Individual Differences in Motor Noise and Adaptation Rate Are Optimally Related

Abstract Individual variations in motor adaptation rate were recently shown to correlate with movement variability or “motor noise” in a forcefield adaptation task. However, this finding could not be replicated in a meta-analysis of adaptation experiments. Possibly, this inconsistency stems from noise being composed of distinct components that relate to adaptation rate in different ways. Indeed, previous modeling and electrophysiological studies have suggested that motor noise can be factored into planning noise, originating from the brain, and execution noise, stemming from the periphery. Were the motor system optimally tuned to these noise sources, planning noise would correlate positively with adaptation rate, and execution noise would correlate negatively with adaptation rate, a phenomenon familiar in Kalman filters. To test this prediction, we performed a visuomotor adaptation experiment in 69 subjects. Using a novel Bayesian fitting procedure, we succeeded in applying the well-established state-space model of adaptation to individual data. We found that adaptation rate correlates positively with planning noise (β = 0.44; 95% HDI = [0.27 0.59]) and negatively with execution noise (β = –0.39; 95% HDI = [–0.50 –0.30]). In addition, the steady-state Kalman gain calculated from planning and execution noise correlated positively with adaptation rate (r = 0.54; 95% HDI = [0.38 0.66]). These results suggest that motor adaptation is tuned to approximate optimal learning, consistent with the “optimal control” framework that has been used to explain motor control. Since motor adaptation is thought to be a largely cerebellar process, the results further suggest the sensitivity of the cerebellum to both planning noise and execution noise.

[1]  Nando de Freitas,et al.  An Introduction to MCMC for Machine Learning , 2004, Machine Learning.

[2]  Philip N. Sabes,et al.  Modeling Sensorimotor Learning with Linear Dynamical Systems , 2006, Neural Computation.

[3]  R C Miall,et al.  System Identification Applied to a Visuomotor Task: Near-Optimal Human Performance in a Noisy Changing Task , 2003, The Journal of Neuroscience.

[4]  Kelvin E. Jones,et al.  Sources of signal-dependent noise during isometric force production. , 2002, Journal of neurophysiology.

[5]  M. Ernst,et al.  The statistical determinants of adaptation rate in human reaching. , 2008, Journal of vision.

[6]  T. Başar,et al.  A New Approach to Linear Filtering and Prediction Problems , 2001 .

[7]  Jerome Carriot,et al.  Learning to expect the unexpected: rapid updating in primate cerebellum during voluntary self-motion , 2015, Nature Neuroscience.

[8]  Philip N. Sabes,et al.  Calibration of visually guided reaching is driven by error-corrective learning and internal dynamics. , 2007, Journal of neurophysiology.

[9]  William J. Browne,et al.  Bayesian and likelihood-based methods in multilevel modeling 1 A comparison of Bayesian and likelihood-based methods for fitting multilevel models , 2006 .

[10]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[11]  Yoshiko Kojima,et al.  Encoding of action by the Purkinje cells of the cerebellum , 2015, Nature.

[12]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[13]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[14]  John K. Kruschke,et al.  Doing Bayesian Data Analysis: A Tutorial with R, JAGS, and Stan , 2014 .

[15]  J. Kruschke Bayesian estimation supersedes the t test. , 2013, Journal of experimental psychology. General.

[16]  M. Brainard,et al.  Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong , 2007, Nature.

[17]  Jörn Diedrichsen,et al.  Cerebellar regions involved in adaptation to force field and visuomotor perturbation. , 2012, Journal of neurophysiology.

[18]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[19]  J. Simpson,et al.  Microcircuitry and function of the inferior olive , 1998, Trends in Neurosciences.

[20]  J. Ioannidis Why Most Published Research Findings Are False , 2005, PLoS medicine.

[21]  Quoc V. Le,et al.  Adding Gradient Noise Improves Learning for Very Deep Networks , 2015, ArXiv.

[22]  Torrin M. Liddell,et al.  The Bayesian New Statistics: Hypothesis testing, estimation, meta-analysis, and power analysis from a Bayesian perspective , 2016, Psychonomic bulletin & review.

[23]  Maurice A. Smith,et al.  Environmental Consistency Determines the Rate of Motor Adaptation , 2014, Current Biology.

[24]  R. Kohn,et al.  On Gibbs sampling for state space models , 1994 .

[25]  J. Krakauer,et al.  An Implicit Plan Overrides an Explicit Strategy during Visuomotor Adaptation , 2006, The Journal of Neuroscience.

[26]  Robert J. van Beers,et al.  How Does Our Motor System Determine Its Learning Rate? , 2012, PloS one.

[27]  Robert J. van Beers,et al.  How does our motor system determine its learning rate , 2012 .

[28]  Eilon Vaadia,et al.  Trial-to-Trial Variability of Single Cells in Motor Cortices Is Dynamically Modified during Visuomotor Adaptation , 2009, The Journal of Neuroscience.

[29]  Reza Shadmehr,et al.  A memory of errors in sensorimotor learning , 2014, Science.

[30]  Opher Donchin,et al.  Individual Movement Variability Magnitudes Are Explained by Cortical Neural Variability , 2017, The Journal of Neuroscience.

[31]  Heidi M. Schambra,et al.  Direct Current Stimulation Promotes BDNF-Dependent Synaptic Plasticity: Potential Implications for Motor Learning , 2010, Neuron.

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

[33]  S. Koekkoek,et al.  Spatiotemporal firing patterns in the cerebellum , 2011, Nature Reviews Neuroscience.

[34]  Konrad P. Körding,et al.  Uncertainty of Feedback and State Estimation Determines the Speed of Motor Adaptation , 2009, Front. Comput. Neurosci..

[35]  MaRSS Lab,et al.  The New Statistics , 2017 .

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

[37]  T. Ebner,et al.  Force field effects on cerebellar Purkinje cell discharge with implications for internal models , 2006, Nature Neuroscience.

[38]  Martin T. Wiechert,et al.  Synaptic diversity enables temporal coding of coincident multi-sensory inputs in single neurons , 2015, Nature Neuroscience.

[39]  Jordan A Taylor,et al.  Explicit and Implicit Processes Constitute the Fast and Slow Processes of Sensorimotor Learning , 2015, The Journal of Neuroscience.

[40]  Kang He,et al.  The Statistical Determinants of the Speed of Motor Learning , 2016, PLoS Comput. Biol..

[41]  Aaron S. Andalman,et al.  Vocal Experimentation in the Juvenile Songbird Requires a Basal Ganglia Circuit , 2005, PLoS biology.

[42]  M. Hoagland,et al.  Feedback Systems An Introduction for Scientists and Engineers SECOND EDITION , 2015 .

[43]  Nicholas G. Polson,et al.  A Monte Carlo Approach to Nonnormal and Nonlinear State-Space Modeling , 1992 .

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

[45]  Allison J Doupe,et al.  Activity in a cortical-basal ganglia circuit for song is required for social context-dependent vocal variability. , 2010, Journal of neurophysiology.

[46]  Jeffrey N. Rouder,et al.  A power fallacy , 2015, Behavior research methods.

[47]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[48]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[49]  Michael Smithson,et al.  Doing Bayesian Data Analysis: A Tutorial with R and BUGS, J.J. Kruschke. Academic Press (2011), 653, $89.95Reviewed by Michael Smithson, ISBN: 9780123814852 , 2011 .

[50]  W. Stacey,et al.  Stochastic resonance improves signal detection in hippocampal CA1 neurons. , 2000, Journal of neurophysiology.

[51]  A. Gelman Prior distributions for variance parameters in hierarchical models (comment on article by Browne and Draper) , 2004 .

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

[53]  P. Rodríguez,et al.  BDNF val66met polymorphism influences motor system function in the human brain. , 2010, Cerebral cortex.

[54]  J. Krakauer,et al.  Explicit and Implicit Contributions to Learning in a Sensorimotor Adaptation Task , 2014, The Journal of Neuroscience.

[55]  Yohsuke R. Miyamoto,et al.  Temporal structure of motor variability is dynamically regulated and predicts motor learning ability , 2014, Nature Neuroscience.

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

[57]  Michael S. Brainard,et al.  Covert skill learning in a cortical-basal ganglia circuit , 2012, Nature.

[58]  W. Bialek,et al.  Physical limits to sensation and perception. , 1987, Annual review of biophysics and biophysical chemistry.

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

[60]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[61]  Torrin M. Liddell,et al.  The Bayesian New Statistics: Hypothesis Testing, Estimation, Meta-Analysis, and Power Analysis from a Bayesian Perspective , 2016 .

[62]  Torrin M. Liddell,et al.  Bayesian data analysis for newcomers , 2018, Psychonomic bulletin & review.

[63]  P. Dean,et al.  The cerebellar microcircuit as an adaptive filter: experimental and computational evidence , 2010, Nature Reviews Neuroscience.

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

[65]  R. J. van Beers,et al.  The role of execution noise in movement variability. , 2004, Journal of neurophysiology.

[66]  A. Doupe,et al.  Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song , 2005, Nature.

[67]  Shogo Ohmae,et al.  Climbing fibers encode a temporal-difference prediction error during cerebellar learning in mice , 2015, Nature Neuroscience.

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

[69]  Heidi Johansen-Berg,et al.  Structural and functional bases for individual differences in motor learning , 2011, Human brain mapping.

[70]  M. Frank,et al.  Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. , 2009, Nature neuroscience.