Distinct basal ganglia territories are engaged in early and advanced motor sequence learning

Abstract

In this study, we used functional MRI (fMRI) at high field (3T) to track the time course of activation in the entire basal ganglia circuitry, as well as other motor-related structures, during the explicit learning of a sequence of finger movements over a month of training. Fourteen right-handed healthy volunteers had to practice 15 min daily a sequence of eight moves using the left hand. MRI sessions were performed on days 1, 14 and 28. In both putamen, activation decreased with practice in rostrodorsal (associative) regions. In contrast, there was a significant signal increase in more caudoventral (sensorimotor) regions of the putamen. Subsequent correlation analyses between signal variations and behavioral variables showed that the error rate (movement accuracy) was positively correlated with signal changes in areas activated during early learning, whereas reaction time (movement speed) was negatively correlated with signal changes in areas activated during advanced learning stages, including the sensorimotor putamen and globus pallidus. These results suggest the possibility that motor representations shift from the associative to the sensorimotor territories of the striato-pallidal complex during the explicit learning of motor sequences, suggesting that motor skills are stored in the sensorimotor territory of the basal ganglia that supports a speedy performance.

Figures

Fig. 1.

Activation patterns in the basal ganglia and cerebellum. (A Upper) Activation maps obtained in the putamen superimposed on a coronal T1-weighted image. There was a progressive activation decrease in the dorsal part of the putamen (arrows) and an increase in a more ventrolateral area (arrowheads) bilaterally, which persisted after 4 weeks of training. (Lower) Percentage signal increase ± SEM averaged across all subjects for each run of the trained sequence confirmed the activation decrease in the dorsal putamen and increase in the ventral putamen (RM-ANOVA). (B Top) Activation maps obtained in the SN (arrowhead, coronal level y = -20 on T2 day 1) and STN (arrows, axial level z = -3 on T1 day 1 and T5 day 28) superimposed on EPI images. During session 1, STN activation was observed during the first run of T-sequence (T1). After 4 weeks of training, these areas were no more activated during the T-sequence. There was no significant signal change in the SN across runs. (Bottom) Signal-to-time curves ± SEM in the STN averaged across all subjects and epochs confirm the activation decrease (RM-ANOVA). (C Left) Activation maps obtained in the cerebellum during the T-sequence (T1 on day 1 and T5 on day 28). Activation in the lateral cerebellar hemispheres, the left DN, and the pons decreased with training. (Right) Percentage signal increase ± SEM averaged across all subjects for each run of the trained sequence in the left and right DN. In the right DN, activation increased transiently during T2 (10 min of practice) and returned to pretraining values. All activation maps are corrected for cluster extent at P < 0.05 (height threshold P < 0.0001).

Fig. 2.

Multiple regression analysis between signal variation across all runs of all MR sessions and behavioral variables (errors and reaction times). Activation maps are superimposed to a T1-weighted (Upper) or an EPI (Lower) template. Shown are whole brain (A) (P < 0.001) and basal ganglia (B)[P < 0.01; two axial views (Left) and two coronal views (Right)] analysis showing areas in which signal changes positively correlated with the number of errors (orange scale) and negatively correlated with reaction times (blue scale). Errors were positively correlated with signal changes in areas activated during early learning. Reaction times were negatively correlated with signal changes in areas activated during late learning.