Robust Control in Human Reaching Movements: A Model-Free Strategy to Compensate for Unpredictable Disturbances

J Neurosci. 2019 Oct 9;39(41):8135-8148. doi: 10.1523/JNEUROSCI.0770-19.2019. Epub 2019 Sep 5.

Abstract

Current models of motor learning suggest that multiple timescales support adaptation to changes in visual or mechanical properties of the environment. These models capture patterns of learning and memory across a broad range of tasks, yet do not consider the possibility that rapid changes in behavior may occur without adaptation. Such changes in behavior may be desirable when facing transient disturbances, or when unpredictable changes in visual or mechanical properties of the task make it difficult to form an accurate model of the perturbation. Whether humans can modulate control strategies without an accurate model of the perturbation remains unknown. Here we frame this question in the context of robust control (H -control), a control strategy that specifically considers unpredictable disturbances by increasing initial movement speed and feedback gains. Correspondingly, we demonstrate in two human reaching experiments including males and females that the occurrence of a single unpredictable disturbance led to an increase in movement speed and in the gain of rapid feedback responses to mechanical disturbances on subsequent movements. This strategy reduced perturbation-related motion regardless of the direction of the perturbation. Furthermore, we found that changes in the control strategy were associated with co-contraction, which amplified the gain of muscle responses to both lengthening and shortening perturbations. These results have important implications for studies on motor adaptation because they highlight that trial-by-trial changes in limb motion also reflected changes in control strategies dissociable from error-based adaptation.SIGNIFICANCE STATEMENT Humans and animals use internal representations of movement dynamics to anticipate the impact of predictable disturbances. However, we are often confronted with transient or unpredictable disturbances, and it remains unknown whether and how the nervous system handles these disturbances over fast time scales. Here we hypothesized that humans can modulate their control strategy to make reaching movements less sensitive to perturbations. We tested this hypothesis in the framework of robust control, and found changes in movement speed and feedback gains consistent with the model predictions. These changes impacted participants' behavior on a trial-by-trial basis. We conclude that compensation for disturbances over fast time scales involves a robust control strategy, which potentially plays a key role in motor planning and execution.

Keywords: motor adaptation; optimal feedback control; reaching control; robust control.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Psychological
  • Adult
  • Algorithms
  • Arm / innervation
  • Arm / physiology
  • Electromyography
  • Feedback, Psychological
  • Female
  • Humans
  • Learning / physiology*
  • Male
  • Middle Aged
  • Models, Neurological
  • Muscle, Skeletal / physiology
  • Psychomotor Performance / physiology*
  • Reaction Time
  • Young Adult