Providing explicit information disrupts implicit motor learning after basal ganglia stroke

Abstract

Despite their purported neuroanatomic and functional isolation, empirical evidence suggests that sometimes conscious explicit processes can influence implicit motor skill learning. Our goal was to determine if the provision of explicit information affected implicit motor-sequence learning after damage to the basal ganglia. Individuals with stroke affecting the basal ganglia (BG) and healthy controls (HC) practiced a continuous implicit motor-sequencing task; half were provided with explicit information (EI) and half were not (No-EI). The focus of brain damage for both BG groups was in the putamen. All of the EI participants were at least explicitly aware of the repeating sequence. Across three days of practice, explicit information had a differential effect on the groups. Explicit information disrupted acquisition performance in participants with basal ganglia stroke but not healthy controls. By retention (day 4), a dissociation was apparent--explicit information hindered implicit learning in participants with basal ganglia lesions but aided healthy controls. It appears that after basal ganglia stroke explicit information is less helpful in the development of the motor plan than is discovering a motor solution using the implicit system alone. This may be due to the increased demand placed on working memory by explicit information. Thus, basal ganglia integrity may be a crucial factor in determining the efficacy of explicit information for implicit motor-sequence learning.

Figure 1

Representations of strokes reconstructed by transcribing lesions from MRI or CT scans onto axial templates using MRIcro software (Rorden 2003). All lesions were reconstructed on the left for illustration purposes. Standard slices are 2-mm thick and displayed from superior (top left) to inferior (bottom right). The color bar represents overlap density (violet = no overlap [0%], red = maximal overlap [100%]). The focus of overlap for the BG EI group was in the putamen (Talairach coordinates -21, 6, 11); the focus of overlap for the BG No-EI group was also in the putamen (Talairach coordinates -21, 1, 12).

Figure 2

Change in tracking error for the groups across three days of practice. The zero line reflects performance on random tracking sequences. Data below this line reflects reductions (improvements) in tracking error for repeated sequences relative to random pattern tracking. Error bars are standard error of the mean (SEM). EI group is closed lines and symbols, No-EI group is dashed lines and open symbols.(A) Healthy Control Groups. Both groups (HC EI and No-EI) benefited from practice regardless of the presence of explicit information. (B) Basal Ganglia Groups. Across practice both BG EI and No-EI showed decreased tracking error. However, the BG EI group's performance was poorer (less change) than that of the No-EI group's.

Figure 3

Learning at the retention test is demonstrated by larger change scores or greater change in tracking error for the learned sequence (relative to random). Explicit information had the opposite effect on the two groups. The HC EI group was aided by explicit information, while the BG EI group was not. HC groups are in solid circles and lines, BG groups are in open circles and dashed lines. Error bars are SEM.

Figure 4

Change in time lag of tracking across three days of practice and at retention. EI group is shown in solid bars; stripped bars represent No-EI group data. Error bars are SEM. (A) Healthy Control Group. Both HC groups decreased their time lag across acquisition. However, the EI group decreased time lag of tracking significantly more than the No-EI group. (B) Basal Ganglia Group. Across practice both BG EI and No-EI showed decreased time lag of tracking; however, this difference was not statistically reliable.

Figure 5

Change in tracking accuracy across three days of practice and at retention. EI group is shown in solid bars; stripped bars represent No-EI group data. Error bars are SEM. All participants improved their tracking accuracy with practice and there were no group differences. (A) Healthy Control Groups, (B) Basal Ganglia Groups.