Abstract

Previous studies support the notion that sensorimotor learning involves multiple processes. We investigated the neuronal basis of these processes by recording single-unit activity in motor cortex of non-human primates (Macaca fascicularis), during adaptation to force-field perturbations. Perturbed trials (reaching to one direction) were practiced along with unperturbed trials (to other directions). The number of perturbed trials relative to the unperturbed ones was either low or high, in two separate practice schedules. Unsurprisingly, practice under high-rate resulted in faster learning with more pronounced generalization, as compared to the low-rate practice. However, generalization and retention of behavioral and neuronal effects following practice in high-rate were less stable; namely, the faster learning was forgotten faster. We examined two subgroups of cells and showed that, during learning, the changes in firing-rate in one subgroup depended on the number of practiced trials, but not on time. In contrast, changes in the second subgroup depended on time and practice; the changes in firing-rate, following the same number of perturbed trials, were larger under high-rate than low-rate learning. After learning, the neuronal changes gradually decayed. In the first subgroup, the decay pace did not depend on the practice rate, whereas in the second subgroup, the decay pace was greater following high-rate practice. This group shows neuronal representation that mirrors the behavioral performance, evolving faster but also decaying faster at learning under high-rate, as compared to low-rate. The results suggest that the stability of a new learned skill and its neuronal representation are affected by the acquisition schedule.

Highlights

  • In sensorimotor learning, the brain remaps a sensory instruction to a motor command when interactions with the environment require it

  • We found support to our hypothesis by the different dynamics of learning and its neuronal representations that evolved by the different practice schedules

  • The high rate practice resulted in a faster acquisition

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Summary

Introduction

The brain remaps a sensory instruction to a motor command when interactions with the environment require it. In a commonly used adaptation paradigm, a force-field is used to perturb arm reaching movements by pushing the hand away from the target, causing the hand to deviate from its planned trajectory. Many studies have shown that humans and monkeys adapt to force-field perturbations, and that their trajectories straighten with practice [1,2,3,4,5]. To re-optimize the movement [6] and minimize kinematic error and effort [7], the brain needs to correctly anticipate the force-field and modify the motor command [8,9]. These two stages are hypothesized to reflect dynamical neuronal subsystems with multiple timescales [15,16]

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