Paradoxical adaptation of successful movements: the crucial role of internal error signals

Abstract Visuo-motor adaptation has been classically studied using movements aimed at visual targets with visual feedback. In this type of experimental design, the respective roles of the different error signals cannot be fully disentangled. Here, we show that visuo-motor adaptation occurs despite the terminal success of the action and the compensation of the external error by a jump of the visual target. By using three grasping task conditions we manipulated the retinal error signal between the seen hand and the target (external error) and the conflict between the hand’s visual reafference and either the proprioceptive or the efference copy signal (internal error), in order to estimate their respective roles in prism adaptation. In all conditions, subjects were asked to rapidly grasp an object. In the classical ‘Prism’ condition the object was stationary, which provided both external and internal errors. In the ‘Prism & Jump’ condition, at movement onset the object was suddenly displaced (jump) toward its virtual image location (visually displaced by the prism) which also corresponded to the location where the movement was planned to and executed through prisms. This jump therefore cancelled the external error (between the seen target and the seen hand), whereas the internal error (between the seen hand and the expected visual reafference of the hand, or between the seen hand and the hand felt by proprioception) was unchanged (because it is independent of the presence of the goal). In the ‘Jump’ condition, the movement was planned and executed without prismatic goggles and consequently with no internal error (no difference between where the hand visual reafference is expected to be and where it actually is), but the object was suddenly displaced at movement onset by a displacement equivalent to a prism shift which provided an external error. The ‘Prism’ and ‘Prism & Jump’ conditions exhibited similar aftereffects, whereas no aftereffect was observed in the ‘Jump’ condition. These results suggest that successful actions can be subjected to adaptation and that internal error is the only signal necessary to elicit true visuomotor adaptation characterized by context-independent generalization.