An explicit strategy prevails when the cerebellum fails to compute movement errors

Abstract

In sensorimotor adaptation, explicit cognitive strategies are thought to be unnecessary because the motor system implicitly corrects performance throughout training. This seemingly automatic process involves computing an error between the planned movement and actual feedback of the movement. When explicitly provided with an effective strategy to overcome an experimentally induced visual perturbation, people are immediately successful and regain good task performance. However, as training continues, their accuracy gets worse over time. This counterintuitive result has been attributed to the independence of implicit motor processes and explicit cognitive strategies. The cerebellum has been hypothesized to be critical for the computation of the motor error signals that are necessary for implicit adaptation. We explored this hypothesis by testing patients with cerebellar degeneration on a motor learning task that puts the explicit and implicit systems in conflict. Given this, we predicted that the patients would be better than controls in maintaining an effective strategy assuming strategic and adaptive processes are functionally and neurally independent. Consistent with this prediction, the patients were easily able to implement an explicit cognitive strategy and showed minimal interference from undesirable motor adaptation throughout training. These results further reveal the critical role of the cerebellum in an implicit adaptive process based on movement errors and suggest an asymmetrical interaction of implicit and explicit processes.

Figures

Fig. 1

a, b Mean trajectory during the baseline (black) and strategy-only (orange) blocks for a representative control participant (a) and patient with ataxia (b). Movements are approximately straight and directed toward the cued green target in the baseline block and to the adjacent (45°CW) blue “aiming target” in the strategy-only block. Shading indicates the 95% confidence intervals of the trajectories. c, d Target errors for these two participants across the phases of the experiment: second baseline phase (black), rotation phase (blue; between vertical dashed lines), washout without feedback (magenta), and washout with feedback (cyan). The rotation was turned on without warning for two movements (red) before the participants were instructed to use a strategy to counteract the rotation. Lower Participants performed 244 movements throughout seven phases of the experiment

Fig. 2

a Mean target error across the experimental session for each group (filled = ataxic; open = controls). The color coding is the same as in Fig. 1. b Drift rate as estimated from regression analysis over the rotation + strategy phase. The individual data are shown as empty circles for the control participants (left) and filled circles for the individuals with ataxia (right)