Critical neural substrates for correcting unexpected trajectory errors and learning from them

Abstract

Our proficiency at any skill is critically dependent on the ability to monitor our performance, correct errors and adapt subsequent movements so that errors are avoided in the future. In this study, we aimed to dissociate the neural substrates critical for correcting unexpected trajectory errors and learning to adapt future movements based on those errors. Twenty stroke patients with focal damage to frontal or parietal regions in the left or right brain hemispheres and 20 healthy controls performed a task in which a novel mapping between actual hand motion and its visual feedback was introduced. Only patients with frontal damage in the right hemisphere failed to correct for this discrepancy during the ongoing movement. However, these patients were able to adapt to the distortion such that their movement direction on subsequent trials improved. In contrast, only patients with parietal damage in the left hemisphere showed a clear deficit in movement adaptation, but not in online correction. Left frontal or right parietal damage did not adversely impact upon either process. Our findings thus identify, for the first time, distinct and lateralized neural substrates critical for correcting unexpected errors during ongoing movements and error-based movement adaptation.

Figure 1

Lesion overlay. Overlap of lesion location in at least 60 (blue), 80 (red) and 100 (yellow) per cent of patients in the groups with left frontal damage, right frontal damage, left parietal damage and right parietal damage.

Figure 2

Comparison of movement profiles for representative subjects in the right normal controls (RNC, black), and right frontal damage (RFD) and right parietal damage (RPD, grey) groups. (A) Last eight trials (last cycle) of the baseline session; (B) First cycle of movements following exposure to the visuomotor rotation (exposure session). (C) Last cycle of movements of the exposure session and (D) first cycle of the after-effect session when the visuomotor rotation was removed.

Figure 3

Performance across all subjects in the right normal controls (RNC, black) and groups with right frontal damage (RFD) and right parietal damage (RPD, grey) during all cycles of the exposure session. (A) Mean ± SE initial direction error. Inset shows the initial direction error on the first cycle of the after-effect session across all subjects in each group. (B) Mean ± SE hand path curvature; (C) mean ± SE final position error.

Figure 4

Amount of correction and its relationship to initial direction error in the right normal controls (RNC, black), and groups with right frontal damage (RFD) and right parietal damage (RPD, grey). (A) Mean ± SE magnitude of correction during the first and last cycles of the exposure session. (B) Relationship between initial direction error and the amount of correction for the representative subjects in Fig. 2. (C) Mean ± SE correction gain (slope of this relationship) across all subjects in the three groups.

Figure 5

Comparison of movement profiles for representative subjects in the left normal controls (LNC, black), and groups with left frontal damage (LFD) and left parietal damage (LPD, grey). (A) Last eight trials (last cycle) of the baseline session. (B) First cycle of movements following exposure to the visuomotor rotation (exposure session). (C) Last cycle of movements of the exposure session and (D) first cycle of the after-effect session when the visuomotor rotation was removed.

Figure 6

Performance across all subjects in the left normal controls (LNC, black), and left frontal damage (LFD) and left parietal damage (LPD, grey) groups during all cycles of the exposure session. (A) Mean ± SE initial direction error. Inset shows the initial direction error on the first cycle of the after-effect session across all subjects in each group. (B) Mean ± SE hand path curvature. (C) Mean ± SE final position error.

Figure 7

Amount of correction and its relationship to initial direction error in the left normal controls (LNC, black), and groups with left frontal damage (LFD) and left parietal damage (LPD, grey). (A) Mean ± SE magnitude of correction during the first and last cycles of the exposure session. (B) Relationship between initial direction error and the amount of correction for the representative subjects in Fig. 5. (C) Mean ± SE correction gain (slope of this relationship) across all subjects in the three groups.