The scaling of motor noise with muscle strength and motor unit number in humans

Understanding the origin of noise, or variability, in the motor system is an important step towards understanding how accurate movements are performed. Variability of joint torque during voluntary activation is affected by many factors such as the precision of the descending motor commands, the number of muscles that cross the joint, their size and the number of motor units in each. To investigate the relationship between the peripheral factors and motor noise, the maximum voluntary torque produced at a joint and the coefficient of variation of joint torque were recorded from six adult human subjects for four muscle/joint groups in the arm. It was found that the coefficient of variation of torque decreases systematically as the maximum voluntary torque increases. This decreasing coefficient of variation means that a given torque or force can be more accurately generated by a stronger muscle than a weaker muscle. Simulations demonstrated that muscles with different strengths and different numbers of motor units could account for the experimental data. In the simulations, the magnitude of the coefficient of variation of muscle force depended primarily on the number of motor units innervating the muscle, which relates positively to muscle strength. This result can be generalised to the situation where more than one muscle is available to perform a task, and a muscle activation pattern must be selected. The optimal muscle activation pattern required to generate a target torque using a group of muscles, while minimizing the consequences of signal dependent noise, is derived.

[1]  C. Sherrington,et al.  Numbers and Contraction-Values of Individual Motor-Units Examined in some Muscles of the Limb , 1930 .

[2]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

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

[4]  B. Feinstein,et al.  Morphologic studies of motor units in normal human muscles. , 1955, Acta anatomica.

[5]  J. Basmajian,et al.  Integrated actions and functions of the chief flexors of the elbow: a detailed electromyographic analysis. , 1957, The Journal of bone and joint surgery. American volume.

[6]  E. Henneman Relation between size of neurons and their susceptibility to discharge. , 1957, Science.

[7]  E CHRISTENSEN,et al.  TOPOGRAPHY OF TERMINAL MOTOR INNERVATION IN STRIATED MUSCLES FROM STILLBORN INFANTS , 1959, American journal of physical medicine.

[8]  R. D. Montgomery Growth of Human Striated Muscle , 1962, Nature.

[9]  G. Somjen,et al.  Excitability and inhibitability of motoneurons of different sizes. , 1965, Journal of neurophysiology.

[10]  E Henneman,et al.  Responses of motoneurons of different sizes to graded stimulation of supraspinal centers of the brain. , 1965, Journal of neurophysiology.

[11]  M. A. MacConaill,et al.  The Ergonomic Aspects of Articular Mechanics , 1966 .

[12]  O. L. Zangwill,et al.  Mechanisms of motor skill development , 1972 .

[13]  J Tanji,et al.  Firing rate of individual motor units in voluntary contraction of abductor digiti minimi muscle in man. , 1973, Experimental neurology.

[14]  Study of motor units and arrangement of myons of human musculus plantaris. , 1976, Acta anatomica.

[15]  H. Devries MUSCLES ALIVE-THEIR FUNCTIONS REVEALED BY ELECTROMYOGRAPHY , 1976 .

[16]  B. P. Yeo Investigations concerning the principle of minimal total muscular force. , 1976, Journal of biomechanics.

[17]  D. Irving,et al.  The numbers of limb motor neurons in the human lumbosacral cord throughout life , 1977, Journal of the Neurological Sciences.

[18]  Antonio Pedotti,et al.  Optimization of muscle-force sequencing in human locomotion , 1978 .

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

[20]  F Buchthal,et al.  Motor unit of mammalian muscle. , 1980, Physiological reviews.

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

[22]  R. L. Linscheid,et al.  Muscles across the elbow joint: a biomechanical analysis. , 1981, Journal of biomechanics.

[23]  E. Bizzi,et al.  Human arm trajectory formation. , 1982, Brain : a journal of neurology.

[24]  R. Johansson,et al.  Changes in motoneurone firing rates during sustained maximal voluntary contractions. , 1983, The Journal of physiology.

[25]  D. McCloskey,et al.  Detections of movements imposed on finger, elbow and shoulder joints. , 1983, The Journal of physiology.

[26]  M. A. Townsend,et al.  Muscular synergism--I. On criteria for load sharing between synergistic muscles. , 1984, Journal of biomechanics.

[27]  B. Gustafsson,et al.  An investigation of threshold properties among cat spinal alpha‐motoneurones. , 1984, The Journal of physiology.

[28]  G. E. Johnson,et al.  Muscular synergism--II. A minimum-fatigue criterion for load sharing between synergistic muscles. , 1984, Journal of biomechanics.

[29]  M. Binder,et al.  Distribution of oligosynaptic group I input to the cat medial gastrocnemius motoneuron pool. , 1985, Journal of neurophysiology.

[30]  B. Calancie,et al.  Limitations of the spike‐triggered averaging technique , 1986, Muscle & nerve.

[31]  P. Helm Clinical mechanics of the hand , 1986 .

[32]  L Stark,et al.  Estimated mechanical properties of synergistic muscles involved in movements of a variety of human joints. , 1988, Journal of biomechanics.

[33]  C. Gielen,et al.  Coordination and inhomogeneous activation of human arm muscles during isometric torques. , 1988, Journal of neurophysiology.

[34]  Edmund Y. S. Chao,et al.  Biomechanics of the hand : a basic research study , 1989 .

[35]  J. Stephens,et al.  Synchronization of motor unit activity during voluntary contraction in man. , 1990, The Journal of physiology.

[36]  M. Flanders,et al.  Arm muscle activation for static forces in three-dimensional space. , 1990, Journal of neurophysiology.

[37]  J F Yang,et al.  Methods for estimating the number of motor units in human muscles , 1990, Annals of neurology.

[38]  R S Johansson,et al.  Measurement of contractile and electrical properties of single human thenar motor units in response to intraneural motor-axon stimulation. , 1990, Journal of neurophysiology.

[39]  T. Miles,et al.  Discharge variability and physiological properties of human masseter motor units , 1991, Brain Research.

[40]  M. Bromberg,et al.  Motor unit number estimation, isometric strength, and electromyographic measures in amyotrophic lateral sclerosis , 1993, Muscle & nerve.

[41]  T S Buchanan,et al.  Estimation of muscle forces about the wrist joint during isometric tasks using an EMG coefficient method. , 1993, Journal of biomechanics.

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

[43]  R. Enoka,et al.  Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. , 1993, Journal of neurophysiology.

[44]  R M Enoka,et al.  Training-related enhancement in the control of motor output in elderly humans. , 1994, Journal of applied physiology.

[45]  G. A. Robinson,et al.  Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. , 1994, Journal of applied physiology.

[46]  J. L. Taylor,et al.  Detection of movements imposed on human hip, knee, ankle and toe joints. , 1995, The Journal of physiology.

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

[48]  Mark B. Bromberg,et al.  Relationships between motor-unit number estimates and isometric strength in distal muscles in ALS/MND , 1996, Journal of the Neurological Sciences.

[49]  C. Gielen,et al.  The relative activation of elbow-flexor muscles in isometric flexion and in flexion/extension movements. , 1997, Journal of biomechanics.

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

[51]  J. Semmler,et al.  Motor unit discharge and force tremor in skill- and strength-trained individuals , 1998, Experimental Brain Research.

[52]  F. Zajac,et al.  Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. , 1998, Journal of biomechanics.

[53]  A. McComas,et al.  1998 ISEK Congress Keynote Lecture: Motor units: how many, how large, what kind? International Society of Electrophysiology and Kinesiology. , 1998, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[54]  E. Luschei,et al.  Discharge characteristics of laryngeal single motor units during phonation in young and older adults and in persons with parkinson disease. , 1999, Journal of neurophysiology.

[55]  Stan C. A. M. Gielen,et al.  A comparison of models explaining muscle activation patterns for isometric contractions , 1999, Biological Cybernetics.

[56]  R M Enoka,et al.  Task- and age-dependent variations in steadiness. , 1999, Progress in brain research.

[57]  D. Hoffman,et al.  Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. , 1999, Journal of neurophysiology.

[58]  S. Kuwabara,et al.  Dissociated small hand muscle involvement in amyotrophic lateral sclerosis detected by motor unit number estimates , 1999, Muscle & nerve.

[59]  R. Enoka,et al.  Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. , 2000, Journal of neurophysiology.

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

[61]  A. Fuglevand,et al.  Discharge behaviour of single motor units during maximal voluntary contractions of a human toe extensor , 2000, The Journal of physiology.

[62]  K. Newell,et al.  Age differences in noise and variability of isometric force production. , 2001, Journal of experimental child psychology.

[63]  C. Luchies,et al.  The effects of motion on force control abilities. , 2001, Clinical biomechanics.

[64]  T J Doherty,et al.  Contractile properties of human motor units in health, aging, and disease , 2001, Muscle & nerve.

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

[66]  Scott L. Delp,et al.  Three-dimensional spatial tuning of neck muscle activation in humans , 2002, Experimental Brain Research.

[67]  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.

[68]  Ashvin Shah,et al.  A computational model of muscle recruitment for wrist movements. , 2002, Journal of neurophysiology.

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

[70]  R. Enoka,et al.  Mechanisms that contribute to differences in motor performance between young and old adults. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

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

[72]  P. Morasso Spatial control of arm movements , 2004, Experimental Brain Research.