Hierarchical control of static prehension: II. Multi-digit synergies

The purpose of this study was to explore the ability of the central nervous system (CNS) to organize synergies at two levels of a hypothetical control hierarchy involved in two-hand multi-finger prehension tasks with one or more persons participating in the task together. At the higher level of the hierarchy, the total force and moment of force produced on an object are distributed between the thumb and the virtual finger (an imagined finger with mechanical output equal to the involved fingers of the hand), while at the lower level the virtual finger action is distributed among the four fingers. We tested a hypothesis that the CNS is able to organize synergies at only one level of the hierarchy. The subjects held vertically one of the two handles, a narrow one and a wide one. They used the four fingers of the right hand opposed by the right hand thumb, the left hand thumb, the left hand index finger, the thumb of an experimenter, the index finger of an experimenter, or an inanimate object. Forces and moments of force produced by each digit were recorded. Indices of synergies stabilizing the mechanical output variables at each of the two levels were computed. Contrary to the expectations, force and moment of force stabilizing synergies were found at one or both levels of the hierarchy across all tasks. Unimanual tasks exhibited higher synergy indices compared to all tasks, while intrapersonal synergy indices were higher than those of interpersonal synergies. The results suggest that both feed-forward and feedback mechanisms may be used to create force and moment of force stabilizing synergies. We invoke the notion of chain effects and generalize it for relations among variance components related to stabilization of different mechanical variables. The reference configuration hypothesis offers a fruitful framework for analysis of prehension synergies.

[1]  M. Latash,et al.  Prehension Synergies , 2004, Exercise and sport sciences reviews.

[2]  Andrew M Gordon,et al.  Development of hand-arm bimanual intensive training (HABIT) for improving bimanual coordination in children with hemiplegic cerebral palsy. , 2006, Developmental medicine and child neurology.

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

[4]  N. A. Bernstein Dexterity and Its Development , 1996 .

[5]  Michael A Riley,et al.  Synergies in intra- and interpersonal interlimb rhythmic coordination. , 2007, Motor control.

[6]  E. Brenner,et al.  Independent movements of the digits in grasping , 2001, Experimental Brain Research.

[7]  Jae Kun Shim,et al.  Prehension synergies in three dimensions. , 2005, Journal of neurophysiology.

[8]  Stacey L. Gorniak,et al.  Hierarchical control of static prehension: I. Biomechanics , 2009, Experimental Brain Research.

[9]  K. Newell,et al.  The scaling of human grip configurations. , 1999, Journal of experimental psychology. Human perception and performance.

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

[11]  M. Loève Probability theory : foundations, random sequences , 1955 .

[12]  Mark L Latash,et al.  Multifinger Prehension: An Overview , 2008, Journal of motor behavior.

[13]  A. G. Feldman Once more on the equilibrium-point hypothesis (lambda model) for motor control. , 1986, Journal of motor behavior.

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

[15]  Mark Latash,et al.  Tangential load sharing among fingers during prehension , 2004, Ergonomics.

[16]  Slobodan Jaric,et al.  Elaborate force coordination of precision grip could be generalized to bimanual grasping techniques , 2007, Neuroscience Letters.

[17]  M L Latash,et al.  On the problem of adequate language in motor control. , 1998, Motor control.

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

[19]  Stacey L. Gorniak,et al.  Hierarchies of synergies: an example of two-hand, multi-finger tasks , 2007, Experimental Brain Research.

[20]  Vladimir M. Zatsiorsky,et al.  Do synergies decrease force variability? A study of single-finger and multi-finger force production , 2008, Experimental Brain Research.

[21]  R S Johansson,et al.  Sensory input and control of grip. , 1998, Novartis Foundation symposium.

[22]  M. Arbib Coordinated control programs for movements of the hand , 1985 .

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

[24]  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.

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

[26]  Bert Steenbergen,et al.  Fingertip force control during bimanual object lifting in hemiplegic cerebral palsy , 2008, Experimental Brain Research.

[27]  A. M. Smith,et al.  Activity in rostral motor cortex in response to predictable force-pulse perturbations in a precision grip task. , 2001, Journal of neurophysiology.

[28]  Fan Gao,et al.  Finger force vectors in multi-finger prehension. , 2003, Journal of biomechanics.

[29]  F. Huddle Coordination , 1966, Open Knowledge Institutions.

[30]  J. F. Soechting,et al.  Two virtual fingers in the control of the tripod grasp. , 2001, Journal of neurophysiology.

[31]  Karl M. Newell,et al.  Coordination of Grip Configurations as a Function of Force Output , 2000, Journal of motor behavior.

[32]  C. Winstein,et al.  Bimanual Training After Stroke: Are Two Hands Better Than One? , 2004, Topics in stroke rehabilitation.

[33]  M. Turvey,et al.  Phase transitions and critical fluctuations in the visual coordination of rhythmic movements between people. , 1990, Journal of experimental psychology. Human perception and performance.

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

[35]  M. Latash,et al.  Control of finger force direction in the flexion-extension plane , 2005, Experimental Brain Research.

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

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

[38]  K. Newell,et al.  Body-scaled transitions in human grip configurations. , 2000, Journal of experimental psychology. Human perception and performance.

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

[40]  Stacey L. Gorniak,et al.  Emerging and disappearing synergies in a hierarchically controlled system , 2007, Experimental Brain Research.

[41]  S. Jaric,et al.  Interlimb and within limb force coordination in static bimanual manipulation task , 2005, Experimental Brain Research.

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

[43]  M. Latash,et al.  Learning multi-finger synergies: an uncontrolled manifold analysis , 2004, Experimental Brain Research.

[44]  J. Foley The co-ordination and regulation of movements , 1968 .

[45]  T. Flash,et al.  The control of hand equilibrium trajectories in multi-joint arm movements , 1987, Biological Cybernetics.

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

[47]  M. Latash,et al.  Prehension synergies: Effects of object geometry and prescribed torques , 2002, Experimental Brain Research.

[48]  Roland S. Johansson,et al.  Sensory Control of Dexterous Manipulation in Humans , 1996 .