Long-Latency Feedback Coordinates Upper-Limb and Hand Muscles during Object Manipulation Tasks123

Visual Overview Suppose that someone bumps into your arm at a party while you are holding a glass of wine. Motion of the disturbed arm will engage rapid and goal-directed feedback responses in the upper-limb. Suppose that someone bumps into your arm at a party while you are holding a glass of wine. Motion of the disturbed arm will engage rapid and goal-directed feedback responses in the upper-limb. Although such responses can rapidly counter the perturbation, it is also clearly desirable not to destabilize your grasp and/or spill the wine. Here we investigated how healthy humans maintain a stable grasp following perturbations by using a paradigm that requires spatial tuning of the motor response dependent on the location of a virtual target. Our results highlight a synchronized expression of target-directed feedback in shoulder and hand muscles occurring at ∼60 ms. Considering that conduction delays are longer for the more distal hand muscles, these results suggest that target-directed responses in hand muscles were initiated before those for the shoulder muscles. These results show that long-latency feedback can coordinate upper limb and hand muscles during object manipulation tasks.

[1]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

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

[3]  Frédéric Crevecoeur,et al.  Priors Engaged in Long-Latency Responses to Mechanical Perturbations Suggest a Rapid Update in State Estimation , 2013, PLoS Comput. Biol..

[4]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

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

[6]  Claire F. Honeycutt,et al.  Planning of Ballistic Movement following Stroke: Insights from the Startle Reflex , 2012, PloS one.

[7]  F Crevecoeur,et al.  Feedback responses rapidly scale with the urgency to correct for external perturbations. , 2013, Journal of neurophysiology.

[8]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[9]  John M. Hollerbach,et al.  Dynamic interactions between limb segments during planar arm movement , 1982, Biological Cybernetics.

[10]  Stephen H. Scott,et al.  Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching , 1999, Journal of Neuroscience Methods.

[11]  Je Hi An,et al.  The Differential Role of Motor Cortex in Stretch Reflex Modulation Induced by Changes in Environmental Mechanics and Verbal Instruction , 2009, Journal of Neuroscience.

[12]  Jörn Diedrichsen,et al.  Rapid feedback corrections during a bimanual postural task. , 2013, Journal of neurophysiology.

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

[14]  J. Flanagan,et al.  Modulation of grip force with load force during point-to-point arm movements , 2004, Experimental Brain Research.

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

[16]  R. Wurtz,et al.  Visual Perception and Corollary Discharge , 2008, Perception.

[17]  Frédéric Danion,et al.  Can the Human Brain Predict the Consequences of Arm Movement Corrections When Transporting an Object? Hints from Grip Force Adjustments , 2007, The Journal of Neuroscience.

[18]  G. Allen,et al.  Cerebrocerebellar communication systems. , 1974, Physiological reviews.

[19]  B. Efron,et al.  The Jackknife Estimate of Variance , 1981 .

[20]  K. J. Cole,et al.  Grip-force responses to unanticipated object loading: load direction reveals body- and gravity-referenced intrinsic task variables , 1996, Experimental Brain Research.

[21]  C. Metz Basic principles of ROC analysis. , 1978, Seminars in nuclear medicine.

[22]  Anthony N. Carlsen,et al.  Can prepared responses be stored subcortically? , 2004, Experimental Brain Research.

[23]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[24]  K. T. Ramesh,et al.  Modelling of non-linear elastic tissues for surgical simulation , 2010, Computer methods in biomechanics and biomedical engineering.

[25]  M. Hepp-Reymond,et al.  EMG activation patterns during force production in precision grip , 2004, Experimental Brain Research.

[26]  G. R. Davis,et al.  Motor nerve conduction velocity distributions in man: results of a new computer-based collision technique. , 1987, Electroencephalography and clinical neurophysiology.

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

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

[29]  G. F. Koshland,et al.  Electromyographic responses to a mechanical perturbation applied during impending arm movements in different directions: one-joint and two-joint conditions , 2000, Experimental Brain Research.

[30]  Maurice A Smith,et al.  Flexible Control of Safety Margins for Action Based on Environmental Variability , 2015, The Journal of Neuroscience.

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

[32]  J R Flanagan,et al.  The Role of Internal Models in Motion Planning and Control: Evidence from Grip Force Adjustments during Movements of Hand-Held Loads , 1997, The Journal of Neuroscience.

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

[34]  G L Gottlieb,et al.  Afferent contributions to stretch-evoked myoelectric responses. , 1982, Journal of neurophysiology.

[35]  Alan M. Wing,et al.  Internal models of the motor system that explain predictive grip force control , 2004 .

[36]  Thomas S. Buchanan,et al.  BIOMECHANICS OF HUMAN MOVEMENT , 2005 .

[37]  Jean-Louis Thonnard,et al.  The cutaneous contribution to adaptive precision grip , 2004, Trends in Neurosciences.

[38]  Jonathan Shemmell,et al.  Interactions between stretch and startle reflexes produce task-appropriate rapid postural reactions , 2015, Front. Integr. Neurosci..

[39]  J. Diedrichsen Optimal Task-Dependent Changes of Bimanual Feedback Control and Adaptation , 2007, Current Biology.

[40]  A. Bastian Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[41]  P. Matthews The human stretch reflex and the motor cortex , 1991, Trends in Neurosciences.

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

[43]  Jeffrey Weiler,et al.  Goal-dependent modulation of the long-latency stretch response at the shoulder, elbow, and wrist. , 2015, Journal of neurophysiology.

[44]  R. Johansson,et al.  Factors influencing the force control during precision grip , 2004, Experimental Brain Research.

[45]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[46]  P. Delwaide,et al.  Age‐related changes in fastest and slowest conducting axons of thenar motor units , 1999, Muscle & nerve.

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

[48]  P. Matthews,et al.  The contrasting stretch reflex responses of the long and short flexor muscles of the human thumb. , 1984, The Journal of physiology.

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

[50]  G. M. Gauthier,et al.  Oculo-manual coordination control: Ocular and manual tracking of visual targets with delayed visual feedback of the hand motion , 2004, Experimental Brain Research.

[51]  Tadashi Isa,et al.  Circuits for skilled reaching and grasping. , 2012, Annual review of neuroscience.

[52]  D. Wolpert,et al.  Principles of sensorimotor learning , 2011, Nature Reviews Neuroscience.

[53]  R. Johansson,et al.  Loads applied tangential to a fingertip during an object restraint task can trigger short-latency as well as long-latency EMG responses in hand muscles , 2003, Experimental Brain Research.

[54]  Thomas M. Jessell,et al.  Skilled reaching relies on a V2a propriospinal internal copy circuit , 2014, Nature.

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

[56]  Christian Ethier,et al.  The comparable size and overlapping nature of upper limb distal and proximal muscle representations in the human motor cortex , 2006, The European journal of neuroscience.