Neural signatures of reward and sensory error feedback processing in motor learning

Abstract

At least two distinct processes have been identified by which motor commands are adapted according to movement-related feedback: reward-based learning and sensory error-based learning. In sensory error-based learning, mappings between sensory targets and motor commands are recalibrated according to sensory error feedback. In reward-based learning, motor commands are associated with subjective value, such that successful actions are reinforced. We designed two tasks to isolate reward- and sensory error-based motor adaptation, and we used electroencephalography in humans to identify and dissociate the neural correlates of reward and sensory error feedback processing. We designed a visuomotor rotation task to isolate sensory error-based learning that was induced by altered visual feedback of hand position. In a reward learning task, we isolated reward-based learning induced by binary reward feedback that was decoupled from the visual target. A fronto-central event-related potential called the feedback-related negativity (FRN) was elicited specifically by binary reward feedback but not sensory error feedback. A more posterior component called the P300 was evoked by feedback in both tasks. In the visuomotor rotation task, P300 amplitude was increased by sensory error induced by perturbed visual feedback and was correlated with learning rate. In the reward learning task, P300 amplitude was increased by reward relative to nonreward and by surprise regardless of feedback valence. We propose that during motor adaptation the FRN specifically reflects a reward-based learning signal whereas the P300 reflects feedback processing that is related to adaptation more generally. NEW & NOTEWORTHY We studied the event-related potentials evoked by feedback stimuli during motor adaptation tasks that isolate reward- and sensory error-based learning mechanisms. We found that the feedback-related negativity was specifically elicited by binary reward feedback, whereas the P300 was observed in both tasks. These results reveal neural processes associated with different learning mechanisms and elucidate which classes of errors, from a computational standpoint, elicit the feedback-related negativity and P300.