The internal model and the leading joint hypothesis: implications for control of multi-joint movements

This article presents a theoretical generalization of recent experimental findings accumulated in support of two concepts of inter-segmental dynamics regulation during multi-joint movements. The concepts are the internal model of inter-segmental dynamics and the leading joint hypothesis (LJH). The internal model of limb dynamics is a well-established interpretation of feed-forward control. Recent experiments have generated new information about the organization of the internal model and its role in regulation of inter-segmental dynamics. The LJH, which proposes a simplified principle of the regulation of inter-segmental dynamics, is at the beginning stage of development. This paper outlines major results obtained in these two research directions and demonstrates that the two groups of findings complement and augment each other, suggesting a simple and robust hierarchical strategy of multi-joint movement control that exploits specific mechanical properties of human limbs.

[1]  F. Mussa-Ivaldi,et al.  The motor system does not learn the dynamics of the arm by rote memorization of past experience. , 1997, Journal of neurophysiology.

[2]  J. J. Buchanan,et al.  Self-organization of trajectory formation , 1997, Biological Cybernetics.

[3]  Peter H. Greene,et al.  Problems of Organization of Motor Systems , 1972 .

[4]  A. Gentile,et al.  A kinematic comparison of single and multijoint pointing movements , 2004, Experimental Brain Research.

[5]  M. Latash,et al.  The relation between posture and movement: A study of a simple synergy in a two-joint task , 1995 .

[6]  W. T. Thach,et al.  Cerebellar ataxia: abnormal control of interaction torques across multiple joints. , 1996, Journal of neurophysiology.

[7]  G. F. Koshland,et al.  Selection of muscles for initiation of planar, three-joint arm movements with different final orientations of the hand , 2004, Experimental Brain Research.

[8]  M. Hallett,et al.  Single-joint rapid arm movements in normal subjects and in patients with motor disorders. , 1996, Brain : a journal of neurology.

[9]  J. F. Soechting,et al.  Coordination of arm movements in three-dimensional space. Sensorimotor mapping during drawing movement , 1986, Neuroscience.

[10]  G. Koshland,et al.  Control of the wrist in three-joint arm movements to multiple directions in the horizontal plane. , 2000, Journal of neurophysiology.

[11]  James R. Bloedel,et al.  On-line compensation for perturbations of a reaching movement is cerebellar dependent: support for the task dependency hypothesis , 2004, Experimental Brain Research.

[12]  Paul Cisek,et al.  Kinematics and kinetics of multijoint reaching in nonhuman primates. , 2003, Journal of neurophysiology.

[13]  W. H. Warren,et al.  Why change gaits? Dynamics of the walk-run transition. , 1995, Journal of experimental psychology. Human perception and performance.

[14]  J. Cooke,et al.  Influence of joint interactional effects on the coordination of planar two-joint arm movements , 2004, Experimental Brain Research.

[15]  G. E. Stelmach,et al.  Commonalities and differences in control of various drawing movements , 2002, Experimental Brain Research.

[16]  John J. Buchanan,et al.  Learning a single limb multijoint coordination pattern: the impact of a mechanical constraint on the coordination dynamics of learning and transfer , 2004, Experimental Brain Research.

[17]  Tomaso Poggio,et al.  Generalization in vision and motor control , 2004, Nature.

[18]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[19]  J. Konczak,et al.  The development toward stereotypic arm kinematics during reaching in the first 3 years of life , 1997, Experimental Brain Research.

[20]  G. Stelmach,et al.  Changes in multi-joint performance with age. , 2002, Motor control.

[21]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[22]  Natalia V Dounskaia,et al.  Influence of biomechanical constraints on horizontal arm movements. , 2002, Motor control.

[23]  Robert L. Sainburg,et al.  Limitations in interlimb transfer of visuomotor rotations , 2004, Experimental Brain Research.

[24]  E. Thelen,et al.  Understanding movement control in infants through the analysis of limb intersegmental dynamics. , 1990, Journal of motor behavior.

[25]  M. Gazzaniga,et al.  The new cognitive neurosciences , 2000 .

[26]  Reza Shadmehr,et al.  Computational nature of human adaptive control during learning of reaching movements in force fields , 1999, Biological Cybernetics.

[27]  Reza Shadmehr,et al.  Learned dynamics of reaching movements generalize from dominant to nondominant arm. , 2003, Journal of neurophysiology.

[28]  R A Scheidt,et al.  Control strategies for the transition from multijoint to single-joint arm movements studied using a simple mechanical constraint. , 2000, Journal of neurophysiology.

[29]  Robert L. Sainburg,et al.  Interlimb transfer of load compensation during rapid elbow joint movements , 2005, Experimental Brain Research.

[30]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[31]  N. Hogan,et al.  Does the nervous system use equilibrium-point control to guide single and multiple joint movements? , 1992, The Behavioral and brain sciences.

[32]  Donald G. MacKay,et al.  The organization of perception and action. A theory for language and other cognitive skills , 1987, The Italian Journal of Neurological Sciences.

[33]  J. A. Scott Kelso,et al.  Self-organization of trajectory formation , 1997, Biological Cybernetics.

[34]  R. F. Zernicke,et al.  Adaptive Dynamics of the Leg Movement Patterns of Human Infants: II. Treadmill stepping in Infants and Adults. , 1994, Journal of motor behavior.

[35]  Natalia V Dounskaia,et al.  Age-related differences in the control of multijoint movements. , 2004, Motor control.

[36]  David A. Rosenbaum,et al.  Hierarchical organization of motor programs. , 1987 .

[37]  James Gordon,et al.  Accuracy of planar reaching movements , 1994, Experimental Brain Research.

[38]  H. Barlow Vision: A computational investigation into the human representation and processing of visual information: David Marr. San Francisco: W. H. Freeman, 1982. pp. xvi + 397 , 1983 .

[39]  Robert L. Sainburg,et al.  Spatial representations and internal models of limb dynamics in motor learning , 1999 .

[40]  Mitsuo Kawato,et al.  A neural network model for arm trajectory formation using forward and inverse dynamics models , 1993, Neural Networks.

[41]  C. Sherrington Observations on the scratch‐reflex in the spinal dog , 1906, The Journal of physiology.

[42]  Mark L. Latash,et al.  Mirror Writing: Learning, Transfer, and Implications for Internal Inverse Models. , 1999, Journal of motor behavior.

[43]  L. A. Jeffress,et al.  Cerebral Mechanisms in Behavior , 1953 .

[44]  Gerard P. van Galen,et al.  Handwriting: Issues for a psychomotor theory ☆ , 1991 .

[45]  John M. Hollerbach,et al.  Dynamic interactions between limb segments during planar arm movement , 1982, Biological Cybernetics.

[46]  J. Kelso,et al.  Self-organization of trajectory formation. I. Experimental evidence. , 1997, Biological cybernetics.

[47]  Reza Shadmehr,et al.  Learning of action through adaptive combination of motor primitives , 2000, Nature.

[48]  R Shadmehr,et al.  Spatial Generalization from Learning Dynamics of Reaching Movements , 2000, The Journal of Neuroscience.

[49]  J R Flanagan,et al.  The Role of Internal Models in Motion Planning and Control: Evidence from Grip Force Adjustments during Movements of Hand-Held Loads , 1997, The Journal of Neuroscience.

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

[51]  E Bizzi,et al.  Motor learning by field approximation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Hagiwara,et al.  The calcium channel , 1983, Trends in Neurosciences.

[53]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[54]  M. Hoy,et al.  Modulation of limb dynamics in the swing phase of locomotion. , 1984, Journal of biomechanics.

[55]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.

[56]  V. Hatzitaki,et al.  Dynamic joint analysis as a method to document coordination disabilities associated with Parkinson's disease. , 1998, Clinical biomechanics.

[57]  O. I. Fukson,et al.  The spinal frog takes into account the scheme of its body during the wiping reflex. , 1980, Science.

[58]  Stephan P. Swinnen,et al.  Directional tuning effects during cyclical two-joint arm movements in the horizontal plane , 2001, Experimental Brain Research.

[59]  S. Schaal,et al.  Origins and violations of the 2/3 power law in rhythmic three-dimensional arm movements , 2000, Experimental Brain Research.

[60]  A. G. Feldman Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .

[61]  G L Gottlieb,et al.  Muscle activation patterns during two types of voluntary single-joint movement. , 1998, Journal of neurophysiology.

[62]  David J. Ostry,et al.  A critical evaluation of the force control hypothesis in motor control , 2003, Experimental Brain Research.

[63]  Natalia Dounskaia,et al.  Disruptions in joint control during drawing arm movements in Parkinson’s disease , 2005, Experimental Brain Research.

[64]  J. Lackner,et al.  Rapid adaptation to Coriolis force perturbations of arm trajectory. , 1994, Journal of neurophysiology.

[65]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[67]  K. Manal,et al.  Shoulder and elbow joint power differ as a general feature of vertical arm movements , 2004, Experimental Brain Research.

[68]  Stephan P. Swinnen,et al.  A Principle of Control of Rapid Multijoint Movements , 2000 .

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

[70]  P L Gribble,et al.  Inter-joint coupling strategy during adaptation to novel viscous loads in human arm movement. , 2004, Journal of neurophysiology.

[71]  K. Lashley The problem of serial order in behavior , 1951 .

[72]  Jack M. Winters,et al.  Biomechanics and Neural Control of Posture and Movement , 2011, Springer New York.

[73]  Lambert Schomaker,et al.  Limb-Segment Selection in Drawing Behaviour , 1993, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[74]  R. Schmidt A schema theory of discrete motor skill learning. , 1975 .

[75]  N. V. Dounskaia Artificial potential method for control of constrained robot motion , 1998, IEEE Trans. Syst. Man Cybern. Part B.

[76]  Amy J. Bastian,et al.  Inter- and intra-limb generalization of adaptation during catching , 2001, Experimental Brain Research.

[77]  D. Meyer,et al.  Control of Serial Order in Rapidly Spoken Syllable Sequences , 1987 .

[78]  Daniel M Wolpert,et al.  Spatial representation of predictive motor learning. , 2003, Journal of neurophysiology.

[79]  David J Ostry,et al.  Generalization of motor learning based on multiple field exposures and local adaptation. , 2005, Journal of neurophysiology.

[80]  W. T. Thach,et al.  Cerebellar ataxia: torque deficiency or torque mismatch between joints? , 2000, Journal of neurophysiology.

[81]  J. Lackner,et al.  Coordinated turn-and-reach movements. I. Anticipatory compensation for self-generated coriolis and interaction torques. , 2003, Journal of neurophysiology.

[82]  C. Atkeson,et al.  Learning arm kinematics and dynamics. , 1989, Annual review of neuroscience.

[83]  M. Kawato,et al.  Internal representations of the motor apparatus: implications from generalization in visuomotor learning. , 1995, Journal of experimental psychology. Human perception and performance.

[84]  R. Zernicke,et al.  Biomechanics and developmental neuromotor control. , 1993, Child development.

[85]  K. Kudo,et al.  Utilization and compensation of interaction torques during ball-throwing movements. , 2003, Journal of neurophysiology.

[86]  C. Chandler,et al.  Computers, brains and the control of movement , 1982, Trends in Neurosciences.

[87]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[88]  P. Zangger,et al.  Muscle spindle control during locomotor movements generated by the deafferented spinal cord. , 1976, Acta physiologica Scandinavica.

[89]  D. Anton Occupational biomechanics , 1986 .

[90]  Yury P. Shimansky Spinal motor control system incorporates an internal model of limb dynamics , 2000, Biological Cybernetics.

[91]  Yury P. Shimansky,et al.  Principles of organization of neural systems controlling automatic movements in animals , 1992, Progress in Neurobiology.

[92]  G. Stelmach,et al.  Multijoint movement control in Parkinson's disease , 2001, Experimental Brain Research.

[93]  David J Ostry,et al.  Transfer of Motor Learning across Arm Configurations , 2002, The Journal of Neuroscience.

[94]  R. Shadmehr,et al.  A Real-Time State Predictor in Motor Control: Study of Saccadic Eye Movements during Unseen Reaching Movements , 2002, The Journal of Neuroscience.

[95]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[96]  W. Rymer,et al.  Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics , 2000, Experimental Brain Research.

[97]  J. Lackner,et al.  Motor adaptation to Coriolis force perturbations of reaching movements: endpoint but not trajectory adaptation transfers to the nonexposed arm. , 1995, Journal of neurophysiology.

[98]  G. Koshland,et al.  General coordination of shoulder, elbow and wrist dynamics during multijoint arm movements , 2001, Experimental Brain Research.

[99]  R L Sainburg,et al.  Intersegmental dynamics are controlled by sequential anticipatory, error correction, and postural mechanisms. , 1999, Journal of neurophysiology.

[100]  Timothy D. Lee,et al.  Motor Control and Learning: A Behavioral Emphasis , 1982 .

[101]  D. Mackay The Organization of Perception and Action , 1987 .

[102]  S. P. Swinnen,et al.  Hierarchical control of different elbow-wrist coordination patterns , 1998, Experimental Brain Research.