Referent control and motor equivalence of reaching from standing.

Motor actions may result from central changes in the referent body configuration, defined as the body posture at which muscles begin to be activated or deactivated. The actual body configuration deviates from the referent configuration, particularly because of body inertia and environmental forces. Within these constraints, the system tends to minimize the difference between these configurations. For pointing movement, this strategy can be expressed as the tendency to minimize the difference between the referent trajectory (RT) and actual trajectory (QT) of the effector (hand). This process may underlie motor equivalent behavior that maintains the pointing trajectory regardless of the number of body segments involved. We tested the hypothesis that the minimization process is used to produce pointing in standing subjects. With eyes closed, 10 subjects reached from a standing position to a remembered target located beyond arm length. In randomly chosen trials, hip flexion was unexpectedly prevented, forcing subjects to take a step during pointing to prevent falling. The task was repeated when subjects were instructed to intentionally take a step during pointing. In most cases, reaching accuracy and trajectory curvature were preserved due to adaptive condition-specific changes in interjoint coordination. Results suggest that referent control and the minimization process associated with it may underlie motor equivalence in pointing. NEW & NOTEWORTHY Motor actions may result from minimization of the deflection of the actual body configuration from the centrally specified referent body configuration, in the limits of neuromuscular and environmental constraints. The minimization process may maintain reaching trajectory and accuracy regardless of the number of body segments involved (motor equivalence), as confirmed in this study of reaching from standing in young healthy individuals. Results suggest that the referent control process may underlie motor equivalence in reaching.

[1]  Anatol G. Feldman,et al.  Changes in the referent body location and configuration may underlie human gait, as confirmed by findings of multi-muscle activity minimizations and phase resetting , 2011, Experimental Brain Research.

[2]  D. Stuart,et al.  Integration of posture and movement: contributions of Sherrington, Hess, and Bernstein. , 2005, Human movement science.

[3]  A. G. Feldman,et al.  Control of wrist position and muscle relaxation by shifting spatial frames of reference for motoneuronal recruitment: possible involvement of corticospinal pathways , 2010, The Journal of physiology.

[4]  A. G. Feldman,et al.  Recent Tests of the Equilibrium-Point Hypothesis (λ Model) , 1998 .

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

[6]  J. Lackner,et al.  Motor adaptation to Coriolis force perturbations of reaching movements: endpoint but not trajectory adaptation transfers to the nonexposed arm. , 1995, Journal of neurophysiology.

[7]  E. Bizzi,et al.  Arm trajectory formation in monkeys , 2004, Experimental Brain Research.

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

[9]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[10]  Reza Shadmehr,et al.  Internal models of limb dynamics and the encoding of limb state , 2005, Journal of neural engineering.

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

[12]  Karl-Theodor Kalveram,et al.  Motor adaptation to different dynamic environments is facilitated by indicative context stimuli , 2004, Psychological research.

[13]  David A. Winter,et al.  Human balance and posture control during standing and walking , 1995 .

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

[15]  A. Straube,et al.  Under Threshold Position Control, Peripheral Mechanisms Compensate Efficiently for Small Perturbations of Arm Movements. , 2016, Motor control.

[16]  A. G. Feldman,et al.  Implicit learning and generalization of stretch response modulation in humans. , 2016, Journal of neurophysiology.

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

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

[19]  Gregor Schöner,et al.  Motor equivalence during multi-finger accurate force production , 2014, Experimental Brain Research.

[20]  J. Kalaska,et al.  Comparison of variability of initial kinematics and endpoints of reaching movements , 1999, Experimental Brain Research.

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

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

[23]  Anatol G. Feldman,et al.  Movement reorganization to compensate for fatigue during sawing , 2002, Experimental Brain Research.

[24]  M. Latash,et al.  Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. , 2011, Journal of neurophysiology.

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

[26]  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.

[27]  T. Flash,et al.  Moving gracefully: quantitative theories of motor coordination , 1987, Trends in Neurosciences.

[28]  Charles Capaday,et al.  The effects of baclofen on the stretch reflex parameters of the cat , 2004, Experimental Brain Research.

[29]  E. Holst Relations between the central Nervous System and the peripheral organs , 1954 .

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

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

[32]  A. G. Feldman,et al.  Arm–Trunk Coordination for Beyond-the-Reach Movements in Adults With Stroke , 2014, Neurorehabilitation and neural repair.

[33]  D J Ostry,et al.  Are complex control signals required for human arm movement? , 1998, Journal of neurophysiology.

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

[35]  S Ma,et al.  Two functionally different synergies during arm reaching movements involving the trunk. , 1995, Journal of neurophysiology.

[36]  T. R. Kaminski,et al.  The effects of stance configuration and target distance on reaching , 2000, Experimental Brain Research.

[37]  A. G. Feldman,et al.  Arm-trunk coordination as a measure of vestibulospinal efficiency. , 2013, Journal of vestibular research : equilibrium & orientation.

[38]  A.D. Kuo,et al.  An optimal control model for analyzing human postural balance , 1995, IEEE Transactions on Biomedical Engineering.

[39]  A. G. Feldman,et al.  Multi-muscle control of head movements in monkeys: the referent configuration hypothesis , 2000, Neuroscience Letters.

[40]  V M Zatsiorsky,et al.  Rambling and trembling in quiet standing. , 2000, Motor control.

[41]  T. Olsen,et al.  The Obesity Paradox in Stroke: Lower Mortality and Lower Risk of Readmission for Recurrent Stroke in Obese Stroke Patients , 2015, International journal of stroke : official journal of the International Stroke Society.

[42]  Mark L. Latash,et al.  The role of kinematic redundancy in adaptation of reaching , 2006, Experimental Brain Research.

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

[44]  María Herrojo Ruiz,et al.  Detecting wrong notes in advance: neuronal correlates of error monitoring in pianists. , 2009, Cerebral cortex.

[45]  J A Kelso,et al.  Analysis of "invariant characteristics" in the motor control of down's syndrome and normal subjects. , 1982, Journal of motor behavior.

[46]  C. Atkeson,et al.  Kinematic features of unrestrained vertical arm movements , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  Anatol G. Feldman,et al.  Referent control of action and perception , 2015, Springer New York.

[49]  G. E. Stelmach,et al.  Prehension with trunk assisted reaching , 1996, Behavioural Brain Research.

[50]  R. Rosen Optimality Principles in Biology , 1967, Springer US.

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

[52]  P. Pigeon,et al.  Recruitment and sequencing of different degrees of freedom during pointing movements involving the trunk in healthy and hemiparetic subjects , 1999, Experimental Brain Research.

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

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

[55]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

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

[57]  J. Hollerbach Computers, brains and the control of movement , 1982, Trends in Neurosciences.

[58]  A. G. Feldman,et al.  Threshold control of motor actions prevents destabilizing effects of proprioceptive delays , 2006, Experimental Brain Research.

[59]  A. G. Feldman Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .