Reach-to-grasp movement as a minimization process

It is known that hand transport and grasping are functionally different but spatially coordinated components of reach-to-grasp (RTG) movements. As an extension of this notion, we suggested that body segments involved in RTG movements are controlled as a coherent ensemble by a global minimization process associated with the necessity for the hand to reach the motor goal. Different RTG components emerge following this process without pre-programming. Specifically, the minimization process may result from the tendency of neuromuscular elements to diminish the spatial gap between the actual arm-hand configuration and its virtual (referent) configuration specified by the brain. The referent configuration is specified depending on the object shape, localization, and orientation. Since the minimization process is gradual, it can be interrupted and resumed following mechanical perturbations, at any phase during RTG movements, including hand closure. To test this prediction of the minimization hypothesis, we asked subjects to reach and grasp a cube placed within the reach of the arm. Vision was prevented during movement until the hand returned to its initial position. As predicted, by arresting wrist motion at different points of hand transport in randomly selected trials, it was possible to halt changes in hand aperture at any phase, not only during hand opening but also during hand closure. Aperture changes resumed soon after the wrist was released. Another test of the minimization hypothesis was made in RTG movements to an object placed beyond the reach of the arm. It has previously been shown (Rossi et al. in J Physiol 538:659–671, 2002) that in such movements, the trunk motion begins to contribute to hand transport only after a critical phase when the shifts in the referent arm configuration have finished (at about the time when hand velocity is maximal). The minimization rule suggests that when the virtual contribution of the arm to hand transport is completed, guidance of hand aperture switches from the arm to the trunk control system. As a consequence, hand aperture changes can be halted by trunk arrests but only if they are prolonged beyond a critical phase. As predicted, hand transport and hand aperture in RTG movements beyond the reach of the arm were halted by trunk arrests only if they were prolonged beyond the time of peak hand velocity. Hand motion and aperture changes resumed only when the trunk was released. While supporting the minimization hypothesis, our findings imply that not only spatial but also temporal characteristics of each component, including the shortest, hand closure component of RTG movements, are controlled in a flexible, task-specific way.

[1]  J. R. Bloedel,et al.  Adaptation of reach-to-grasp movement in response to force perturbations , 2003, Experimental Brain Research.

[2]  M. Jeannerod,et al.  Orienting the finger opposition space during prehension movements. , 1994, Journal of motor behavior.

[3]  Yury P. Shimansky,et al.  Role of vision in aperture closure control during reach-to-grasp movements , 2007, Experimental Brain Research.

[4]  C. Prablanc,et al.  Integrated control of hand transport and orientation during prehension movements , 1996, Experimental Brain Research.

[5]  R N Lemon,et al.  The importance of the cortico-motoneuronal system for control of grasp. , 1998, Novartis Foundation symposium.

[6]  A G Feldman,et al.  Vestibular system may provide equivalent motor actions regardless of the number of body segments involved in the task. , 2007, Journal of neurophysiology.

[7]  M. L. McCurdy,et al.  Contribution of primate magnocellular red nucleus to timing of hand preshaping during reaching to grasp. , 2002, Journal of neurophysiology.

[8]  Mindy F Levin,et al.  Threshold position control and the principle of minimal interaction in motor actions. , 2007, Progress in brain research.

[9]  A. G. Feldman,et al.  Referent configuration of the body: a global factor in the control of multiple skeletal muscles , 2004, Experimental Brain Research.

[10]  Daniel M. Dubois,et al.  Computing Anticipatory Systems , 1998 .

[11]  B. Bergum,et al.  Attention and performance IX , 1982 .

[12]  M. Jeannerod The timing of natural prehension movements. , 1984, Journal of motor behavior.

[13]  M. Jeannerod,et al.  Influence of object position and size on human prehension movements , 1997, Experimental Brain Research.

[14]  S. Keele,et al.  Toward a Functional Analysis of the Basal Ganglia , 1998, Journal of Cognitive Neuroscience.

[15]  Emanuel Todorov,et al.  Evidence for the Flexible Sensorimotor Strategies Predicted by Optimal Feedback Control , 2007, The Journal of Neuroscience.

[16]  Patrick Haggard,et al.  Coordinated responses following mechanical perturbation of the arm during prehension , 2004, Experimental Brain Research.

[17]  P. Cheney,et al.  Properties of primary motor cortex output to forelimb muscles in rhesus macaques. , 2004, Journal of neurophysiology.

[18]  Bruce Bridgeman,et al.  Efference copy and its limitations , 2007, Comput. Biol. Medicine.

[19]  M Flanders,et al.  Coordination of a step with a reach. , 2000, Journal of vestibular research : equilibrium & orientation.

[20]  Miya K. Rand,et al.  Effect of speed manipulation on the control of aperture closure during reach-to-grasp movements , 2006, Experimental Brain Research.

[21]  Alan M. Wing,et al.  Remote responses to perturbation in human prehension , 1991, Neuroscience Letters.

[22]  S. Adamovich,et al.  Pointing in 3D space to remembered targets. I. Kinesthetic versus visual target presentation. , 1998, Journal of neurophysiology.

[23]  D. Wolpert,et al.  Motor prediction , 2001, Current Biology.

[24]  Jean-Louis Vercher,et al.  On the nature of the vestibular control of arm-reaching movements during whole-body rotations , 2005, Experimental Brain Research.

[25]  G. Stelmach,et al.  Reach-to-grasp movements during obstacle avoidance , 1998, Experimental Brain Research.

[26]  S. Adamovich,et al.  Pointing in 3D space to remembered targets II: Effects of movement speed toward kinesthetically defined targets , 1999, Experimental Brain Research.

[27]  E. Brenner,et al.  A new view on grasping. , 1999, Motor control.

[28]  M Jeannerod,et al.  Grasping an object: one movement, several components. , 1998, Novartis Foundation symposium.

[29]  A. G. Feldman,et al.  Control processes underlying elbow flexion movements may be independent of kinematic and electromyographic patterns: experimental study and modelling , 1997, Neuroscience.

[30]  A G Feldman,et al.  One-trial adaptation of movement to changes in load. , 1996, Journal of neurophysiology.

[31]  J. R. Bloedel,et al.  Control of aperture closure during reach-to-grasp movements in parkinson’s disease , 2005, Experimental Brain Research.

[32]  Anatol G. Feldman,et al.  Threshold position control of arm movement with anticipatory increase in grip force , 2007, Experimental Brain Research.

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

[34]  Archana P. Sangole,et al.  Palmar arch dynamics during reach-to-grasp tasks , 2008, Experimental Brain Research.

[35]  A. G. Feldman,et al.  The influence of different descending systems on the tonic stretch reflex in the cat. , 1972, Experimental neurology.

[36]  Alan Wing,et al.  Coordination of hand aperture with the spatial path of hand transport , 1998, Experimental Brain Research.

[37]  Jiping He,et al.  Control of hand orientation and arm movement during reach and grasp , 2006, Experimental Brain Research.

[38]  Howard Poizner,et al.  Hand trajectory invariance in reaching movements involving the trunk , 2001, Experimental Brain Research.

[39]  A. G. Feldman,et al.  The origin and use of positional frames of reference in motor control , 1995, Behavioral and Brain Sciences.

[40]  M. Jeannerod Intersegmental coordination during reaching at natural visual objects , 1981 .

[41]  A R Gibson,et al.  Construction of a reach-to-grasp. , 2007, Novartis Foundation symposium.

[42]  A. G. Feldman,et al.  The timing of control signals underlying fast point-to-point arm movements , 2001, Experimental Brain Research.

[43]  M. Berkinblit,et al.  Pointing to remembered targets in 3-D space in Parkinson's disease. , 1998, Motor control.

[44]  Arnold Mitnitski,et al.  Sequential control signals determine arm and trunk contributions to hand transport during reaching in humans , 2002, The Journal of physiology.

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

[46]  J. Lackner,et al.  Coriolis-force-induced trajectory and endpoint deviations in the reaching movements of labyrinthine-defective subjects. , 2001, Journal of neurophysiology.

[47]  James R. Bloedel,et al.  Temporal control of the reach and grip components during a prehension task in humans , 1996, Neuroscience Letters.

[48]  P. Matthews A study of certain factors influencing the stretch reflex of the decerebrate cat , 1959, The Journal of physiology.

[49]  Jonathan Vaughan,et al.  The posture-based motion planning framework: new findings related to object manipulation, moving around obstacles, moving in three spatial dimensions, and haptic tracking. , 2009, Advances in experimental medicine and biology.

[50]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[52]  M Jeannerod,et al.  Models for the programming of goal-directed movements (or how to get things less complex). , 1986, Archives internationales de physiologie et de biochimie.

[53]  J. Steeves,et al.  Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrate cat , 2004, Experimental Brain Research.

[54]  G. Stelmach,et al.  Grip reorganization during wrist transport: the influence of an Altered aperture , 1996, Experimental Brain Research.

[55]  Anatol G. Feldman,et al.  Basic elements of arm postural control analyzed by unloading , 2005, Experimental Brain Research.

[56]  A. G. Feldman,et al.  Central modifications of reflex parameters may underlie the fastest arm movements. , 1997, Journal of neurophysiology.

[57]  Michael T Turvey,et al.  Nature of motor control: perspectives and issues. , 2009, Advances in experimental medicine and biology.

[58]  Yiannis Demiris,et al.  Object Grasping using the Minimum Variance Model , 2006, Biological Cybernetics.

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

[60]  Tamar Flash,et al.  Motor primitives in vertebrates and invertebrates , 2005, Current Opinion in Neurobiology.

[61]  S.C.J. Garth,et al.  Neural networks for artificial intelligence , 1989 .

[62]  G. Stelmach,et al.  Alterations in transport path differentially affect temporal and spatial movement parameters , 2002, Experimental Brain Research.

[63]  M. Flanders,et al.  Do arm postures vary with the speed of reaching? , 1999, Journal of neurophysiology.

[64]  Anatol G. Feldman,et al.  Threshold control of arm posture and movement adaptation to load , 2006, Experimental Brain Research.

[65]  A. G. Feldman New insights into action–perception coupling , 2009, Experimental Brain Research.

[66]  Roland S. Johansson,et al.  Modulation of corticospinal influence over hand muscles during gripping tasks in man and monkey , 1996 .

[67]  Martha L. McCurdy,et al.  Discharge of primate magnocellular red nucleus neurons during reaching to grasp in different spatial locations , 2001, Experimental Brain Research.

[68]  J. Houk,et al.  Outline for a Theory of Motor Behavior: Involving Cooperative Actions of the Cerebellum, Basal Ganglia, and Cerebral Cortex , 1993 .

[69]  George E. Stelmach,et al.  Spatial and temporal control of trunk-assisted prehensile actions , 2000, Experimental Brain Research.

[70]  Michelle J Johnson,et al.  Attractor and Lyapunov models for reach and grasp movements with application to robot-assisted therapy. , 2009, Nonlinear dynamics, psychology, and life sciences.

[71]  Jinsung Wang,et al.  Coordination among the body segments during reach-to-grasp action involving the trunk , 1998, Experimental Brain Research.

[72]  Armin Biess,et al.  A Computational Model for Redundant Human Three-Dimensional Pointing Movements: Integration of Independent Spatial and Temporal Motor Plans Simplifies Movement Dynamics , 2007, The Journal of Neuroscience.