Muscle synergies during voluntary body sway: combining across-trials and within-a-trial analyses

We investigated co-varied changes in muscle activity during voluntary sway tasks that required a quick shift of the center of pressure (COP). We hypothesized that multi-muscle synergies (defined as task-specific covariation of elemental variables, muscle modes) stabilize a COP location in the anterior–posterior direction prior to a voluntary COP shift and that during the shift the synergies would weaken. Standing subjects performed two tasks, a cyclic COP shift over a range corresponding to 80% of the maximal amplitude of voluntary COP shift at 1 Hz and a unidirectional quick COP shift over the same nominal amplitude. The cyclic sway task was used to define muscle modes (M-modes, leg and trunk muscle groups with parallel scaling of muscle activation level within a group) and the relations between small changes in the magnitudes of M-modes [in the principal component analysis (PCA), the M-mode magnitudes are equivalent to PC scores] and COP shifts. A novel approach was used involving PCA applied to indices of muscle integrated activity measured both within a trial and across trials. The unidirectional sway task was performed in a self-paced (SP) manner and under a typical simple reaction time (RT) instruction. M-modes were also defined along trials at those tasks; they have been shown to be similar across tasks. Integrated indices of muscle activity in the SP-sway and RT-sway tasks were transformed into the M-modes. Variance in the M-mode space was partitioned into two components, one that did not affect the average value of COP shift (VUCM) and the other that did (VORT). An index (ΔV) corresponding to the normalized difference between VUCM and VORT was computed. During steady-state posture, ΔV was positive corresponding to most M-mode variance lying in a sub-space corresponding to a stable COP location across trials. Positive ΔV values have been interpreted as reflecting a multi-M-mode synergy stabilizing the COP location. The magnitude of ΔV was larger in SP trials than in RT trials. During voluntary COP shifts, the ΔV magnitude dropped to zero or even became negative. We conclude that M-mode synergies stabilize COP location during quiet standing, while these synergies weaken or disappear during fast voluntary COP shifts. Under RT conditions, the COP stabilizing synergies were weaker supposedly to facilitate a quick COP shift without time for preparation. The suggested method of M-mode identification may potentially be applied to analysis of postural synergies in persons with impaired postural control such as elderly persons, persons with atypical development, or in the course of rehabilitation after an injury.

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

[2]  F. Horak,et al.  Central programming of postural movements: adaptation to altered support-surface configurations. , 1986, Journal of neurophysiology.

[3]  S. Bouisset,et al.  Segmental Movement as a Perturbation to Balance? Facts and Concepts , 1990 .

[4]  Jack M. Winters,et al.  Multiple Muscle Systems , 1990, Springer New York.

[5]  G. L. Gottlieb,et al.  Reconstruction of shifting elbow joint compliant characteristics during fast and slow movements , 1991, Neuroscience.

[6]  M. Latash,et al.  Electromechanical delay: An experimental artifact. , 1992, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[7]  J. Massion Movement, posture and equilibrium: Interaction and coordination , 1992, Progress in Neurobiology.

[8]  G. Schöner Recent Developments and Problems in Human Movement Science and Their Conceptual Implications , 1995 .

[9]  D. Winter,et al.  Unified theory regarding A/P and M/L balance in quiet stance. , 1996, Journal of neurophysiology.

[10]  M. Latash,et al.  Anticipatory postural adjustments during self-paced and reaction-time movements , 1998, Experimental Brain Research.

[11]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

[12]  J. Massion,et al.  Axial synergies during human upper trunk bending , 1998, Experimental Brain Research.

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

[14]  M. Merzenich,et al.  Computational model of the role of sensory disorganization in focal task-specific dystonia. , 2000, Journal of neurophysiology.

[15]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

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

[17]  M. Latash,et al.  Motor Control Strategies Revealed in the Structure of Motor Variability , 2002, Exercise and sport sciences reviews.

[18]  M. Latash,et al.  Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes , 2003, Biological Cybernetics.

[19]  M. Latash,et al.  Muscle modes during shifts of the center of pressure by standing persons: effect of instability and additional support , 2004, Experimental Brain Research.

[20]  F. Popescu,et al.  Implications of low mechanical impedance in upper limb reaching motion. , 2003, Motor control.

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

[22]  Vladimir M. Zatsiorsky,et al.  Finger interaction during accurate multi-finger force production tasks in young and elderly persons , 2004, Experimental Brain Research.

[23]  D. J. Bennett Torques generated at the human elbow joint in response to constant position errors imposed during voluntary movements , 2004, Experimental Brain Research.

[24]  Neville Hogan,et al.  Stability properties of human reaching movements , 2004, Experimental Brain Research.

[25]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[26]  M. Latash,et al.  Age-related changes in finger coordination in static prehension tasks. , 2004, Journal of applied physiology.

[27]  Wynne A. Lee,et al.  Effects of arm acceleration and behavioral conditions on the organization of postural adjustments during arm flexion , 2004, Experimental Brain Research.

[28]  Lena H Ting,et al.  A limited set of muscle synergies for force control during a postural task. , 2005, Journal of neurophysiology.

[29]  E. Bizzi,et al.  Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors , 2005, The Journal of Neuroscience.

[30]  Fethi Ben Ouezdou,et al.  Adjustment of the human arm viscoelastic properties to the direction of reaching , 2006, Biological Cybernetics.

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

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

[33]  J. Hollerbach,et al.  Time-varying stiffness of human elbow joint during cyclic voluntary movement , 2005, Experimental Brain Research.

[34]  Marcos Duarte,et al.  Speed-accuracy trade-off in voluntary postural movements. , 2005, Motor control.

[35]  F. Lacquaniti,et al.  Coordination of Locomotion with Voluntary Movements in Humans , 2005, The Journal of Neuroscience.

[36]  Emilio Bizzi,et al.  Shared and specific muscle synergies in natural motor behaviors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[38]  Andrea d'Avella,et al.  Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. , 2006, Journal of neurophysiology.

[39]  Vladimir M. Zatsiorsky,et al.  Muscle synergies involved in preparation to a step made under the self-paced and reaction time instructions , 2006, Clinical Neurophysiology.