Hierarchies of synergies: an example of two-hand, multi-finger tasks

We explored the ability of the central nervous system (CNS) to assemble synergies stabilizing the output of sets of effectors at two levels of a control hierarchy. Specifically, we asked a question: can the CNS organize both two-hand and within-a-hand force stabilizing synergies in a simple two-hand force production task that involves two fingers per hand? Intuitively, one could expect a positive answer; that is, forces produced by each hand are expected to co-vary negatively across trials to bring down the total force variability, while forces produced by each finger within-a-hand are expected to co-vary negatively to reduce the variability of that hand’s contribution to the total force. The subjects were instructed to follow a trapezoidal time profile with the signal corresponding to the force produced by a set of instructed fingers in one-hand tasks with two-finger force production and in two-hand tasks with involvement of both symmetrical and asymmetrical finger pairs in the two hands. Finger force co-variation across trials was quantified and used as an index of stabilization of the force produced by all the instructed fingers, and of the force produced by finger pairs within-a-hand. No major differences were seen between the dominant and the non-dominant hand and between the two-hand tasks with symmetrical and asymmetrical finger involvement. Stronger synergies were seen in the index–middle finger pair as compared to the ring-little finger pair. The main result of the study is the significantly weaker or even lacking two-finger force stabilizing synergies within-a-hand during two-hand tasks while such synergies were present in one-hand tasks. This observation points at a potential limitation in the ability of the CNS to organize synergies at two levels of a control hierarchy simultaneously. It also allows suggesting a hypothesis on two types of synergies in the human motor repertoire, well-practiced synergies that form a library serving as the foundation for all novel actions, and freshly assembled synergies.

[1]  D. Domkin,et al.  Structure of joint variability in bimanual pointing tasks , 2002, Experimental Brain Research.

[2]  Robert L. Sainburg,et al.  Handedness: Differential Specializations for Control of Trajectory and Position , 2005, Exercise and sport sciences reviews.

[3]  Robert L Sainburg,et al.  Interlimb differences in control of movement extent. , 2004, Journal of neurophysiology.

[4]  Vladimir M. Zatsiorsky,et al.  Anticipatory covariation of finger forces during self-paced and reaction time force production , 2005, Neuroscience Letters.

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

[6]  Sun Wook Kim,et al.  Anticipatory adjustments of multi-finger synergies in preparation for self-triggered perturbations , 2006, Experimental Brain Research.

[7]  Vladimir M. Zatsiorsky,et al.  Coupling phenomena during asynchronous submaximal two-hand, multi-finger force production tasks in humans , 2002, Neuroscience Letters.

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

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

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

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

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

[13]  Minoru Shinohara,et al.  Effects of age and gender on finger coordination in MVC and submaximal force-matching tasks. , 2003, Journal of applied physiology.

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

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

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

[17]  J. F. Soechting,et al.  Force synergies for multifingered grasping , 2000, Experimental Brain Research.

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

[19]  Mark L. Latash,et al.  A study of a bimanual synergy associated with holding an object , 1998 .

[20]  B. Vereijken,et al.  Free(z)ing Degrees of Freedom in Skill Acquisition , 1992 .

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

[22]  M. Latash,et al.  Prehension synergies: trial-to-trial variability and principle of superposition during static prehension in three dimensions. , 2005, Journal of neurophysiology.

[23]  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.

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

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

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

[27]  J. Massion,et al.  Postural forearm changes induced by predictable in time or voluntary triggered unloading in man , 2004, Experimental Brain Research.

[28]  M. Latash,et al.  Two kinematic synergies in voluntary whole-body movements during standing. , 2006, Journal of neurophysiology.

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

[30]  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.

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

[32]  M. Latash,et al.  Muscle synergies involved in shifting the center of pressure while making a first step , 2005, Experimental Brain Research.

[33]  J. Massion,et al.  Acquisition of co-ordination between posture and movement in a bimanual task , 2004, Experimental Brain Research.

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

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

[36]  M. Latash,et al.  Muscle synergies during shifts of the center of pressure by standing persons , 2003, Experimental Brain Research.

[37]  M. Latash,et al.  Motor variability within a multi-effector system: experimental and analytical studies of multi-finger production of quick force pulses , 2005, Experimental Brain Research.

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

[39]  J. Abbs,et al.  Control of complex motor gestures: orofacial muscle responses to load perturbations of lip during speech. , 1984, Journal of neurophysiology.

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

[41]  Jae Kun Shim,et al.  Is there a timing synergy during multi-finger production of quick force pulses? , 2004, Experimental brain research.

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

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

[44]  M. Latash,et al.  Muscle synergies during voluntary body sway: combining across-trials and within-a-trial analyses , 2006, Experimental Brain Research.

[45]  Mark L. Latash,et al.  Joint angle variability in 3D bimanual pointing: uncontrolled manifold analysis , 2005, Experimental Brain Research.