Rapid Correction of Aimed Movements by Summation of Force-Field Primitives

Spinal circuits form building blocks for movement construction. In the frog, such building blocks have been described as isometric force fields. Microstimulation studies showed that individual force fields can be combined by vector summation. Summation and scaling of a few force-field types can, in theory, produce a large range of dynamic force-field structures associated with limb behaviors. We tested for the first time whether force-field summation underlies the construction of real limb behavior in the frog. We examined the organization of correction responses that circumvent path obstacles during hindlimb wiping trajectories. Correction responses were triggered on-line during wiping by cutaneous feedback signaling obstacle collision. The correction response activated a force field that summed with an ongoing sequence of force fields activated during wiping. Both impact force and time of impact within the wiping motor pattern scaled the evoked correction response amplitude. However, the duration of the correction response was constant and similar to the duration of other muscles activated in different phases of wiping. Thus, our results confirm that both force-field summation and scaling occur during real limb behavior, that force fields represent fixed-timing motor elements, and that these motor elements are combined in chains and in combination contingent on the interaction of feedback and central motor programs.

[1]  Jean-Jacques E. Slotine,et al.  Robot analysis and control , 1988, Autom..

[2]  E. Bizzi,et al.  The construction of movement by the spinal cord , 1999, Nature Neuroscience.

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

[4]  Mark D'Esposito,et al.  Letter from the Special Issue Editor , 2000, Journal of Cognitive Neuroscience.

[5]  G. Loeb Motoneurone task groups: coping with kinematic heterogeneity. , 1985, The Journal of experimental biology.

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

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

[8]  S. Rossignol,et al.  A kinematic and electromyographic study of cutaneous reflexes evoked from the forelimb of unrestrained walking cats. , 1987, Journal of neurophysiology.

[9]  Maja J. Matarić,et al.  Behavior-based primitives for articulated control , 1998 .

[10]  F. A. Mussa-lvaldi,et al.  Convergent force fields organized in the frog's spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Matthew M. Williamson,et al.  Postural primitives: Interactive Behavior for a Humanoid Robot Arm , 1996 .

[12]  Emilio Bizzi,et al.  Modular organization of motor behavior in the frog's spinal cord , 1995, Trends in Neurosciences.

[13]  H. Forssberg Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. , 1979, Journal of neurophysiology.

[14]  Pattie Maes,et al.  Postural primitives: Interactive Behavior for a Humanoid Robot Arm , 1996 .

[15]  O. I. Fukson,et al.  Adaptability of innate motor patterns and motor control mechanisms , 1986, Behavioral and Brain Sciences.

[16]  S. Giszter,et al.  Afferent roles in hindlimb wipe-reflex trajectories: free-limb kinematics and motor patterns. , 2000, Journal of neurophysiology.

[17]  E. Bizzi,et al.  Low dimensionality of supraspinally induced force fields. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  S. Giszter,et al.  Output Units of Motor Behavior: An Experimental and Modeling Study , 2000, Journal of Cognitive Neuroscience.

[19]  William J. Kargo,et al.  Augmenting Postural Primitives in Spinal Cord: Dynamic Force-Field Structures Used in Trajectory Generation , 2000 .

[20]  W. Rymer,et al.  Wipe and flexion reflexes of the frog. I. Kinematics and EMG patterns. , 1993, Journal of neurophysiology.

[21]  C Ghez,et al.  The control of rapid limb movement in the cat. IV. Updating of ongoing isometric responses. , 1984, Experimental brain research.

[22]  E. Bizzi,et al.  Kinematic strategies and sensorimotor transformations in the wiping movements of frogs. , 1989, Journal of neurophysiology.

[23]  Robert M. Sanner,et al.  Stable Adaptive Control of Robot Manipulators Using Neural Networks , 1995, Neural Computation.

[24]  F A Mussa-Ivaldi,et al.  Computations underlying the execution of movement: a biological perspective. , 1991, Science.

[25]  William J. Kargo,et al.  Conserved temporal dynamics and vector superposition of primitives in frog wiping reflexes during spontaneous extensor deletions , 2000, Neurocomputing.

[26]  E. Bizzi,et al.  Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog. , 1998, Journal of neurophysiology.

[27]  W J Kargo,et al.  Segmental Afferent Regulation of Hindlimb Wiping in the Spinal Frog , 1998, Annals of the New York Academy of Sciences.

[28]  Ferdinando A. Mussa-Ivaldi,et al.  Nonlinear force fields: a distributed system of control primitives for representing and learning movements , 1997, Proceedings 1997 IEEE International Symposium on Computational Intelligence in Robotics and Automation CIRA'97. 'Towards New Computational Principles for Robotics and Automation'.

[29]  E. Bizzi,et al.  Linear combinations of primitives in vertebrate motor control. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.

[31]  P. Stein,et al.  Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  T. Nichols A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. , 1994, Acta anatomica.

[33]  P. Stein The vertebrate scratch reflex. , 1983, Symposia of the Society for Experimental Biology.

[34]  J. Smith,et al.  Adaptive control for backward quadrupedal walking. III. Stumbling corrective reactions and cutaneous reflex sensitivity. , 1993, Journal of neurophysiology.

[35]  Jean-Jacques E Slotine,et al.  The intermediate cerebellum may function as a wave-variable processor , 1996, Neuroscience Letters.

[36]  N. Hogan,et al.  Quantization of continuous arm movements in humans with brain injury. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Jean-Jacques E. Slotine,et al.  Space-frequency localized basis function networks for nonlinear system estimation and control , 1995, Neurocomputing.

[38]  Arthur Prochazka,et al.  Sensory control of locomotion , 1997, Proceedings of the 1997 American Control Conference (Cat. No.97CH36041).

[39]  Joseph A. Doeringer,et al.  Intermittency in preplanned elbow movements persists in the absence of visual feedback. , 1998, Journal of neurophysiology.