Evolution of Motor Memory During the Seconds After Observation of Motor Error

• Published in: Journal of neurophysiology Vol. 97; no. 6; pp. 3976 - 3985
• Main Authors: Huang, Vincent S, Shadmehr, Reza
• Format: Journal Article
• Language: English
• Published: United States Am Phys Soc 01-06-2007
• Subjects: Adaptation, Physiological; Bayes Theorem; Humans; Memory - physiology; Models, Biological; Movement - physiology; Predictive Value of Tests; Psychomotor Performance - physiology; Task Performance and Analysis; Time Factors
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.01281.2006

Laboratory for Computational Motor Control, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland
Submitted 6 December 2006;
accepted in final form 4 April 2007
When a movement results in error, the nervous system amends the motor commands that generate the subsequent movement. Here we show that this adaptation depends not just on error, but also on passage of time between the two movements. We observed that subjects learned a reaching task faster, i.e., with fewer trials, when the intertrial time intervals (ITIs) were lengthened. We hypothesized two computational mechanisms that could have accounted for this. First, learning could have been driven by a Bayesian process where the learner assumed that errors are the result of perturbations that have multiple timescales. In theory, longer ITIs can produce faster learning because passage of time might increase uncertainty, which in turn increases sensitivity to error. Second, error in a trial may result in a trace that decays with time. If the learner continued to sample from the trace during the ITI, then adaptation would increase with increased ITIs. The two models made separate predictions: The Bayesian model predicted that when movements are separated by random ITIs, the learner would learn most from a trial that followed a long time interval. In contrast, the trace model predicted that the learner would learn most from a trial that preceded a long time interval. We performed two experiments to test for these predictions and in both experiments found evidence for the trace model. We suggest that motor error produces an error memory trace that decays with a time constant of about 4 s, continuously promoting adaptation until the next movement.
Address for reprint requests and other correspondence: V. Huang, Johns Hopkins University School of Medicine, 720 Rutland Ave., 416 Traylor Building, Baltimore, MD 21205 (E-mail: vhuang{at}jhu.edu )