Neurophysiological and Dynamical Control Principles Underlying Variable and Stereotyped Movement Patterns During Motor Skill Acquisition
Kazutoshi Kudo*1, Makoto Miyazaki*2, Hirofumi Sekiguchi*3,
Hiroshi Kadota*4, Shinya Fujii*4,*5, Akito Miura*1,*5,
Michiko Yoshie*1,*5,*6, and Hiroki Nakata*7
*1Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan
*2Research Institute of Kochi University of Technology, 185 Miyanokuchi, Tosayamada, Kochi 782-8502, Japan
*3Faculty of Business and Information Sciences, Jobu University
*4Division of Physical and Health Education, Graduate School of Education, The University of Tokyo
*5Japan Society for the Promotion of Science
*6Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex
*7Faculty of Sport Sciences, Waseda University
While novices who are unfamiliar to a new motor skill typically show variable and unstable movements, highly skilled experts show a stable and accurate performance. These distinct differences in motor control between experts and novices have led researchers to hypothesize that neuromotor noise is reduced in the process of motor skill acquisition. On the other hand, it should be noted that novices’ movements have other characteristics; they are habituated and stereotyped. In this review, we discuss the principles governing spatiotemporal organization of movements in novices and experts while solving specific motor problems under varied conditions, by introducing experimental and theoretical studies that use neurophysiological techniques such as electromyography, functional magnetic resonance imaging, and transcranial magnetic stimulation, and mathematical models such as stochastic and dynamical models. On the basis of the findings from a variety of perceptual-motor skills (e.g., ballthrowing, badminton smash, long-distance running, piano and drum performance, street dance, a popular hand game of rock-paper-scissors, and temporal order judgement task), we argue that the novices’ characteristic movement patterns were organized under specific constraints and typical strategy, without which the variability would increase even more, while experts’ movements were organized with functional and compensatory variability that can drive out erroneous noise variability. We also showed that in a particular type of interlimb coordination, skilled and unskilled movement patterns could be seamlessly described as the time evolution of nonlinear and self-organized dynamical systems, suggesting that the dynamical systems approach is a major candidate for understanding the principle underlying organization of experts’ and novices’ movements.
Hiroshi Kadota, Shinya Fujii, Akito Miura,
Michiko Yoshie, and Hiroki Nakata, “Neurophysiological and Dynamical Control Principles Underlying Variable and Stereotyped Movement Patterns During Motor Skill Acquisition,” J. Adv. Comput. Intell. Intell. Inform., Vol.15, No.8, pp. 942-953, 2011.
-  R. A. Schmidt, H. Zelaznik, B. Hawkins et al., “Motor Output Variability: Theory for the Accuracy of Rapid Motor Acts,” Psychological Review, Vol.86, pp. 415-451, 1979.
-  A. T. Welford, “Fundamentals of Skill,” Methuen, 1968.
-  N. A. Bernstein, “On Dexterity and its Development,” in M. L. Latash and M. T. Turvey, “Dexterity and its development,” Lawrence Erlbaum, pp. 1-244, 1996.
-  A. Miura, K. Kudo, T. Ohtsuki et al., “Coordination Modes in Sensorimotor Synchronization of Whole-Body Movement: A Study of Street Dancers and Non-Dancers,” Human Movement Science (in press).
-  J. A. S. Kelso, “Dynamic Patterns,” MIT Press, 1995.
-  K. M. Newell and D. M. Corcos, “Variability and Motor Control,” Human Kinetics, 1993.
-  S. Sakurai and T. Ohtsuki, “Muscle Activity and Accuracy of Performance of the Smash Stroke in Badminton with Reference to Skill and Practice,” J. of Sports Sciences, Vol.18, pp. 901-914, 2000.
-  Y. Nakayama, K. Kudo, and T. Ohtsuki, “Variability and Fluctuation in Running Gait Cycle of Trained Runners and Non-Runners,” Gait & Posture, Vol.31, pp. 331-335, 2010.
-  S. Fujii, K. Kudo, T. Ohtsuki et al., “Tapping Performance and Underlying Wrist Muscle Activity of Non-Drummers, Drummers, and the World’s Fastest Drummer,” Neuroscience Letters, Vol.459, pp. 69-73, 2009.
-  S. Fujii, K. Kudo, M. Shinya et al., “Wrist Muscle Activity During Rapid Unimanual Tapping with a Drumstick in Drummers and Non-Drummers,” Motor Control, Vol.13, pp. 237-250, 2009.
-  A. P. Georgopoulos, J. F. Kalaska, and J. T. Massey, “Spatial Trajectories and Reaction Times of Aimed Movements: Effects of Practice, Uncertainty and Change of Target Location,” J. of Neurophysiology, Vol.46, pp. 725-743, 1981.
-  I. M. Franks and R. B.Wilberg, “The Generation of Movement Patterns During the Acquisition of a Pursuit Tracking Task,” Human Movement Science, Vol.1, pp. 251-272, 1982.
-  T. A. Salthouse, “Effects of Practice on a Typing-Like Keying Task,” Acta Psychologica, Vol.62, pp. 189-198, 1986.
-  B. Vereijken, R. E. A. Vanemmerik, H. T. A. Whiting et al., “Free(z)ing Degrees of Freedom in Skill Acquisition,” J. of Motor Behavior, Vol.24, pp. 133-142, 1992.
-  K. Kudo, T. Ito, S. Tsutsui et al., “Compensatory Coordination of Release Parameters in a Throwing Task,” J. of Motor Behavior, Vol.32, pp. 337-345, 2000.
-  S. Furuya and H. Kinoshita, “Organization of the Upper Limb Movement for Piano Key-Depression Differs Between Expert Pianists and Novice Players,” Experimental Brain Research, Vol.185, pp. 581-593, 2008.
-  R. Osu, D. W. Franklin, H. Kato et al., “Short- and Long-Term Changes in Joint Co-Contraction Associated with Motor Learning as Revealed from Surface EMG,” J. of Neurophysiology, Vol.88, pp. 991-1004, 2002.
-  H. Heuer, “Control of the Dominant and Nondominant Hand: Exploitation and Taming of Nonmuscular Forces,” Experimental Brain Research, Vol.178, pp. 363-373, 2007.
-  G. P. Van Galen, M. Muller, R. G. J. Meulenbroek et al., “Forearm EMG Response Activity During Motor Performance in Individuals Prone to Increased Stress Reactivity,” American J. of Industrial Medicine, Vol.41, pp. 406-419, 2002.
-  M. Yoshie, K. Kudo, and T. Ohtsuki, “Effects of Psychological Stress on State Anxiety, Electromyographic Activity, and Arpeggio Performance in Pianists,” Medical Problems of Performing Artists, Vol.23, pp. 120-132, 2008.
-  P. L. Gribble, L. I. Mullin, N. Cothros et al., “Role of Cocontraction in Arm Movement Accuracy,” J. of Neurophysiology, Vol.89, pp. 2396-2405, 2003.
-  M. Yoshie, K. Kudo, T. Murakoshi et al., “Music Performance Anxiety in Skilled Pianists: Effects of Social-Evaluative Performance Situation on Subjective, Autonomic, and Electromyographic Reactions,” Experimental Brain Research, Vol.199, pp. 117-126, 2009.
-  M. Yoshie, K. Kudo, and T. Ohtsuki, “Motor/Autonomic Stress Responses in a Competitive Piano Performance,” Annals of the New York Academy of Sciences, Vol.1169, pp. 368-371, 2009.
-  J. R. Pijpers, R. R. D. Oudejans, F. Holsheimer et al., “Anxiety-Performance Relationships in Climbing: A Process-Oriented Approach,” Psychology of Sport and Exercise, Vol.4, pp. 283-304, 2003.
-  G. Hajcak, C.Molnar, M. S. George et al., “Emotion Facilitates Action: A Transcranial Magnetic Stimulation Study of Motor Cortex Excitability During Picture Viewing,” Psychophysiology, Vol.44, pp. 91-97, 2007.
-  T. Baumgartner, M. Willi, and L. Jäncke, “Modulation of Corticospinal Activity by Strong Emotions Evoked by Pictures and Classical Music: A Transcranial Magnetic Stimulation Study,” Neuroreport, Vol.18, pp. 261-265, 2007.
-  D. Schutter, D. Hofman, and J. Van Honk, “Fearful Faces Selectively Increase Corticospinal Motor Tract Excitability: A Transcranial Magnetic Stimulation Study,” Psychophysiology, Vol.45, pp. 345-348, 2008.
-  N. A. Bernstein, “The Co-ordination and Regulation ofMovement,” Pergamon Press, 1967.
-  K. Kudo and T. Ohtsuki, “Adaptive Variability in Skilled Human Movements,” Information and Media Technologies, Vol.3, pp. 409-420, 2008.
-  E. Todorov and M. I. Jordan, “Optimal Feedback Control as a Theory of Motor Coordination,” Nature Neuroscience, Vol.5, pp. 1226-1235, 2002.
-  J. P. Scholz and G. Schoner, “The Uncontrolled Manifold Concept: Identifying Control Variables for a Functional Task,” Experimental Brain Research, Vol.126, pp. 289-306, 1999.
-  M. L. Latash, J. P. Scholz, and G. Schoner, “Toward a New Theory of Motor Synergies,” Motor Control, Vol.11, pp. 276-308, 2007.
-  M. L. Latash, Z. M. Li, and V. M. Zatsiorsky, “A Principle of Error Compensation Studied Within a Task of Force Production by a Redundant Set of Fingers,” Experimental Brain Research, Vol.122, pp. 131-138, 1998.
-  G. A. Arutyunyan, V. S. Gurfinkel, and M. L. Mirskii, “Organization ofMovements on Execution byMan of an Exact Postural Task,” Biophysics, Vol.14, pp. 1162-1167, 1969.
-  K. P. Kording, S. P. Ku, and D. M. Wolpert, “Bayesian Integration in Force Estimation,” J. of Neurophysiology, Vol.92, pp. 3161-3165, 2004.
-  K. P. Kording and D. M. Wolpert, “Bayesian Decision Theory in Sensorimotor Control,” Trends in Cognitive Sciences, Vol.10, pp. 319-326, 2006.
-  D.M.Wolpert, “Probabilistic Models in Human Sensorimotor Control,” Human Movement Science, Vol.26, pp. 511-524, 2007.
-  D. Kersten, P. Mamassian, and A. Yuille, “Object Perception as Bayesian Inference,” Annual Review of Psychology, Vol.55, pp. 271-304, 2004.
-  D. C. Knill and A. Pouget, “The Bayesian Brain: the Role of Uncertainty in Neural Coding and Computation,” Trends in Neuroscience, Vol.27, pp. 712-719, 2004.
-  K. P. Kording and D. M. Wolpert, “Bayesian Integration in Sensorimotor Learning,” Nature, Vol.427, pp. 244-247, 2004.
-  H. Tassinari, T. E. Hudson, andM. S. Landy, “Combining Priors and Noisy Visual Cues in a Rapid Pointing Task,” J. of Neuroscience, Vol.26, 10154-63, 2006.
-  M. Jazayeri and M. N. Shadlen, “Temporal Context Calibrates Interval Timing,” Nature Neuroscience, Vol.13, pp. 1020-1026, 2010.
-  J. Lopez-Moliner, D. T. Field, and J. P.Wann, “Interceptive Timing: Prior Knowledge Matters,” J. of Vision, Vol.7, No.11, pp. 1-8, 2007.
-  M.Miyazaki, D. Nozaki, and Y. Nakajima, “Testing Bayesian Models of Human Coincidence Timing,” J. of Neurophysiology, Vol.94, pp. 395-399, 2005.
-  M. Miyazaki, S. Yamamoto, S. Uchida et al., “Bayesian Calibration of Simultaneity in Tactile Temporal Order Judgment,” Nature Neuroscience, Vol.9, pp. 875-877, 2006.
-  H. Nakata, K. Inui, Y. Nishihira et al., “Effects of a Go/NoGo Task on Event-Related Potentials Following Somatosensory Stimulation,” Clinical Neurophysiology, Vol.115, pp. 361-368, 2004.
-  H. Nakata, K. Inui, T.Wasaka et al., “Somato-Motor Inhibitory Processing in Humans: a Study with MEG and ERP,” European J. of Neuroscience, Vol.22, pp. 1784-1792, 2005.
-  R. Simson, H. G. Vaughan, and W. Ritter, “Scalp Topography of Potentials in Auditory and Visual-Discrimination Tasks,” Electroencephalography and Clinical Neurophysiology, Vol.42, pp. 528-535, 1977.
-  K. Kudo and T. Ohtsuki, “Functional Modification of Agonist-Antagonist Electromyographic Activity for Rapid Movement Inhibition,” Experimental Brain Research, Vol.122, pp. 23-30, 1998.
-  A. R. Aron, P. C. Fletcher, T. Bullmore et al., “Stop-Signal Inhibition Disrupted by Damage to Right Inferior Frontal Gyrus in Humans,” Nature Neuroscience, Vol.6, pp. 115-116, 2003.
-  G. D. Logan and W. B. Cowan, “On the Ability to Inhibit Thought and Action: A Theory of an Act of Control,” Psychological Review, Vol.91, pp. 295-327, 1984.
-  J. Chikazoe, S. Konishi, T. Asari et al., “Activation of Right Inferior Frontal Gyrus During Response Inhibition Across Response Modalities,” J. of Cognitive Neuroscience, Vol.19, pp. 69-80, 2007.
-  H. Nakata, K. Sakamoto, A. Ferretti et al., “Somato-Motor Inhibitory Processing in Humans: an Event-Related Functional MRI Study,” Neuroimage, Vol.39, pp. 1858-1866, 2008.
-  N. Kida, S. Oda, and M. Matsumura, “Intensive Baseball Practice Improves the Go/NoGo Reaction Time, but not the Simple Reaction Time,” Cognitive Brain Research, Vol.22, pp. 257-264, 2005.
-  H. Nakamoto and S. Mori, “Effects of Stimulus-Response Compatibility in Mediating Expert Performance in Baseball Players,” Brain research, Vol.1189, pp. 179-188, 2008.
-  F. Di Russo, F. Taddei, T. Apnile et al., “Neural Correlates of Fast Stimulus Discrimination and Response Selection in Top-Level Fencers,” Neuroscience Letters, Vol.408, pp. 113-118, 2006.
-  H. Kadota, Y. Nakajima, M. Miyazaki et al., “Anterior Prefrontal Cortex Activities During the Inhibition of Stereotyped Responses in a Neuropsychological Rock-Paper-Scissors Task,” Neuroscience Letters, Vol.453, pp. 1-5, 2009.
-  H. Kadota, H. Sekiguchi, S. Takeuchi et al., “The Role of the Dorsolateral Prefrontal Cortex in the Inhibition of Stereotyped Responses” Experimental Brain Research, Vol.203, pp. 593-600, 2010.
-  H. Kashima and M. Kato, “Tests for Frontal Function-Pattern of Frontal Dysfunction and its Assessment,” Shinkei Kenkyu no Shinpo, Vol.37, pp. 93-110, 1993.
-  M. Matsubara, S. Yamaguchi, J. Xu et al., “Neural Correlates for the Suppression of Habitual Behavior: a Functional MRI Study,” J. of Cognitive Neuroscience, Vol.16, pp. 944-954, 2004.
-  K. Kudo, M. Miyazaki, T. Kimura et al., “Selective Activation and Deactivation of the Human Brain Structures Between Speeded and Precisely Timed Tapping Responses to Identical Visual Stimulus: an fMRI Study,” Neuroimage, Vol.22, pp. 1291-1301, 2004.
-  K. A. Ericsson, R. T. Krampe, and C. Teschromer, “The Role of Deliberate Practice in the Acquisition of Expert Performance,” Psychological Review, Vol.100, pp. 363-406, 1993.
-  P. M. Fitts and M. I. Posner, “Human Performance,” Brooks Cole, 1967.
-  H. Haken, “Synergetics, an Introduction: Non-Equilibrium Phase Transitions and Self-Organization in Physics, Chemistry and Biology,” Springer, 1977.
-  S. Fujii, K. Kudo, T. Ohtsuki et al., “Intrinsic Constraint of Asymmetry Acting as a Control Parameter on Rapid, Rhythmic Bimanual Coordination: A Study of Professional Drummers and Non-Drummers,” J. of Neurophysiology, Vol.104, pp. 2178-2186, 2010.
-  H. Haken, J. A. S. Kelso, and H. Bunz, “A Theoretical Model of Phase Transitions in Human Hand Movements,” Biological Cybernetics, Vol.51, pp. 347-356, 1985.
-  G. Schöner, H. Haken, and J. A. S. Kelso, “A Stochastic Theory of Phase Transitions in Human Hand Movement,” Biological Cybernetics, Vol.53, pp. 247-257, 1986.
-  J. Scholz and J. A. S. Kelso, “Intentional Switching Between Patterns of Bimanual Coordination Depends on the Intrinsic Dynamics of the Patterns,” J. of Motor Behavior, Vol.22, pp. 98-124, 1990.
-  J. A. S. Kelso, J. P. Scholz, and G. Schöner, “Dynamics Governs Switching Among Patterns of Coordination in Biological Movement,” Physics Letter A, Vol.134, pp. 8-12, 1988.
-  H. J. de Poel, C. L. Peper, and P. J. Beek, “Laterally Focused Attention Modulates Asymmetric Coupling in Rhythmic Interlimb Coordination,” Psychological Research, 2006.
-  E. L. Amazeen, P. G. Amazeen, P. J. Treffner et al., “Attention and Handedness in Bimanual Coordination Dynamics,” J. of Experimental Psychology: Human Perception and Performance, Vol.23, pp. 1552-1560, 1997.
-  J. J. Jeka and J. A. S. Kelso, “Manipulating Symmetry in the Coordination Dynamics of Human Movement,” J. of Experimental Psychology: Human Perception and Performance, Vol.21, pp. 360-374, 1995.
-  S. H. Strogatz, “Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering,” Perseus Books, 1994.
-  K. Kudo, H. Park, B. A. Kay et al., “Environmental Coupling Modulates the Attractors of Rhythmic Coordination,” J. of Experimental Psychology: Human Perception and Performance, Vol.32, pp. 599-609, 2006.
-  K. Ohgane, S. Ei, K. Kudo et al., “Emergence of Adaptability to Time Delay in Bipedal Locomotion,” Biological Cybernetics, Vol.90, pp. 125-132, 2004.
-  T. F. Munte, E. Altenmuller, and L. Jancke, “The Musician’s Brain as a Model of Neuroplasticity,” Nature Reviews Neuroscience, Vol.3, pp. 473-478, 2002.
-  S. L. Bengtsson, Z. Nagy, S. Skare et al., “Extensive Piano Practicing Has Regionally Specific Effects onWhiteMatter Development,” Nature Neuroscience, Vol.8, pp. 1148-1150, 2005.
-  H. Nakata, M. Yoshie, A. Miura et al., “Characteristics of the Athletes’ Brain: Evidence from Neurophysiology and Neuroimaging,” Brain Research Reviews, Vol.62, pp. 197-211, 2010.
-  W. Fujisaki, S. Shimojo, M. Kashino et al., “Recalibration of Audiovisual Simultaneity,” Nature Neuroscience, Vol.7, pp. 773-778, 2004.
-  J. V. Hanson, J. Heron, and D. Whitaker, “Recalibration of Perceived Time Across Sensory Modalities,” Experimental Brain Research, Vol.185, pp. 347-352, 2008.
-  J. Vroomen, M. Keetels, B. de Gelder et al., “Recalibration of Temporal Order Perception by Exposure to Audio-Visual Asynchrony,” Cognitive Brain Research, Vol.22, pp. 32-35, 2004.
-  D. H. Arnold and K. Yarrow, “Temporal Recalibration of Vision,” Proc. of the Royal Society B: Biological sciences, Vol.278, pp. 535-538, 2011.
-  Y. Sato, T. Toyoizumi, and K. Aihara, “Bayesian Inference Explains Perception of Unity and Ventriloquism Aftereffect: Identification of Common Sources of Audiovisual Stimuli,” Neural Computation, Vol.19, pp. 3335-3355, 2007.
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