Load emphasizes muscle effort minimization during selection of arm movement direction

BackgroundDirectional preferences during center-out horizontal shoulder-elbow movements were previously established for both the dominant and non-dominant arm with the use of a free-stroke drawing task that required random selection of movement directions. While the preferred directions were mirror-symmetrical in both arms, they were attributed to a tendency specific for the dominant arm to simplify control of interaction torque by actively accelerating one joint and producing largely passive motion at the other joint. No conclusive evidence has been obtained in support of muscle effort minimization as a contributing factor to the directional preferences. Here, we tested whether distal load changes directional preferences, making the influence of muscle effort minimization on the selection of movement direction more apparent.MethodsThe free-stroke drawing task was performed by the dominant and non-dominant arm with no load and with 0.454 kg load at the wrist. Motion of each arm was limited to rotation of the shoulder and elbow in the horizontal plane. Directional histograms of strokes produced by the fingertip were calculated to assess directional preferences in each arm and load condition. Possible causes for directional preferences were further investigatedby studying optimization across directions of a number of cost functions.ResultsPreferences in both arms to move in the diagonal directions were revealed. The previously suggested tendency to actively accelerate one joint and produce passive motion at the other joint was supported in both arms and load conditions. However, the load increased the tendency to produce strokes in the transverse diagonal directions (perpendicular to the forearm orientation) in both arms. Increases in required muscle effort caused by the load suggested that the higher frequency of movements in the transverse directions represented increased influence of muscle effort minimization on the selection of movement direction. This interpretation was supported by cost function optimization results.ConclusionsWhile without load, the contribution of muscle effort minimization was minor, and therefore, not apparent, the load revealed this contribution by enhancing it. Unlike control of interaction torque, the revealed tendency to minimize muscle effort was independent of arm dominance.

[1]  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.

[2]  Philippe Lefèvre,et al.  Optimal integration of gravity in trajectory planning of vertical pointing movements. , 2009, Journal of neurophysiology.

[3]  Natalia Dounskaia,et al.  The internal model and the leading joint hypothesis: implications for control of multi-joint movements , 2005, Experimental Brain Research.

[4]  J. F. Soechting,et al.  Moving effortlessly in three dimensions: does Donders' law apply to arm movement? , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  P. Cisek,et al.  The influence of predicted arm biomechanics on decision making. , 2011, Journal of neurophysiology.

[6]  Francesco Nori,et al.  Evidence for Composite Cost Functions in Arm Movement Planning: An Inverse Optimal Control Approach , 2011, PLoS Comput. Biol..

[7]  Alexander Rm,et al.  A minimum energy cost hypothesis for human arm trajectories. , 1997 .

[8]  R. McN. Alexander,et al.  A minimum energy cost hypothesis for human arm trajectories , 1997, Biological Cybernetics.

[9]  Stephan P. Swinnen,et al.  Directional tuning effects during cyclical two-joint arm movements in the horizontal plane , 2001, Experimental Brain Research.

[10]  Vladimir M Zatsiorsky,et al.  Optimization-Based Models of Muscle Coordination , 2002, Exercise and sport sciences reviews.

[11]  N. A. Borghese,et al.  Time-varying mechanical behavior of multijointed arm in man. , 1993, Journal of neurophysiology.

[12]  David Zipser,et al.  Reaching to grasp with a multi-jointed arm. I. Computational model. , 2002, Journal of neurophysiology.

[13]  Sascha E. Engelbrecht,et al.  Minimum Principles in Motor Control. , 2001, Journal of mathematical psychology.

[14]  D J Ostry,et al.  Compensation for interaction torques during single- and multijoint limb movement. , 1999, Journal of neurophysiology.

[15]  M. Kawato,et al.  Formation and control of optimal trajectory in human multijoint arm movement , 1989, Biological Cybernetics.

[16]  Michael I. Jordan,et al.  Obstacle Avoidance and a Perturbation Sensitivity Model for Motor Planning , 1997, The Journal of Neuroscience.

[17]  C. Chandler,et al.  Computers, brains and the control of movement , 1982, Trends in Neurosciences.

[18]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[19]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.

[20]  H. Hatze,et al.  Energy-optimal controls in the mammalian neuromuscular system , 1977, Biological Cybernetics.

[21]  Michael C. Minnotte,et al.  Nonparametric testing of the existence of modes , 1997 .

[22]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[23]  D. W. Scott,et al.  The Mode Tree: A Tool for Visualization of Nonparametric Density Features , 1993 .

[24]  Natalia Dounskaia,et al.  The role of intrinsic factors in control of arm movement direction: implications from directional preferences. , 2011, Journal of neurophysiology.

[25]  Mark L. Nagurka,et al.  A Suboptimal Trajectory Planning Algorithm for Robotic Manipulators , 1988 .

[26]  E. Bizzi,et al.  Neural, mechanical, and geometric factors subserving arm posture in humans , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  H. Cruse Constraints for joint angle control of the human arm , 1986, Biological Cybernetics.

[28]  Raul Benitez,et al.  Motor adaptation as a greedy optimization of error and effort. , 2007, Journal of neurophysiology.

[29]  Amir Karniel,et al.  Minimum Acceleration Criterion with Constraints Implies Bang-Bang Control as an Underlying Principle for Optimal Trajectories of Arm Reaching Movements , 2008, Neural Computation.

[30]  G. F. Koshland,et al.  Selection of muscles for initiation of planar, three-joint arm movements with different final orientations of the hand , 2004, Experimental Brain Research.

[31]  James Gordon,et al.  Accuracy of planar reaching movements , 1994, Experimental Brain Research.

[32]  Emmanuel Guigon,et al.  Computational Motor Control : Redundancy and Invariance , 2007 .

[33]  Jeremy D Wong,et al.  The central nervous system does not minimize energy cost in arm movements. , 2010, Journal of neurophysiology.

[34]  G. E. Stelmach,et al.  Commonalities and differences in control of various drawing movements , 2002, Experimental Brain Research.

[35]  Natalia Dounskaia,et al.  Limitations on coupling of bimanual movements caused by arm dominance: when the muscle homology principle fails. , 2010, Journal of neurophysiology.

[36]  R. Sainburg Evidence for a dynamic-dominance hypothesis of handedness , 2001, Experimental Brain Research.

[37]  N. Dounskaia,et al.  Interlimb differences of directional biases for stroke production , 2011, Experimental Brain Research.

[38]  N. Dounskaia,et al.  The role of vision, speed, and attention in overcoming directional biases during arm movements , 2011, Experimental Brain Research.

[39]  A. Izenman,et al.  Philatelic Mixtures and Multimodal Densities , 1988 .

[40]  Neville Hogan,et al.  The mechanics of multi-joint posture and movement control , 1985, Biological Cybernetics.

[41]  Natalia V Dounskaia,et al.  Directional biases reveal utilization of arm's biomechanical properties for optimization of motor behavior. , 2007, Journal of neurophysiology.

[42]  D. Anton Occupational biomechanics , 1986 .

[43]  Michael I. Jordan,et al.  Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study , 1995, Experimental Brain Research.

[44]  Natalia Dounskaia,et al.  Control of Human Limb Movements: The Leading Joint Hypothesis and Its Practical Applications , 2010, Exercise and sport sciences reviews.

[45]  R. Sainburg,et al.  Differences in control of limb dynamics during dominant and nondominant arm reaching. , 2000, Journal of neurophysiology.

[46]  A. Bowman,et al.  Applied smoothing techniques for data analysis : the kernel approach with S-plus illustrations , 1999 .

[47]  W. L. Nelson Physical principles for economies of skilled movements , 1983, Biological Cybernetics.

[48]  Robert L Sainburg,et al.  Handedness: dominant arm advantages in control of limb dynamics. , 2002, Journal of neurophysiology.