.

[74]  Inge Zijdewind,et al.  Motor fatigue and cognitive task performance in humans , 2002, The Journal of physiology.

[75]  C. Heckman,et al.  Hill muscle model errors during movement are greatest within the physiologically relevant range of motor unit firing rates. , 2003, Journal of biomechanics.

[76]  Rieko Osu,et al.  Different mechanisms involved in adaptation to stable and unstable dynamics. , 2003, Journal of neurophysiology.

[77]  K. Newell,et al.  Effects of aging on force variability, single motor unit discharge patterns, and the structure of 10, 20, and 40 Hz EMG activity , 2003, Neurobiology of Aging.

[78]  Reinhard Blickhan,et al.  Stabilizing function of antagonistic neuromusculoskeletal systems: an analytical investigation , 2003, Biological Cybernetics.

[79]  Paul L Gribble,et al.  Role of cocontraction in arm movement accuracy. , 2003, Journal of neurophysiology.

[80]  Roger M Enoka,et al.  Changes in muscle activation can prolong the endurance time of a submaximal isometric contraction in humans. , 2003, Journal of applied physiology.

[81]  W. Zev Rymer,et al.  Elbow impedance during goal-directed movements , 2003, Experimental Brain Research.

[82]  L. Selen,et al.  Trunk muscle activation in low-back pain patients, an analysis of the literature. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[83]  Roger M Enoka,et al.  Multiple features of motor-unit activity influence force fluctuations during isometric contractions. , 2003, Journal of neurophysiology.

[84]  M. Kawato,et al.  Functional significance of stiffness in adaptation of multijoint arm movements to stable and unstable dynamics , 2003, Experimental Brain Research.

[85]  Gregor Schöner,et al.  Effect of accuracy constraint on joint coordination during pointing movements , 2003, Experimental Brain Research.

[86]  D. J. Bennett Torques generated at the human elbow joint in response to constant position errors imposed during voluntary movements , 2004, Experimental Brain Research.

[87]  M. Kawato,et al.  Optimal impedance control for task achievement in the presence of signal-dependent noise. , 2004, Journal of neurophysiology.

[88]  Bart Visser,et al.  Effects of precision demands and mental pressure on muscle activation and hand forces in computer mouse tasks , 2004, Ergonomics.

[89]  M. Kawato,et al.  Impedance control balances stability with metabolically costly muscle activation. , 2004, Journal of neurophysiology.

[90]  Theodore E. Milner,et al.  Dependence of elbow viscoelastic behavior on speed and loading in voluntary movements , 2004, Experimental Brain Research.

[91]  Peter J Beek,et al.  Effector dynamics of rhythmic wrist activity and its implications for (modeling) bimanual coordination. , 2004, Human movement science.

[92]  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.

[93]  Kelvin E. Jones,et al.  The scaling of motor noise with muscle strength and motor unit number in humans , 2004, Experimental Brain Research.

[94]  R. J. van Beers,et al.  The role of execution noise in movement variability. , 2004, Journal of neurophysiology.

[95]  S. Pasalar,et al.  Effects of speeds and force fields on submovements during circular manual tracking in humans , 2005, Experimental Brain Research.

[96]  R. Enoka,et al.  Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. , 2004, Journal of applied physiology.

[97]  R. Enoka,et al.  The 1- to 2-Hz oscillations in muscle force are exacerbated by stress, especially in older adults. , 2004, Journal of applied physiology.

[98]  J. H. van Dieen,et al.  Does activity reduce the influence of neural noise on motor performance , 2004 .

[99]  M. Latash,et al.  Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis , 2005, Experimental Brain Research.

[100]  M. Latash,et al.  Learning multi-finger synergies: an uncontrolled manifold analysis , 2004, Experimental Brain Research.

[101]  Maarten F. Bobbert,et al.  The contribution of muscle properties in the control of explosive movements , 1993, Biological Cybernetics.

[102]  J. Scholz,et al.  Learning a throwing task is associated with differential changes in the use of motor abundance , 2005, Experimental Brain Research.

[103]  T J Ebner,et al.  Kinematic analysis of manual tracking in monkeys: characterization of movement intermittencies during a circular tracking task. , 2004, Journal of neurophysiology.

[104]  Ruud G. J. Meulenbroek,et al.  Differential effects of mental load on proximal and distal arm muscle activity , 2005, Experimental Brain Research.

[105]  S. Schaal,et al.  Computational motor control in humans and robots , 2005, Current Opinion in Neurobiology.

[106]  Ruud G. J. Meulenbroek,et al.  Trunk use and co-contraction in cerebral palsy as regulatory mechanisms for accuracy control , 2005, Neuropsychologia.

[107]  M. Pozzo,et al.  Relationship between perceived exertion and mean power frequency of the EMG signal from the upper trapezius muscle during isometric shoulder elevation , 2005, European Journal of Applied Physiology.

[108]  Karl-Theodor Kalveram,et al.  Threading neural feedforward into a mechanical spring: How biology exploits physics in limb control , 2005, Biological Cybernetics.

[109]  J. Sandfeld,et al.  Effect of computer mouse gain and visual demand on mouse clicking performance and muscle activation in a young and elderly group of experienced computer users. , 2005, Applied ergonomics.

[110]  C. Moritz,et al.  Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. , 2005, Journal of neurophysiology.

[111]  Idsart Kingma,et al.  Factors underlying the perturbation resistance of the trunk in the first part of a lifting movement , 2005, Biological Cybernetics.

[112]  J. Houk,et al.  Kinematic properties of on-line error corrections in the monkey , 2005, Experimental Brain Research.

[113]  R. Enoka,et al.  Time to task failure differs with load type when old adults perform a submaximal fatiguing contraction , 2005, Muscle & nerve.

[114]  R. Enoka,et al.  Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults , 2005, Muscle & nerve.

[115]  J. Hollerbach,et al.  Time-varying stiffness of human elbow joint during cyclic voluntary movement , 2005, Experimental Brain Research.

[116]  A. Barto,et al.  Approximate optimal control as a model for motor learning. , 2005, Psychological review.

[117]  Daniel M Wolpert,et al.  Optimal control of redundant muscles in step-tracking wrist movements. , 2005, Journal of neurophysiology.

[118]  Peter J. Beek,et al.  Impedance is modulated to meet accuracy demands during goal-directed arm movements , 2006, Experimental Brain Research.

[119]  T. Sinkjaer,et al.  Contribution of afferent feedback to the soleus muscle activity during human locomotion. , 2005, Journal of neurophysiology.

[120]  Deric Wisleder,et al.  Influence of biomechanical factors on substructure of pointing movements , 2005, Experimental Brain Research.

[121]  Peter J. Beek,et al.  Can co-activation reduce kinematic variability? A simulation study , 2005, Biological Cybernetics.

[122]  Maarten F Bobbert,et al.  Length-dependent [Ca2+] sensitivity adds stiffness to muscle. , 2005, Journal of biomechanics.

[123]  Wouter Hulstijn,et al.  Muscular co-contraction covaries with task load to control the flow of motion in fine motor tasks , 2005, Biological Psychology.

[124]  Dario Farina,et al.  Experimental muscle pain changes motor control strategies in dynamic contractions , 2005, Experimental Brain Research.

[125]  Maarten F Bobbert,et al.  Is equilibrium point control feasible for fast goal-directed single-joint movements? , 2006, Journal of neurophysiology.

[126]  J. H. van Dieen,et al.  Joint impedance attenuates neuro-muscular noise during target tracking , 2006 .

[127]  The nervous system transitions rapidly between incompatible control strategies by predictively exploiting the margins of error of the task , 2006 .

[128]  J. Cholewicki,et al.  The effects of trunk stiffness on postural control during unstable seated balance , 2006, Experimental Brain Research.

[129]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[130]  I. Hwang,et al.  Exertion dependent alternations in force fluctuation and limb acceleration during sustained fatiguing contraction , 2006, European Journal of Applied Physiology.

[131]  Peter J Beek,et al.  Impedance modulation and feedback corrections in tracking targets of variable size and frequency. , 2006, Journal of neurophysiology.

[132]  C. Christakos,et al.  Parallel neuronal mechanisms underlying physiological force tremor in steady muscle contractions of humans. , 2006, Journal of neurophysiology.

[133]  Karl M. Newell,et al.  Are age-related increases in force variability due to decrements in strength? , 2006, Experimental Brain Research.

[134]  K. Granata,et al.  Active trunk stiffness increases with co-contraction. , 2006, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[135]  Neville Hogan,et al.  Avoiding Spurious Submovement Decompositions II: A Scattershot Algorithm , 2006, Biological Cybernetics.

[136]  L. Selen,et al.  Fatigue-induced changes of impedance and performance in target tracking , 2007, Experimental Brain Research.

[137]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[138]  J. Lackner,et al.  Fingertip contact influences human postural control , 2007, Experimental Brain Research.

[139]  Mary A. Shook,et al.  Chronic Work-Related Myalgia: Neuromuscular Mechanisms Behind Work-Related Chronic Muscle Pain Syndromes , 2008 .

[140]  M. Desmurget,et al.  Computational motor control: feedback and accuracy , 2008, The European journal of neuroscience.

[141]  J H van Dieën,et al.  Fatigue effects on tracking performance and muscle activity. , 2008, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[142]  L. Selen,et al.  Suppression of neuromuscular noise through impedance modulation , 2008 .