Competition between movement plans increases motor variability: evidence of a shared resource for movement planning

Various lines of evidence indicate that multiple movements can be prepared in parallel. Here, we show that preparing more than one movement comes with a cost: a movement plan is more variable if it is prepared simultaneously with another plan. This suggests that the representations of movement plans share a common neural resource and implies that the number of alternative plans is constrained by noise.

[1]  Markus Siegel,et al.  Neural substrates of cognitive capacity limitations , 2011, Proceedings of the National Academy of Sciences.

[2]  P. Cisek Integrated Neural Processes for Defining Potential Actions and Deciding between Them: A Computational Model , 2006, The Journal of Neuroscience.

[3]  John W. Krakauer,et al.  Motor Planning , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[4]  Jochen Ditterich,et al.  New advances in understanding decisions among multiple alternatives , 2012, Current Opinion in Neurobiology.

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

[6]  R. Ivry,et al.  Moving to Directly Cued Locations Abolishes Spatial Interference During Bimanual Actions , 2001, Psychological science.

[7]  Kris S Chaisanguanthum,et al.  Motor Variability Arises from a Slow Random Walk in Neural State , 2014, The Journal of Neuroscience.

[8]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

[9]  Herbert Heuer,et al.  The influence of movement cues on intermanual interactions , 2006, Psychological research.

[10]  J Randall Flanagan,et al.  Where One Hand Meets the Other: Limb-Specific and Action-Dependent Movement Plans Decoded from Preparatory Signals in Single Human Frontoparietal Brain Areas , 2013, The Journal of Neuroscience.

[11]  P. Bays Spikes not slots: noise in neural populations limits working memory , 2015, Trends in Cognitive Sciences.

[12]  W. Ma,et al.  A detection theory account of change detection. , 2004, Journal of vision.

[13]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[14]  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.

[15]  J. J. D. Gon,et al.  Reaction-time-dependent differences in the initial movement direction of fast goal-directed arm movements , 1991 .

[16]  D. Rosenbaum Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

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

[18]  Paul Cisek,et al.  Cortical mechanisms of action selection: the affordance competition hypothesis , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[19]  Paul M Bays,et al.  The precision of visual working memory is set by allocation of a shared resource. , 2009, Journal of vision.

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

[21]  T. Vilis,et al.  Integration of target and effector information in human posterior parietal cortex for the planning of action. , 2005, Journal of neurophysiology.

[22]  Jason P. Gallivan,et al.  Action plan co-optimization reveals the parallel encoding of competing reach movements , 2015, Nature Communications.

[23]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

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

[25]  Flavio T. P. Oliveira,et al.  Transcranial magnetic stimulation of posterior parietal cortex affects decisions of hand choice , 2010, Proceedings of the National Academy of Sciences.

[26]  Gerald Westheimer,et al.  Quantifying target conspicuity in contextual modulation by visual search. , 2011, Journal of vision.

[27]  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.

[28]  Flavio T. P. Oliveira,et al.  The Representation of Action , 2008, Current directions in psychological science.

[29]  P. Cisek,et al.  Rapid prediction of biomechanical costs during action decisions. , 2014, Journal of neurophysiology.

[30]  James H Elder,et al.  Cue dynamics underlying rapid detection of animals in natural scenes. , 2009, Journal of vision.

[31]  Julie Duque,et al.  Behavioral / Systems / Cognitive Evidence for Two Concurrent Inhibitory Mechanisms during Response Preparation , 2010 .

[32]  Oostwoud Wijdenes,et al.  3. Fast and Fine-tuned Corrections , .

[33]  H. Deubel,et al.  Attentional landscapes in reaching and grasping , 2010, Vision Research.

[34]  Paul M Bays,et al.  Dynamic Shifts of Limited Working Memory Resources in Human Vision , 2008, Science.

[35]  W. Ma,et al.  Changing concepts of working memory , 2014, Nature Neuroscience.

[36]  Robert J Summers,et al.  Neuronal convergence in early contrast vision: binocular summation is followed by response nonlinearity and area summation. , 2009, Journal of vision.

[37]  J. Palmer Attentional limits on the perception and memory of visual information. , 1990, Journal of experimental psychology. Human perception and performance.

[38]  Paul M Bays,et al.  Noise in Neural Populations Accounts for Errors in Working Memory , 2014, The Journal of Neuroscience.

[39]  Paul M Bays,et al.  Dynamic Updating of Working Memory Resources for Visual Objects , 2011, The Journal of Neuroscience.

[40]  Wei Ji Ma,et al.  Variability in encoding precision accounts for visual short-term memory limitations , 2012, Proceedings of the National Academy of Sciences.

[41]  Craig S. Chapman,et al.  Reaching for the unknown: Multiple target encoding and real-time decision-making in a rapid reach task , 2010, Cognition.

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

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

[44]  Paul M Bays,et al.  Temporal dynamics of encoding, storage, and reallocation of visual working memory. , 2011, Journal of vision.

[45]  Heiner Deubel,et al.  Attention allocation before antisaccades. , 2016, Journal of vision.

[46]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[47]  A. Osman,et al.  Dimensional overlap: cognitive basis for stimulus-response compatibility--a model and taxonomy. , 1990, Psychological review.

[48]  G. Pellizzer,et al.  Motor planning: effect of directional uncertainty with discrete spatial cues , 2003, Experimental Brain Research.

[49]  Marilyn L. Shaw,et al.  A capacity allocation model for reaction time. , 1978 .

[50]  J. Kelso,et al.  Are movements prepared in parts? Not under compatible (naturalized) conditions. , 1980, Journal of experimental psychology. General.

[51]  John T. Serences,et al.  Reconstructions of Information in Visual Spatial Working Memory Degrade with Memory Load , 2014, Current Biology.

[52]  Peter Redgrave,et al.  Layered Control Architectures in Robots and Vertebrates , 1999, Adapt. Behav..

[53]  N Moray,et al.  Where is capacity limited? A survey and a model. , 1967, Acta psychologica.

[54]  W. E. Hick Quarterly Journal of Experimental Psychology , 1948, Nature.

[55]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[56]  D. Kahneman,et al.  Attention and Effort , 1973 .

[57]  Brandie M. Stewart,et al.  Motor, not visual, encoding of potential reach targets , 2014, Current Biology.

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

[59]  Robert Oostenveld,et al.  Competitive interactions in sensorimotor cortex: oscillations express separation between alternative movement targets. , 2014, Journal of neurophysiology.

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

[61]  C. Ghez,et al.  Discrete and continuous planning of hand movements and isometric force trajectories , 1997, Experimental Brain Research.

[62]  R. Andersen,et al.  Posterior Parietal Cortex Encodes Autonomously Selected Motor Plans , 2007, Neuron.

[63]  S. Luck,et al.  Discrete fixed-resolution representations in visual working memory , 2008, Nature.

[64]  K. Nakayama,et al.  Hidden cognitive states revealed in choice reaching tasks , 2009, Trends in Cognitive Sciences.

[65]  Donald A. Norman,et al.  Attention to Action , 1986 .

[66]  S. Bestmann,et al.  Time-Dependent Changes in Human Corticospinal Excitability Reveal Value-Based Competition for Action during Decision Processing , 2012, The Journal of Neuroscience.

[67]  John W. Krakauer,et al.  Hedging Your Bets: Intermediate Movements as Optimal Behavior in the Context of an Incomplete Decision , 2015, PLoS Comput. Biol..