Rapid visuomotor feedback gains are tuned to the task dynamics

Here, we test whether rapid visuomotor feedback responses are selectively tuned to the task dynamics. The responses do not exhibit gain scaling, but they do vary with the level and stability of task dynamics. Moreover, these feedback gains are independently tuned to perturbations to the left and right, depending on these dynamics. Our results demonstrate that the sensorimotor control system regulates the feedback gain as part of the adaptation process, tuning them appropriately to the environment.

[1]  E. Henneman Relation between size of neurons and their susceptibility to discharge. , 1957, Science.

[2]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[3]  R. Stein,et al.  The relation between the surface electromyogram and muscular force. , 1975, The Journal of physiology.

[4]  C. Marsden,et al.  Servo action in the human thumb. , 1976, The Journal of physiology.

[5]  W. Tatton,et al.  Dependence of EMG Responses Evoked by Imposed Wrist Displacements on Pre-existing Activity in the Stretched Muscles , 1984, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[6]  C. Prablanc,et al.  Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement , 1986, Nature.

[7]  P. Matthews Observations on the automatic compensation of reflex gain on varying the pre‐existing level of motor discharge in man. , 1986, The Journal of physiology.

[8]  R. B. Stein,et al.  A method for simulating the reflex output of a motoneuron pool , 1987, Journal of Neuroscience Methods.

[9]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  J. Lackner,et al.  Rapid adaptation to Coriolis force perturbations of arm trajectory. , 1994, Journal of neurophysiology.

[11]  D. J. Bennett Stretch reflex responses in the human elbow joint during a voluntary movement. , 1994, The Journal of physiology.

[12]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[13]  E. Brenner,et al.  Fast Responses of the Human Hand to Changes in Target Position. , 1997, Journal of motor behavior.

[14]  F. Mussa-Ivaldi,et al.  The motor system does not learn the dynamics of the arm by rote memorization of past experience. , 1997, Journal of neurophysiology.

[15]  D. Wolpert,et al.  Temporal and amplitude generalization in motor learning. , 1998, Journal of neurophysiology.

[16]  B. Day,et al.  Voluntary modification of automatic arm movements evoked by motion of a visual target , 1999, Experimental Brain Research.

[17]  R Shadmehr,et al.  Electromyographic Correlates of Learning an Internal Model of Reaching Movements , 1999, The Journal of Neuroscience.

[18]  R A Scheidt,et al.  Persistence of motor adaptation during constrained, multi-joint, arm movements. , 2000, Journal of neurophysiology.

[19]  Rieko Osu,et al.  The central nervous system stabilizes unstable dynamics by learning optimal impedance , 2001, Nature.

[20]  Rieko Osu,et al.  Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. , 2002, Journal of neurophysiology.

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

[22]  J. Saunders,et al.  Humans use continuous visual feedback from the hand to control fast reaching movements , 2003, Experimental Brain Research.

[23]  J. Vercher,et al.  Target and hand position information in the online control of goal-directed arm movements , 2003, Experimental Brain Research.

[24]  M. Kawato,et al.  Adaptation to Stable and Unstable Dynamics Achieved By Combined Impedance Control and Inverse Dynamics Model , 2003 .

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

[26]  S. Scott Optimal feedback control and the neural basis of volitional motor control , 2004, Nature Reviews Neuroscience.

[27]  Shin'ya Nishida,et al.  Large-Field Visual Motion Directly Induces an Involuntary Rapid Manual Following Response , 2005, The Journal of Neuroscience.

[28]  David W Franklin,et al.  Impedance control and internal model use during the initial stage of adaptation to novel dynamics in humans , 2005, The Journal of physiology.

[29]  K. Shenoy,et al.  A Central Source of Movement Variability , 2006, Neuron.

[30]  Shin'ya Nishida,et al.  Spatiotemporal Tuning of Rapid Interactions between Visual-Motion Analysis and Reaching Movement , 2006, The Journal of Neuroscience.

[31]  Mark M. Churchland,et al.  Supplemental Data A Central Source of Movement Variability , 2006 .

[32]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[33]  Rieko Osu,et al.  Endpoint Stiffness of the Arm Is Directionally Tuned to Instability in the Environment , 2007, The Journal of Neuroscience.

[34]  Emanuel Todorov,et al.  Evidence for the Flexible Sensorimotor Strategies Predicted by Optimal Feedback Control , 2007, The Journal of Neuroscience.

[35]  D. Ostry,et al.  Muscle cocontraction following dynamics learning , 2008, Experimental Brain Research.

[36]  D. Wolpert,et al.  Specificity of Reflex Adaptation for Task-Relevant Variability , 2008, The Journal of Neuroscience.

[37]  H. Gomi Implicit online corrections of reaching movements , 2008, Current Opinion in Neurobiology.

[38]  J. A. Pruszynski,et al.  Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. , 2008, Journal of neurophysiology.

[39]  Rieko Osu,et al.  CNS Learns Stable, Accurate, and Efficient Movements Using a Simple Algorithm , 2008, The Journal of Neuroscience.

[40]  Reza Shadmehr,et al.  Motor Adaptation as a Process of Reoptimization , 2008, The Journal of Neuroscience.

[41]  Mark J Wagner,et al.  Shared Internal Models for Feedforward and Feedback Control , 2008, The Journal of Neuroscience.

[42]  J. A. Pruszynski,et al.  Long-Latency Reflexes of the Human Arm Reflect an Internal Model of Limb Dynamics , 2008, Current Biology.

[43]  Jörn Diedrichsen,et al.  Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? , 2008, Journal of neurophysiology.

[44]  Hiroaki Gomi,et al.  Temporal development of anticipatory reflex modulation to dynamical interactions during arm movement. , 2009, Journal of neurophysiology.

[45]  Stephen H Scott,et al.  Long-latency responses during reaching account for the mechanical interaction between the shoulder and elbow joints. , 2009, Journal of neurophysiology.

[46]  Gary C. Sing,et al.  Primitives for Motor Adaptation Reflect Correlated Neural Tuning to Position and Velocity , 2009, Neuron.

[47]  R. J. Beers,et al.  Motor Learning Is Optimally Tuned to the Properties of Motor Noise , 2009, Neuron.

[48]  Heinrich H Bülthoff,et al.  Seeing the hand while reaching speeds up on‐line responses to a sudden change in target position , 2009, The Journal of physiology.

[49]  Daniel M. Wolpert,et al.  A modular planar robotic manipulandum with end-point torque control , 2009, Journal of Neuroscience Methods.

[50]  J. A. Pruszynski,et al.  Temporal evolution of "automatic gain-scaling". , 2009, Journal of neurophysiology.

[51]  Alexander Borst,et al.  One Rule to Grow Them All: A General Theory of Neuronal Branching and Its Practical Application , 2010, PLoS Comput. Biol..

[52]  Gary C. Sing,et al.  Reduction in Learning Rates Associated with Anterograde Interference Results from Interactions between Different Timescales in Motor Adaptation , 2010, PLoS Comput. Biol..

[53]  R. Trumbower,et al.  Interactions between limb and environmental mechanics influence stretch reflex sensitivity in the human arm. , 2010, Journal of neurophysiology.

[54]  Li Li,et al.  Differentially Expressed RNA from Public Microarray Data Identifies Serum Protein Biomarkers for Cross-Organ Transplant Rejection and Other Conditions , 2010, PLoS Comput. Biol..

[55]  J. A. Pruszynski,et al.  The long-latency reflex is composed of at least two functionally independent processes. , 2011, Journal of neurophysiology.

[56]  E. Brenner,et al.  Fast and fine-tuned corrections when the target of a hand movement is displaced , 2011, Experimental Brain Research.

[57]  David W. Franklin,et al.  Computational Mechanisms of Sensorimotor Control , 2011, Neuron.

[58]  J. Andrew Pruszynski,et al.  Primary motor cortex underlies multi-joint integration for fast feedback control , 2011, Nature.

[59]  Dmitry Kobak,et al.  Adaptation Paths to Novel Motor Tasks Are Shaped by Prior Structure Learning , 2012, The Journal of Neuroscience.

[60]  Sae Franklin,et al.  Visuomotor feedback gains upregulate during the learning of novel dynamics , 2012, Journal of neurophysiology.

[61]  Brian L. Day,et al.  Direct visuomotor mapping for fast visually-evoked arm movements , 2012, Neuropsychologia.

[62]  Jörn Diedrichsen,et al.  Structural learning in feedforward and feedback control. , 2012, Journal of neurophysiology.

[63]  R. Shadmehr,et al.  Preparing to Reach: Selecting an Adaptive Long-Latency Feedback Controller , 2012, The Journal of Neuroscience.

[64]  L. Selen,et al.  Deliberation in the Motor System: Reflex Gains Track Evolving Evidence Leading to a Decision , 2012, The Journal of Neuroscience.

[65]  D. Wolpert,et al.  Gone in 0.6 Seconds: The Encoding of Motor Memories Depends on Recent Sensorimotor States , 2012, The Journal of Neuroscience.

[66]  Helen J. Huang,et al.  Reduction of Metabolic Cost during Motor Learning of Arm Reaching Dynamics , 2012, The Journal of Neuroscience.

[67]  S. Scott The computational and neural basis of voluntary motor control and planning , 2012, Trends in Cognitive Sciences.

[68]  D. Wolpert,et al.  The Temporal Evolution of Feedback Gains Rapidly Update to Task Demands , 2013, The Journal of Neuroscience.

[69]  Stephen H Scott,et al.  Rapid Feedback Responses Correlate with Reach Adaptation and Properties of Novel Upper Limb Loads , 2013, The Journal of Neuroscience.

[70]  J. Diedrichsen,et al.  A Dedicated Binding Mechanism for the Visual Control of Movement , 2014, Current Biology.

[71]  Helen J. Huang,et al.  Reductions in muscle coactivation and metabolic cost during visuomotor adaptation. , 2014, Journal of neurophysiology.

[72]  Frédéric Crevecoeur,et al.  Rapid Online Selection between Multiple Motor Plans , 2014, The Journal of Neuroscience.

[73]  Sae Franklin,et al.  Fractionation of the visuomotor feedback response to directions of movement and perturbation , 2014, Journal of neurophysiology.

[74]  Daniel M Wolpert,et al.  Rapid Visuomotor Corrective Responses during Transport of Hand-Held Objects Incorporate Novel Object Dynamics , 2015, The Journal of Neuroscience.

[75]  Hiroaki Gomi,et al.  Online gain update for manual following response accompanied by gaze shift during arm reaching. , 2015, Journal of neurophysiology.

[76]  David W Franklin,et al.  Rapid Feedback Responses Arise From Precomputed Gains. , 2016, Motor control.

[77]  Masaya Hirashima,et al.  Visuomotor Map Determines How Visually Guided Reaching Movements are Corrected Within and Across Trials123 , 2016, eNeuro.

[78]  Sae Franklin,et al.  Temporal Evolution of Spatial Computations for Visuomotor Control , 2016, The Journal of Neuroscience.