Interaction of finger enslaving and error compensation in multiple finger force production

Previous studies have documented two patterns of finger interaction during multi-finger pressing tasks, enslaving and error compensation, which do not agree with each other. Enslaving is characterized by positive correlation between instructed (master) and non-instructed (slave) finger(s) while error compensation can be described as a pattern of negative correlation between master and slave fingers. We hypothesize that pattern of finger interaction, enslaving or compensation depends on the initial force level and the magnitude of the targeted force change. Subjects were instructed to press with four fingers (I index, M middle, R ring, and L little) from a specified initial force to target forces following a ramp target line. Force–force relations between master and each of three slave fingers were analyzed during the ramp phase of trials by calculating correlation coefficients within each master–slave pair and then two-factor ANOVA was performed to determine effect of initial force and force increase on the correlation coefficients. It was found that, as initial force increased, the value of the correlation coefficient decreased and in some cases became negative, i.e. the enslaving transformed into error compensation. Force increase magnitude had a smaller effect on the correlation coefficients. The observations support the hypothesis that the pattern of inter-finger interaction—enslaving or compensation—depends on the initial force level and, to a smaller degree, on the targeted magnitude of the force increase. They suggest that the controller views tasks with higher steady-state forces and smaller force changes as implying a requirement to avoid large changes in the total force.

[1]  C. Verdan,et al.  Syndrome of the quadriga. , 1960, The Surgical clinics of North America.

[2]  Donald O. Walter,et al.  Models of the structural-functional organization of certain biological systems , 1973 .

[3]  Michael H. Kutner.  Applied Linear Statistical Models , 1974 .

[4]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

[5]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[6]  Anomalous insertion of the flexor pollicis longus. , 1982, The Journal of hand surgery.

[7]  T. Ohtsuki.  Inhibition of individual fingers during grip strength exertion. , 1981, Ergonomics.

[8]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[9]  Tatsuyuki Ohtsuki,et al.  Decrease in human voluntary isometric arm strength induced by simultaneous bilateral exertion , 1983, Behavioural Brain Research.

[10]  R. Johansson,et al.  Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. , 1984, Human neurobiology.

[11]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[12]  R. Lemon,et al.  Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. , 1986, The Journal of physiology.

[13]  W. Mcmaster,et al.  Permissible limits of flexor digitorum profundus tendon advancement--an anatomic study. , 1987, The Journal of hand surgery.

[14]  A. Rico Aguado,et al.  Flexor digitorum profundus common to thumb and index finger, associated with a post-traumatic distal adherence of both tendons. , 1988, Journal of hand surgery.

[15]  L. Ruby,et al.  Variations of the flexor digitorum superficialis of the small finger. , 1989, The Journal of hand surgery.

[16]  T. Reilly,et al.  Journal of Sports Sciences , 2011, Journal of sports sciences.

[17]  P. Stern,et al.  Tendinitis, overuse syndromes, and tendon injuries. , 1990, Hand clinics.

[18]  Robert A. Chase,et al.  Principles of Human Anatomy, Fifth Edition , 1990 .

[19]  M J Botte,et al.  Anatomy of the juncturae tendinum of the hand. , 1990, The Journal of hand surgery.

[20]  Ellen R. Girden,et al.  ANOVA: Repeated Measures , 1991 .

[21]  S. Bandinelli,et al.  Motor reorganization after upper limb amputation in man. A study with focal magnetic stimulation. , 1991, Brain : a journal of neurology.

[22]  M. Schieber.  Individuated finger movements of rhesus monkeys: a means of quantifying the independence of the digits. , 1991, Journal of neurophysiology.

[23]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[24]  W P Cooney,et al.  Flexor tendon forces: in vivo measurements. , 1992, The Journal of hand surgery.

[25]  C. Archontides,et al.  Inter-limb interactions and constraints in the expression of maximum force: a review, some implications and suggested underlying mechanisms. , 1993, Journal of sports sciences.

[26]  C J Snijders,et al.  The hand of the musician: the kinematics of the bidigital finger system with anatomical restrictions. , 1993, Journal of biomechanics.

[27]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[28]  S. Gandevia,et al.  Limited independent flexion of the thumb and fingers in human subjects. , 1994, The Journal of physiology.

[29]  J. Donoghue,et al.  Shared neural substrates controlling hand movements in human motor cortex. , 1995, Science.

[30]  MH Schieber.  Muscular production of individuated finger movements: the roles of extrinsic finger muscles , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Loukia D. Loukopoulos,et al.  Planning reaches by evaluating stored postures. , 1995, Psychological review.

[32]  G. Gottlieb,et al.  Coordinating movement at two joints: a principle of linear covariance. , 1996, Journal of neurophysiology.

[33]  J N Leijnse,et al.  Measuring force transfers in the deep flexors of the musician's hand: theoretical analysis, clinical examples. , 1997, Journal of biomechanics.

[34]  W J Kraemer,et al.  Muscle activation and force production during bilateral and unilateral concentric and isometric contractions of the knee extensors in men and women at different ages. , 1997, Electromyography and clinical neurophysiology.

[35]  M. Latash,et al.  A principle of error compensation studied within a task of force production by a redundant set of fingers , 1998, Experimental Brain Research.

[36]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

[37]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.

[38]  Vladimir M. Zatsiorsky,et al.  Coordinated force production in multi-finger tasks: finger interaction and neural network modeling , 1998, Biological Cybernetics.

[39]  Karl M. Newell,et al.  Motor redundancy during maximal voluntary contraction in four-finger tasks , 1998, Experimental Brain Research.

[40]  Israel M. Gelfand,et al.  Changes in the force-sharing pattern induced by modifications of visual feedback during force production by a set of fingers , 1998, Experimental Brain Research.

[41]  J. Massion,et al.  Axial synergies during human upper trunk bending , 1998, Experimental Brain Research.

[42]  M. Latash,et al.  Force sharing among fingers as a model of the redundancy problem , 1998, Experimental Brain Research.

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

[44]  T. Cope,et al.  Recruitment order among motoneurons from different motor nuclei. , 1999, Journal of neurophysiology.

[45]  Timothy C. Cope,et al.  Orderly recruitment among motoneurons supplying different muscles , 1999, Journal of Physiology-Paris.

[46]  J. Massion,et al.  Kinematic synergies and equilibrium control during trunk movement under loaded and unloaded conditions , 1999, Experimental Brain Research.

[47]  M H Schieber,et al.  Quantifying the Independence of Human Finger Movements: Comparisons of Digits, Hands, and Movement Frequencies , 2000, The Journal of Neuroscience.

[48]  M. Latash,et al.  Enslaving effects in multi-finger force production , 2000, Experimental Brain Research.

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

[50]  Vladimir M. Zatsiorsky,et al.  Characteristics of finger force production during one- and two-hand tasks , 2000 .

[51]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

[52]  Gabriel Curio,et al.  Representational overlap of adjacent fingers in multiple areas of human primary somatosensory cortex depends on electrical stimulus intensity: an fMRI study , 2001, Brain Research.

[53]  M. Schieber.  Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[54]  M. Latash,et al.  Structure of motor variability in marginally redundant multifinger force production tasks , 2001, Experimental Brain Research.

[55]  Gregor Schöner,et al.  Understanding finger coordination through analysis of the structure of force variability , 2002, Biological Cybernetics.

[56]  M. Latash,et al.  Motor Control Strategies Revealed in the Structure of Motor Variability , 2002, Exercise and sport sciences reviews.

[57]  Mark L Latash,et al.  Central mechanisms of finger interaction during one- and two-hand force production at distal and proximal phalanges , 2002, Brain Research.

[58]  S. Slobounov,et al.  The role of sub-maximal force production in the enslaving phenomenon , 2002, Brain Research.

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

[60]  M. Latash,et al.  Finger coordination during discrete and oscillatory force production tasks , 2002, Experimental Brain Research.

[61]  Nirmal K. Bose,et al.  Anatomically and experimentally based neural networks modeling force coordination in static multi-finger tasks , 2002, Neurocomputing.

[62]  Vladimir M Zatsiorsky,et al.  Optimization-Based Models of Muscle Coordination , 2002, Exercise and sport sciences reviews.

[63]  S C Gandevia,et al.  Distribution of the forces produced by motor unit activity in the human flexor digitorum profundus , 2002, The Journal of physiology.

[64]  S. Slobounov,et al.  Motor-related cortical potentials accompanying enslaving effect in single versus combination of fingers force production tasks , 2002, Clinical Neurophysiology.

[65]  Gregor Schöner,et al.  A mode hypothesis for finger interaction during multi-finger force-production tasks , 2003, Biological Cybernetics.

[66]  Vladimir M. Zatsiorsky,et al.  Finger interaction during multi-finger tasks involving finger addition and removal , 2003, Experimental Brain Research.

[67]  M. Latash,et al.  Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes , 2003, Biological Cybernetics.

[68]  Jae Kun Shim,et al.  The human central nervous system needs time to organize task-specific covariation of finger forces , 2003, Neuroscience Letters.

[69]  Fan Gao,et al.  Matrix analyses of interaction among fingers in static force production tasks , 2003, Biological Cybernetics.

[70]  M. Latash,et al.  Prehension synergies: trial-to-trial variability and hierarchical organization of stable performance , 2003, Experimental Brain Research.

[71]  M. Latash,et al.  Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without Down syndrome , 2003, Experimental Brain Research.

[72]  Vladimir M. Zatsiorsky,et al.  Finger interaction during accurate multi-finger force production tasks in young and elderly persons , 2004, Experimental Brain Research.

[73]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[74]  Hans Hultborn,et al.  Key mechanisms for setting the input-output gain across the motoneuron pool. , 2004, Progress in brain research.

[75]  Teresa L Brininger,et al.  Motion enslaving among multiple fingers of the human hand. , 2004, Motor control.

[76]  Y. Shinoda,et al.  Spinal branching of pyramidal tract neurons in the monkey , 1979, Experimental Brain Research.

[77]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[78]  L. Nashner,et al.  Relation of automatic postural responses and reaction-time voluntary movements of human leg muscles , 2004, Experimental Brain Research.

[79]  Vladimir M. Zatsiorsky,et al.  A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model , 2005, Biological Cybernetics.

[80]  Halla B. Olafsdottir,et al.  The emergence and disappearance of multi-digit synergies during force-production tasks , 2005, Experimental Brain Research.

[81]  Mark L. Latash,et al.  Feed-forward control of a redundant motor system , 2006, Biological Cybernetics.

[82]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[83]  Todd C. Pataky,et al.  Finger interaction during maximal radial and ulnar deviation efforts: experimental data and linear neural network modeling , 2007, Experimental Brain Research.

[84]  Gregor Schöner,et al.  Toward a new theory of motor synergies. , 2007, Motor control.

[85]  Sheng Li,et al.  Error compensation during finger force production after one- and four-finger voluntarily fatiguing exercise , 2007, Experimental Brain Research.

[86]  M. Latash,et al.  Digit force adjustments during finger addition/removal in multi-digit prehension , 2008, Experimental Brain Research.

[87]  Marcos Duarte,et al.  Do synergies improve accuracy? A study of speed-accuracy trade-offs during finger force production. , 2008, Motor control.

[88]  Sun Wook Kim,et al.  Finger inter-dependence: linking the kinetic and kinematic variables. , 2008, Human Movement Science.

[89]  Mark L Latash,et al.  Multifinger ab- and adduction strength and coordination. , 2008, Journal of hand therapy : official journal of the American Society of Hand Therapists.

[90]  J. Szentágothai,et al.  Brain Research , 2009, Experimental Neurology.

[91]  R. K. Simpson.  Nature Neuroscience , 2022 .