Learning from Sensory and Reward Prediction Errors during Motor Adaptation

Abstract

Voluntary motor commands produce two kinds of consequences. Initially, a sensory consequence is observed in terms of activity in our primary sensory organs (e.g., vision, proprioception). Subsequently, the brain evaluates the sensory feedback and produces a subjective measure of utility or usefulness of the motor commands (e.g., reward). As a result, comparisons between predicted and observed consequences of motor commands produce two forms of prediction error. How do these errors contribute to changes in motor commands? Here, we considered a reach adaptation protocol and found that when high quality sensory feedback was available, adaptation of motor commands was driven almost exclusively by sensory prediction errors. This form of learning had a distinct signature: as motor commands adapted, the subjects altered their predictions regarding sensory consequences of motor commands, and generalized this learning broadly to neighboring motor commands. In contrast, as the quality of the sensory feedback degraded, adaptation of motor commands became more dependent on reward prediction errors. Reward prediction errors produced comparable changes in the motor commands, but produced no change in the predicted sensory consequences of motor commands, and generalized only locally. Because we found that there was a within subject correlation between generalization patterns and sensory remapping, it is plausible that during adaptation an individual's relative reliance on sensory vs. reward prediction errors could be inferred. We suggest that while motor commands change because of sensory and reward prediction errors, only sensory prediction errors produce a change in the neural system that predicts sensory consequences of motor commands.

Author Summary

It is thought that motor adaptation relies on sensory prediction errors to form an estimate of the perturbation. Here, we present evidence that motor adaptation can be driven by both sensory and reward prediction errors. We found that learning from sensory prediction error altered the predicted consequences of motor commands, leaving behind a sensory remapping, whereas learning from reward prediction error produced comparable change in motor commands, but did not produce a sensory remapping. It is possible that the neural basis of learning from sensory and reward prediction errors are distinct because they produce different generalization patterns.