Artificial Gravity Reveals that Economy of Action Determines the Stability of Sensorimotor Coordination

Background When we move along in time with a piece of music, we synchronise the downward phase of our gesture with the beat. While it is easy to demonstrate this tendency, there is considerable debate as to its neural origins. It may have a structural basis, whereby the gravitational field acts as an orientation reference that biases the formulation of motor commands. Alternatively, it may be functional, and related to the economy with which motion assisted by gravity can be generated by the motor system. Methodology/Principal Findings We used a robotic system to generate a mathematical model of the gravitational forces acting upon the hand, and then to reverse the effect of gravity, and invert the weight of the limb. In these circumstances, patterns of coordination in which the upward phase of rhythmic hand movements coincided with the beat of a metronome were more stable than those in which downward movements were made on the beat. When a normal gravitational force was present, movements made down-on-the-beat were more stable than those made up-on-the-beat. Conclusions/Significance The ubiquitous tendency to make a downward movement on a musical beat arises not from the perception of gravity, but as a result of the economy of action that derives from its exploitation.

[1]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[2]  H. Zelaznik,et al.  Motor-output variability: a theory for the accuracy of rapid motor acts. , 1979, Psychological review.

[3]  J. Kelso Phase transitions and critical behavior in human bimanual coordination. , 1984, The American journal of physiology.

[4]  Rudolf Arnheim Perceptual Dynamics in Musical Expression , 1984 .

[5]  D. Humphrey Representation of movements and muscles within the primate precentral motor cortex: historical and current perspectives. , 1986, Federation proceedings.

[6]  R. Lemon The output map of the primate motor cortex , 1988, Trends in Neurosciences.

[7]  P A Bandettini,et al.  Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. , 1994, Brain research. Cognitive brain research.

[8]  Richard G. Carson,et al.  Expressions of asymmetries and anchoring in bimanual coordination , 1994 .

[9]  C. Svarer,et al.  Rate Dependence of Regional Cerebral Activation during Performance of a Repetitive Motor Task: A PET Study , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[10]  G. Schlaug,et al.  Cerebral activation covaries with movement rate , 1996, Neuroreport.

[11]  W. Prinz Perception and Action Planning , 1997 .

[12]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement velocity: a PET study. , 1998, Journal of neurophysiology.

[13]  Daniel M. Wolpert,et al.  Signal-dependent noise determines motor planning , 1998, Nature.

[14]  Marion A. Eppler,et al.  Development of Visually Guided Locomotion , 1998 .

[15]  David N. Lee Guiding Movement by Coupling Taus , 1998 .

[16]  Alain Berthoz,et al.  The sensorimotor and cognitive integration of gravity , 1998, Brain Research Reviews.

[17]  S. Riek,et al.  The influence of joint position on the dynamics of perception-action coupling , 1998, Experimental Brain Research.

[18]  R Chua,et al.  Changes in posture alter the attentional demands of voluntary movement , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[20]  A. Fuchs,et al.  Event‐related changes in neuromagnetic activity associated with syncopation and synchronization timing tasks , 2001, Human brain mapping.

[21]  W. Prinz,et al.  Perceptual basis of bimanual coordination , 2001, Nature.

[22]  F. Lacquaniti,et al.  Does the brain model Newton's laws? , 2001, Nature Neuroscience.

[23]  R. Carson,et al.  Resistance training enhances the stability of sensorimotor coordination , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  Charles Capaday,et al.  Neural mechanisms involved in the functional linking of motor cortical points , 2002, Experimental Brain Research.

[25]  S. Riek The effects of viscous loading of the human forearm flexors on the stability of coordination. , 2004, Human movement science.

[26]  C. Elger,et al.  Transcranial magnetic stimulation: specific and non-specific facilitation of magnetic motor evoked potentials , 1990, Journal of Neurology.

[27]  Richard G. Carson,et al.  Neuromuscular-skeletal constraints upon the dynamics of perception-action coupling , 2004, Experimental Brain Research.

[28]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Richard G Carson,et al.  Changes in muscle coordination with training. , 2006, Journal of applied physiology.

[30]  C. Papaxanthis,et al.  Motor planning of arm movements is direction-dependent in the gravity field , 2007, Neuroscience.

[31]  J. A. Scott Kelso,et al.  Coordination Dynamics of Large-scale Neural Circuitry Underlying Rhythmic Sensorimotor Behavior , 2009, Journal of Cognitive Neuroscience.