A switching cost for motor planning

Movement planning consists of choosing the endpoint of the movement and selecting the motor program that will bring the effector on the endpoint. It is widely accepted that movement endpoint is updated on a trial-by-trial basis with respect to the observed errors and that the motor program for a given movement follows the rules of optimal feedback control. Here, we show clear limitations of these predictions because of the existence of a switching cost for motor planning. First, this cost prevented participants from tuning their motor program appropriately for each individual trial. This was true even when the participants selected the width of the target that they reached toward or when they had learned the appropriate motor program previously. These data are compatible with the existence of a switching cost such as those found in cognitive studies. Interestingly, this cost of switching shares many features of costs reported in cognitive task switching experiments and, when tested in the same participants, was correlated with it. Second, we found that randomly changing the width of a target over the course of a reaching experiment prevents the motor system from updating the endpoint of movements on the basis of the performance on the previous trial if the width of the target has changed. These results provide new insights into the process of motor planning and how it relates to optimal control theory and to a selection by consequences process rather than to an error-based process for action selection.

[1]  A. Haith,et al.  Independence of Movement Preparation and Movement Initiation , 2016, The Journal of Neuroscience.

[2]  Eileen Kowler,et al.  The effect of expectations on slow oculomotor control—IV. Anticipatory smooth eye movements depend on prior target motions , 1984, Vision Research.

[3]  Catherine M Arrington,et al.  PSYCHOLOGICAL SCIENCE Research Article The Cost of a Voluntary Task Switch , 2022 .

[4]  K. A. Hadland,et al.  The Effect of Cingulate Cortex Lesions on Task Switching and Working Memory , 2003, Journal of Cognitive Neuroscience.

[5]  D. Alan Allport,et al.  SHIFTING INTENTIONAL SET - EXPLORING THE DYNAMIC CONTROL OF TASKS , 1994 .

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

[7]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[8]  The Effect of Blocked, Random, and Systematically Increasing Practice on learning of Different Types of Basketball Passes , 2012 .

[9]  Jeremy D Wong,et al.  The central nervous system does not minimize energy cost in arm movements. , 2010, Journal of neurophysiology.

[10]  D M Wolpert,et al.  The influence of previous experience on predictive motor control , 2001, Neuroreport.

[11]  Stephen H Scott,et al.  Influence of the behavioral goal and environmental obstacles on rapid feedback responses. , 2012, Journal of neurophysiology.

[12]  R. Johansson,et al.  Independent control of human finger‐tip forces at individual digits during precision lifting. , 1992, The Journal of physiology.

[13]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

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

[15]  Daniel M Wolpert,et al.  Parallel specification of competing sensorimotor control policies for alternative action options , 2016, Nature Neuroscience.

[16]  S. Keele,et al.  Changing internal constraints on action: the role of backward inhibition. , 2000, Journal of experimental psychology. General.

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

[18]  Catherine M Arrington,et al.  Voluntary task switching: chasing the elusive homunculus. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[19]  Etienne Olivier,et al.  Short-Latency Influence of Medial Frontal Cortex on Primary Motor Cortex during Action Selection under Conflict , 2009, The Journal of Neuroscience.

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

[21]  E. Procyk,et al.  Anterior cingulate activity during routine and non-routine sequential behaviors in macaques , 2000, Nature Neuroscience.

[22]  Jörn Diedrichsen,et al.  Dissociating Task-set Selection from Task-set Inhibition in the Prefrontal Cortex , 2006, Journal of Cognitive Neuroscience.

[23]  Jonathan B Dingwell,et al.  Trial-to-trial dynamics and learning in a generalized, redundant reaching task. , 2013, Journal of neurophysiology.

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

[25]  Olivier White,et al.  Flexible Switching of Feedback Control Mechanisms Allows for Learning of Different Task Dynamics , 2013, PloS one.

[26]  D. Elliott,et al.  The Utilization of Visual Feedback Information during Rapid Pointing Movements , 1985, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[27]  L. Cohen,et al.  Kinematically specific interhemispheric inhibition operating in the process of generation of a voluntary movement. , 2005, Cerebral cortex.

[28]  F. Horak,et al.  Cerebellar control of postural scaling and central set in stance. , 1994, Journal of neurophysiology.

[29]  O. Hikosaka,et al.  Switching from automatic to controlled action by monkey medial frontal cortex , 2007, Nature Neuroscience.

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

[31]  Jeremy D Wong,et al.  The cost of moving optimally: kinematic path selection. , 2014, Journal of neurophysiology.

[32]  G. D. Logan Task Switching , 2022 .

[33]  Andrea M Philipp,et al.  Control and interference in task switching--a review. , 2010, Psychological bulletin.

[34]  James L. Lyons,et al.  Optimal Control Strategies Under Different Feedback Schedules: Kinematic Evidence , 2002, Journal of motor behavior.

[35]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

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

[37]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[38]  H N Zelaznik,et al.  Target-size influences on reaction time with movement time controlled. , 1980, Journal of motor behavior.

[39]  Mark Shelhamer,et al.  Similarities in error processing establish a link between saccade prediction at baseline and adaptation performance. , 2014, Journal of neurophysiology.

[40]  J Tanji,et al.  Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. , 1996, Journal of neurophysiology.

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

[42]  L. Selen,et al.  Impedance Control Reduces Instability That Arises from Motor Noise , 2009, The Journal of Neuroscience.

[43]  Aymar de Rugy,et al.  Muscle Coordination Is Habitual Rather than Optimal , 2012, The Journal of Neuroscience.

[44]  Louise P. Kirsch,et al.  Information about the Weight of Grasped Objects from Vision and Internal Models Interacts within the Primary Motor Cortex , 2010, The Journal of Neuroscience.

[45]  A. Karlsen [Selection by consequences]. , 1992, Tidsskrift for den Norske laegeforening : tidsskrift for praktisk medicin, ny raekke.

[46]  G. Barnes,et al.  Oculomotor prediction of accelerative target motion during occlusion: long-term and short-term effects , 2010, Experimental Brain Research.

[47]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[48]  Philip N. Sabes,et al.  How Each Movement Changes the Next: An Experimental and Theoretical Study of Fast Adaptive Priors in Reaching , 2011, The Journal of Neuroscience.

[49]  R. J. van Beers,et al.  What Autocorrelation Tells Us about Motor Variability: Insights from Dart Throwing , 2013, PloS one.

[50]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[51]  S. Monsell,et al.  Costs of a predictible switch between simple cognitive tasks. , 1995 .

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

[53]  Jean-Jacques Orban de Xivry,et al.  Kalman Filtering Naturally Accounts for Visually Guided and Predictive Smooth Pursuit Dynamics , 2013, The Journal of Neuroscience.

[54]  R. Ivry,et al.  The coordination of movement: optimal feedback control and beyond , 2010, Trends in Cognitive Sciences.

[55]  Eli Brenner,et al.  Random walk of motor planning in task-irrelevant dimensions. , 2013, Journal of neurophysiology.

[56]  A. Milner,et al.  To halve and to halve not: An analysis of line bisection judgements in normal subjects , 1992, Neuropsychologia.

[57]  Jean-Jacques Orban de Xivry Trial-to-trial reoptimization of motor behavior due to changes in task demands is limited. , 2013 .

[58]  Harry J. Wyatt,et al.  Smooth pursuit eye movements with imaginary targets defined by extrafoveal cues , 1994, Vision Research.

[59]  J. O. de Xivry Trial-to-Trial Reoptimization of Motor Behavior Due to Changes in Task Demands Is Limited , 2013, PLoS ONE.

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

[61]  Kenji Kawano,et al.  Trial-by-trial updating of the gain in preparation for smooth pursuit eye movement based on past experience in humans. , 2008, Journal of neurophysiology.

[62]  J. A. Pruszynski,et al.  Optimal feedback control and the long-latency stretch response , 2012, Experimental Brain Research.

[63]  Julie Duque,et al.  Role of corticospinal suppression during motor preparation. , 2009, Cerebral cortex.

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