Distinct coordinate systems for adaptations of movement direction and extent.

Learned compensations for perturbed visual feedback of movement extent and direction generalize differently to unpracticed movement directions, which suggests different underlying neural mechanisms. Here we investigated whether gain and rotation adaptations are consistent with representation in different coordinate systems. Subjects performed a force-aiming task with the wrist and learned different gains or rotations for different force directions. Generalization was tested without visual feedback for the same extrinsic directions but with the forearm in a different pronation-supination orientation. When the change in forearm orientation caused the adapted visuomotor map to conflict in extrinsic and joint-based coordinates, rotation generalization occurred in extrinsic coordinates but with reduced magnitude. In contrast, gain generalization appeared reduced and phase shifted. When the forearm was rotated further, such that all imposed perturbations aligned in both joint-based and extrinsic coordinates in both postures, rotation generalization was further reduced, whereas there was neither reduction nor phase shift in the pattern of extent generalization. These results show that rotation generalization was expressed in extrinsic coordinates, and that generalization magnitude was modulated by posture. In contrast, gain generalization appeared to depend on target direction defined by an integrated combination of extrinsic and joint-based coordinates and was not reduced substantially by posture changes alone. Although the quality of the model fit underlying our interpretation prevents us from making strong conclusions, the data suggest that adaptations of movement direction and extent are represented according to distinct coordinate systems.NEW & NOTEWORTHY Visuomotor gain and rotation adaptations generalize differently to novel movement directions, which suggests different neural mechanisms. When extrinsic and joint-based coordinates are effectively dissociated in an isometric aiming task, we find that they also generalize in different coordinate systems. Specifically, rotation generalized in extrinsic coordinates and decayed as posture departed from that adopted during adaptation. In contrast, gain generalization was expressed according to mixed extrinsic/joint-based coordinates and was not substantially reduced by postural changes.

[1]  Marco Davare,et al.  Dissociable contribution of the parietal and frontal cortex to coding movement direction and amplitude , 2015, Front. Hum. Neurosci..

[2]  P. Viviani,et al.  Frames of reference and control parameters in visuomanual pointing. , 1998, Journal of experimental psychology. Human perception and performance.

[3]  C Ghez,et al.  Learning of Visuomotor Transformations for Vectorial Planning of Reaching Trajectories , 2000, The Journal of Neuroscience.

[4]  Paolo Viviani,et al.  Altering the visuomotor gain , 2002, Experimental Brain Research.

[5]  M. Lappe,et al.  Eye position effects in saccadic adaptation. , 2011, Journal of neurophysiology.

[6]  H. Jeffreys,et al.  The Theory of Probability , 1896 .

[7]  M. Lappe,et al.  Eye position effects in saccadic adaptation in macaque monkeys. , 2012, Journal of neurophysiology.

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

[9]  Howard G. Wu,et al.  The Generalization of Visuomotor Learning to Untrained Movements and Movement Sequences Based on Movement Vector and Goal Location Remapping , 2013, The Journal of Neuroscience.

[10]  J. Krakauer,et al.  Generalization of Motor Learning Depends on the History of Prior Action , 2006, PLoS biology.

[11]  J. Kalaska,et al.  Comparison of variability of initial kinematics and endpoints of reaching movements , 1999, Experimental Brain Research.

[12]  R Shadmehr,et al.  Spatial Generalization from Learning Dynamics of Reaching Movements , 2000, The Journal of Neuroscience.

[13]  D. Wolpert,et al.  The effect of contextual cues on the encoding of motor memories , 2013, Journal of neurophysiology.

[14]  Maurice A. Smith,et al.  Motor Memory Is Encoded as a Gain-Field Combination of Intrinsic and Extrinsic Action Representations , 2012, Journal of Neuroscience.

[15]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[16]  Daniel M Wolpert,et al.  Adaptation to a visuomotor shift depends on the starting posture. , 2002, Journal of neurophysiology.

[17]  J. Krakauer,et al.  Learning not to generalize: modular adaptation of visuomotor gain. , 2010, Journal of neurophysiology.

[18]  David J Ostry,et al.  Transfer of Motor Learning across Arm Configurations , 2002, The Journal of Neuroscience.

[19]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Randall Flanagan,et al.  Motor learning of novel dynamics is not represented in a single global coordinate system: evaluation of mixed coordinate representations and local learning , 2013, Journal of neurophysiology.

[21]  R. Shadmehr,et al.  A Gain-Field Encoding of Limb Position and Velocity in the Internal Model of Arm Dynamics , 2003, PLoS biology.

[22]  Jinsung Wang,et al.  Adaptation to Visuomotor Rotations Remaps Movement Vectors, Not Final Positions , 2005, The Journal of Neuroscience.

[23]  Philip N. Sabes,et al.  Sensory integration for reaching: models of optimality in the context of behavior and the underlying neural circuits. , 2011, Progress in brain research.

[24]  R. Caminiti,et al.  Shift of preferred directions of premotor cortical cells with arm movements performed across the workspace , 2004, Experimental Brain Research.

[25]  Reza Shadmehr,et al.  Internal models of limb dynamics and the encoding of limb state , 2005, Journal of neural engineering.

[26]  Y. Rossetti,et al.  Three timescales in prism adaptation. , 2015, Journal of neurophysiology.

[27]  Ilana Nisky,et al.  Learning and generalization in an isometric visuomotor task. , 2015, Journal of neurophysiology.

[28]  A. de Rugy,et al.  Changes in wrist muscle activity with forearm posture: implications for the study of sensorimotor transformations. , 2012, Journal of neurophysiology.

[29]  A. Haith,et al.  Unlearning versus savings in visuomotor adaptation: comparing effects of washout, passage of time, and removal of errors on motor memory , 2013, Front. Hum. Neurosci..

[30]  James Gordon,et al.  Accuracy of planar reaching movements , 1994, Experimental Brain Research.

[31]  R. Andersen,et al.  The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements , 2006, Neuropsychologia.

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

[33]  Zoubin Ghahramani,et al.  Modular decomposition in visuomotor learning , 1997, Nature.

[34]  David M. Huberdeau,et al.  Formation of a long-term memory for visuomotor adaptation following only a few trials of practice. , 2015, Journal of neurophysiology.

[35]  J. F. Soechting,et al.  Errors in pointing are due to approximations in sensorimotor transformations. , 1989, Journal of neurophysiology.

[36]  Aymar de Rugy,et al.  Generalization of visuomotor adaptation to different muscles is less efficient: Experiment and model , 2010 .

[37]  Aymar de Rugy,et al.  The synergistic organization of muscle recruitment constrains visuomotor adaptation. , 2009, Journal of neurophysiology.