Reduction in Learning Rates Associated with Anterograde Interference Results from Interactions between Different Timescales in Motor Adaptation

Prior experiences can influence future actions. These experiences can not only drive adaptive changes in motor output, but they can also modulate the rate at which these adaptive changes occur. Here we studied anterograde interference in motor adaptation – the ability of a previously learned motor task (Task A) to reduce the rate of subsequently learning a different (and usually opposite) motor task (Task B). We examined the formation of the motor system's capacity for anterograde interference in the adaptive control of human reaching-arm movements by determining the amount of interference after varying durations of exposure to Task A (13, 41, 112, 230, and 369 trials). We found that the amount of anterograde interference observed in the learning of Task B increased with the duration of Task A. However, this increase did not continue indefinitely; instead, the interference reached asymptote after 15–40 trials of Task A. Interestingly, we found that a recently proposed multi-rate model of motor adaptation, composed of two distinct but interacting adaptive processes, predicts several key features of the interference patterns we observed. Specifically, this computational model (without any free parameters) predicts the initial growth and leveling off of anterograde interference that we describe, as well as the asymptotic amount of interference that we observe experimentally (R2 = 0.91). Understanding the mechanisms underlying anterograde interference in motor adaptation may enable the development of improved training and rehabilitation paradigms that mitigate unwanted interference.

[1]  John R. Anderson,et al.  Reflections of the Environment in Memory Form of the Memory Functions , 2022 .

[2]  P. R. Davidson,et al.  Scaling down motor memories: de-adaptation after motor learning , 2004, Neuroscience Letters.

[3]  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.

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

[5]  J R Anderson,et al.  Practice and retention: a unifying analysis. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[6]  J. Wixted The psychology and neuroscience of forgetting. , 2004, Annual review of psychology.

[7]  E. Bizzi,et al.  Motor Learning with Unstable Neural Representations , 2007, Neuron.

[8]  Sarah E. Criscimagna-Hemminger,et al.  Size of error affects cerebellar contributions to motor learning. , 2010, Journal of neurophysiology.

[9]  L. Porter,et al.  Negative transfer in verbal learning. , 1953, Journal of experimental psychology.

[10]  Reza Shadmehr,et al.  Impairment of Retention But Not Acquisition of a Visuomotor Skill Through Time-Dependent Disruption of Primary Motor Cortex , 2007, The Journal of Neuroscience.

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

[12]  D. Ostry,et al.  Stimulation of the Posterior Parietal Cortex Interferes with Arm Trajectory Adjustments during the Learning of New Dynamics , 2004, The Journal of Neuroscience.

[13]  J. Randall Flanagan,et al.  Interference between velocity-dependent and position-dependent force-fields indicates that tasks depending on different kinematic parameters compete for motor working memory , 2005, Experimental Brain Research.

[14]  Michael C. Anderson,et al.  Remembering can cause forgetting: retrieval dynamics in long-term memory. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[15]  John W Krakauer,et al.  Motor learning and consolidation: the case of visuomotor rotation. , 2009, Advances in experimental medicine and biology.

[16]  R. Shadmehr,et al.  Adaptation and generalization in acceleration-dependent force fields , 2006, Experimental Brain Research.

[17]  N. Schweighofer,et al.  Dual Adaptation Supports a Parallel Architecture of Motor Memory , 2009, The Journal of Neuroscience.

[18]  J. Krakauer,et al.  Explaining savings for visuomotor adaptation: linear time-invariant state-space models are not sufficient. , 2008, Journal of neurophysiology.

[19]  Gary C. Sing,et al.  Primitives for Motor Adaptation Reflect Correlated Neural Tuning to Position and Velocity , 2009, Neuron.

[20]  Emilio Bizzi,et al.  Intermittent Practice Facilitates Stable Motor Memories , 2006, The Journal of Neuroscience.

[21]  D.Sc. Joseph Berkson Are there Two Regressions , 1950 .

[22]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[23]  J. Krakauer,et al.  Adaptation to Visuomotor Transformations: Consolidation, Interference, and Forgetting , 2005, The Journal of Neuroscience.

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

[25]  Wayne A. Wickelgren,et al.  Trace resistance and the decay of long-term memory. , 1972 .

[26]  David J Ostry,et al.  Neural averaging in motor learning. , 2007, Journal of neurophysiology.

[27]  R. Shadmehr,et al.  Spontaneous recovery of motor memory during saccade adaptation. , 2008, Journal of neurophysiology.

[28]  R. Shadmehr,et al.  Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. , 2005, Journal of neurophysiology.

[29]  Sarah E. Criscimagna-Hemminger,et al.  Consolidation Patterns of Human Motor Memory , 2008, The Journal of Neuroscience.

[30]  T. Ebner,et al.  Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. , 2004, Journal of neurophysiology.

[31]  R Shadmehr,et al.  Electromyographic Correlates of Learning an Internal Model of Reaching Movements , 1999, The Journal of Neuroscience.

[32]  D. Rubin,et al.  One Hundred Years of Forgetting : A Quantitative Description of Retention , 1996 .

[33]  Konrad Paul Kording,et al.  Relevance of error: what drives motor adaptation? , 2009, Journal of neurophysiology.

[34]  Scott E. Bevans,et al.  Effect of visual error size on saccade adaptation in monkey. , 2003, Journal of neurophysiology.

[35]  D. Challet,et al.  Optimal approximations of power laws with exponentials: application to volatility models with long memory , 2007 .

[36]  Kaoru Yoshida,et al.  Memory of Learning Facilitates Saccadic Adaptation in the Monkey , 2004, The Journal of Neuroscience.

[37]  Kurt A. Thoroughman,et al.  Motor adaptation to single force pulses: sensitive to direction but insensitive to within-movement pulse placement and magnitude. , 2006, Journal of neurophysiology.

[38]  Vincent S. Huang,et al.  Persistence of motor memories reflects statistics of the learning event. , 2009, Journal of neurophysiology.

[39]  Emilio Bizzi,et al.  Disruption of Primary Motor Cortex before Learning Impairs Memory of Movement Dynamics , 2006, The Journal of Neuroscience.

[40]  D. Lewis,et al.  Facilitation and interference in performance on the modified Mashburn apparatus: I. The effects of varying the amount of original learning. , 1951, Journal of experimental psychology.

[41]  K. Linnet,et al.  Performance of Deming regression analysis in case of misspecified analytical error ratio in method comparison studies. , 1998, Clinical chemistry.

[42]  N Gochman,et al.  Incorrect least-squares regression coefficients in method-comparison analysis. , 1979, Clinical chemistry.

[43]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[44]  Konrad Paul Kording,et al.  The dynamics of memory as a consequence of optimal adaptation to a changing body , 2007, Nature Neuroscience.

[45]  D. Rubin,et al.  The Precise Time Course of Retention , 1999 .

[46]  H. Hellendoorn,et al.  Applications of statistics in clinical chemistry. A critical evaluation of regression lines. , 1975, Clinica chimica acta; international journal of clinical chemistry.

[47]  R. Shadmehr,et al.  Cerebellar Contributions to Adaptive Control of Saccades in Humans , 2009, The Journal of Neuroscience.

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

[49]  R. Miall,et al.  Adaptation to rotated visual feedback: a re-examination of motor interference , 2003, Experimental Brain Research.

[50]  R. Shadmehr,et al.  Mechanisms influencing acquisition and recall of motor memories. , 2002, Journal of neurophysiology.

[51]  Shana K. Carpenter,et al.  The Wickelgren Power Law and the Ebbinghaus Savings Function , 2007, Psychological science.

[52]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

[53]  J Randall Flanagan,et al.  Visuomotor rotations of varying size and direction compete for a single internal model in motor working memory. , 2002, Journal of experimental psychology. Human perception and performance.

[54]  R Shadmehr,et al.  Time-dependent motor memory processes in amnesic subjects. , 1998, Journal of neurophysiology.

[55]  Robert M. Gagne,et al.  On the relation between similarity and transfer of training in the learning of discriminative motor tasks. , 1950 .

[56]  D. Wolpert,et al.  Failure to Consolidate the Consolidation Theory of Learning for Sensorimotor Adaptation Tasks , 2004, The Journal of Neuroscience.

[57]  E. Bizzi,et al.  Consolidation in human motor memory , 1996, Nature.

[58]  Wilsaan M. Joiner,et al.  Long-term retention explained by a model of short-term learning in the adaptive control of reaching. , 2008, Journal of neurophysiology.

[59]  Amy J Bastian,et al.  Cerebellar damage impairs automaticity of a recently practiced movement. , 2002, Journal of neurophysiology.