Cue-induced changes in the stability of finger force-production tasks revealed by the uncontrolled manifold analysis.

A motor system configured to maximize the stability of its current state cannot dexterously transition between states. Yet, we routinely resolve the stability-dexterity conflict and rapidly change our current behavior without allowing it to become unstable before the desired transition. The phenomenon called anticipatory synergy adjustment (ASA) partly describes how the central nervous system handles this conflict. ASA is a continuous decrease in the stability of the current motor state beginning 150-400 ms before a rapid state transition accomplished using redundant sets of motor inputs (more input variables than task-specific output variables). So far, ASAs have been observed only when the timing of the upcoming transition is known. We utilized a multifinger, isometric force-production task to demonstrate that compared with a condition where no state transition is expected, the stability of the current state is lower by ~12% when a participant is cued to make a transition, even when the nature and timing of that transition are unknown. This result (stage 1 ASA) is distinct from its traditional version (stage 2 ASA), and it describes early destabilization that occurs solely in response to the expectation to move. Stage 2 ASA occurs later, only if the timing of the transition is known sufficiently in advance. Stage 1 ASA lasts much longer (~1.5 s) and may scale in response to the perceived difficulty of the upcoming task. Therefore, this work reveals a much refined view of the processes that underlie the resolution of the stability-dexterity conflict. NEW & NOTEWORTHY We compared the stability of multifinger, isometric force-production tasks for trials in which force changes of unknown direction and timing were expected with trials in which there was no expectation of any force change. Mere expectation of a change caused the stability of the current motor state to drop. This novel result provides a much refined view of the processes that facilitate dexterous switching between motor states.

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

[2]  M. Latash,et al.  Anticipatory synergy adjustments: preparing a quick action in an unknown direction , 2013, Experimental Brain Research.

[3]  Z Hasan,et al.  The Human Motor Control System's Response to Mechanical Perturbation: Should It, Can It and Does It Ensure Stability? , 2005, Journal of motor behavior.

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

[5]  M. Maier,et al.  Upper Limb Outcome Measures Used in Stroke Rehabilitation Studies: A Systematic Literature Review , 2016, PloS one.

[6]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

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

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

[9]  Geert J. M. van Boxtel,et al.  Negative Slow Waves as Indices of Anticipation: The Bereitschaftspotential, the Contingent Negative Variation, and the Stimulus-Preceding Negativity , 2011 .

[10]  D. Nenchev Restricted Jacobian Matrices of Redundant Manipulators in Constrained Motion Tasks , 1992 .

[11]  M. Turvey,et al.  Variability and Determinism in Motor Behavior , 2002, Journal of motor behavior.

[12]  C. Brunia,et al.  Waiting in readiness: gating in attention and motor preparation. , 1993, Psychophysiology.

[13]  C D Marsden,et al.  Simple and choice reaction time and the use of advance information for motor preparation in Parkinson's disease. , 1992, Brain : a journal of neurology.

[14]  M. Latash,et al.  Stability of vertical posture explored with unexpected mechanical perturbations: synergy indices and motor equivalence , 2018, Experimental Brain Research.

[15]  Dagmar Sternad,et al.  Motor learning: changes in the structure of variability in a redundant task. , 2009, Advances in experimental medicine and biology.

[16]  Vladimir M. Zatsiorsky,et al.  Adjustments of prehension synergies in response to self-triggered and experimenter-triggered load and torque perturbations , 2006, Experimental Brain Research.

[17]  Christopher A. Zirker,et al.  Angular momentum synergies during walking , 2009, Experimental Brain Research.

[18]  Mark L. Latash,et al.  The bliss (not the problem) of motor abundance (not redundancy) , 2012, Experimental Brain Research.

[19]  Xuemei Huang,et al.  Changes in Multidigit Synergies and Their Feed-Forward Adjustments in Multiple Sclerosis , 2017, Journal of motor behavior.

[20]  C. Brunia,et al.  Achilles tendon reflexes and surface EMG activity during anticipation of a significant event and preparation for a voluntary movement. , 1985, Journal of motor behavior.

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

[22]  Mark L Latash,et al.  Elderly show decreased adjustments of motor synergies in preparation to action. , 2007, Clinical biomechanics.

[23]  J. Kelso,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980, Journal of experimental psychology. General.

[24]  R. Emmerik,et al.  On Variability and Stability in Human Movement , 2000 .

[25]  M. Latash,et al.  Changes in multifinger interaction and coordination in Parkinson's disease. , 2012, Journal of neurophysiology.

[26]  W. Smith The Integrative Action of the Nervous System , 1907, Nature.

[27]  M. L. Latash,et al.  Neural control of movement stability: Lessons from studies of neurological patients , 2015, Neuroscience.

[28]  S. Studenski,et al.  Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed , 2005, Journal of NeuroEngineering and Rehabilitation.

[29]  G. Schöner,et al.  Motor equivalence and self-motion induced by different movement speeds , 2011, Experimental Brain Research.

[30]  John Peter Scholz,et al.  Does hand dominance affect the use of motor abundance when reaching to uncertain targets? , 2009, Human movement science.

[31]  G. J. Thomas The Co-ordination and Regulation of Movements , 1967 .

[32]  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.

[33]  Gregor Schöner,et al.  Redundancy, Self-Motion, and Motor Control , 2009, Neural Computation.

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

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

[36]  Dagmar Sternad,et al.  Stability and predictability in human control of complex objects. , 2018, Chaos.

[37]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[38]  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.

[39]  M. Latash,et al.  Two stages and three components of the postural preparation to action , 2011, Experimental Brain Research.

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

[41]  J. Brobeck The Integrative Action of the Nervous System , 1948, The Yale Journal of Biology and Medicine.

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

[43]  M. Latash,et al.  Challenging gait leads to stronger lower-limb kinematic synergies: The effects of walking within a more narrow pathway , 2015, Neuroscience Letters.

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

[45]  Sandra Maria Sbeghen Ferreira de Freitas,et al.  Effect of motor planning on use of motor abundance , 2007, Neuroscience Letters.

[46]  V. M. Zatsiorsky,et al.  Synergies in the space of control variables within the equilibrium-point hypothesis , 2016, Neuroscience.

[47]  M. Latash,et al.  An apparent contradiction: increasing variability to achieve greater precision? , 2013, Experimental Brain Research.

[48]  M. Latash,et al.  Motor equivalence (ME) during reaching: is ME observable at the muscle level? , 2013, Motor control.

[49]  Joel W. Burdick,et al.  On the inverse kinematics of redundant manipulators: characterization of the self-motion manifolds , 1989, Proceedings, 1989 International Conference on Robotics and Automation.

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

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

[52]  Mark L Latash,et al.  Equifinality and its violations in a redundant system: multifinger accurate force production. , 2013, Journal of neurophysiology.

[53]  Jonathan B. Dingwell,et al.  Do Humans Optimally Exploit Redundancy to Control Step Variability in Walking? , 2010, PLoS Comput. Biol..

[54]  F. Horak,et al.  Postural inflexibility in parkinsonian subjects , 1992, Journal of the Neurological Sciences.

[55]  Mark L Latash,et al.  Anticipatory synergy adjustments in preparation to self-triggered perturbations in elderly individuals. , 2008, Journal of applied biomechanics.

[56]  Keith E. Gordon,et al.  General and Specific Strategies Used to Facilitate Locomotor Maneuvers , 2015, PloS one.

[57]  Gregor Schöner,et al.  Use of the uncontrolled manifold (UCM) approach to understand motor variability, motor equivalence, and self-motion. , 2014, Advances in experimental medicine and biology.

[58]  Vladimir M. Zatsiorsky,et al.  Effects of muscle vibration on multi-finger interaction and coordination , 2013, Experimental Brain Research.

[59]  A. Prochazka Sensorimotor gain control: A basic strategy of motor systems? , 1989, Progress in Neurobiology.

[60]  G. Schöner,et al.  Motor equivalent control of the center of mass in response to support surface perturbations , 2007, Experimental Brain Research.

[61]  Michael S Landy,et al.  Motor control is decision-making , 2012, Current Opinion in Neurobiology.

[62]  M. Latash,et al.  Two aspects of feedforward postural control: anticipatory postural adjustments and anticipatory synergy adjustments. , 2011, Journal of neurophysiology.

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

[64]  Shunta Togo,et al.  Anticipatory synergy adjustments reflect individual performance of feedforward force control , 2016, Neuroscience Letters.

[65]  M. Latash,et al.  Anticipatory postural adjustments and anticipatory synergy adjustments: preparing to a postural perturbation with predictable and unpredictable direction , 2017, Experimental Brain Research.

[66]  S. Debener,et al.  Simultaneous recording of EEG and BOLD responses: a historical perspective. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[67]  M. Latash,et al.  Task-specific stability of abundant systems: Structure of variance and motor equivalence , 2015, Neuroscience.

[68]  P. J. Foley The foreperiod and simple reaction time. , 1959, Canadian journal of psychology.

[69]  M. Latash,et al.  Preparation to a quick whole-body action: control with referent body orientation and multi-muscle synergies , 2019, Experimental Brain Research.

[70]  Anatol G Feldman,et al.  Space and time in the context of equilibrium-point theory. , 2011, Wiley interdisciplinary reviews. Cognitive science.

[71]  T. Stoffregen,et al.  Affordances as constraints on the control of stance , 1988 .

[72]  S. Ambike,et al.  Expectation of movement generates contrasting changes in multifinger synergies in young and older adults , 2018, Experimental Brain Research.

[73]  Michael Pauen,et al.  Analysis of a choice-reaction task yields a new interpretation of Libet's experiments. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[74]  G. Myer,et al.  Training the Antifragile Athlete: A Preliminary Analysis of Neuromuscular Training Effects on Muscle Activation Dynamics. , 2015, Nonlinear dynamics, psychology, and life sciences.