Passive motor learning: Oculomotor adaptation in the absence of behavioral errors

Abstract

Motor adaptation is commonly thought to be a trial-and-error process in which the accuracy of movement improves with repetition of behavior. We challenged this view by testing whether erroneous movements are necessary for motor adaptation. In the eye movement system, the association between movements and errors can be disentangled, since errors in the predicted stimulus trajectory can be perceived even without movements. We modified a smooth pursuit eye movement adaptation paradigm in which monkeys learn to make an eye movement that predicts an upcoming change in target direction. We trained the monkeys to fixate on a target while covertly, an additional target initially moved in one direction and then changed direction after 250 ms. The monkeys showed a learned response to infrequent probe trials in which they were instructed to follow the moving target. Further experiments confirmed that probing learning or residual eye movements during fixation did not drive learning. These results show that motor adaptation can be elicited in the absence of movement and provide an animal model for studying the implementation of passive motor learning. Current models assume that the interaction between movement and error signals underlies adaptive motor learning. Our results point to other mechanisms that may drive learning in the absence of movement.

Significance statement What are the signals that drive learning? Many experimental and theoretical studies have approached this question from the perspective of motor adaptation as it is both extremely relevant to everyday life and allows for tight experimental control. Motor adaptation is thought to be a gradual process in which errors in behavior are corrected. Here we challenged this view and developed a behavioral paradigm for studying whether movement is necessary for motor adaptation. We found that motor adaptive learning can be elicited in the absence of movement, thus suggesting that motor adaptation has a crucial passive component.