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.functional MRI ͉ human ͉ subthalamic nucleus T here is now ample evidence from a number of sources that indicates that the basal ganglia are implicated in the formation of motor skills (1). In human studies using brain-imaging techniques, for example, changes of activity have been observed in the basal ganglia at different stages of the acquisition of motor abilities. Decreases of activity in the basal ganglia were reported during the early phase of trial-and-error learning of sequential movements (2). Using a similar task, Toni et al. (3) also reported a decrease of activity in the caudate nucleus, pre-supplementary motor area (SMA), and prefrontal cortex during the first hour of the acquisition process (3). By contrast, studies of implicit motor learning showed that the striatum was more active when subjects reached asymptotic performance, thus suggesting that this structure may be critical for the long-term storage of motor sequences (4-7). However, other investigations (8, 9) failed to document the presence of a greater increase in activity during the execution of well-learned sequential movements compared with the early learning phase.Although still conjectural, differences in the patterns of activation described above may reflect the involvement of different cortico-basal ganglia circuits during the acquisition process, because it is now known that cortical areas project to the striatum in separate associative, premotor, and sensorimotor circuits (10, 11). Indeed, previous imaging works have shown that rostral striatal areas are activated during learning of new motor sequences (2, 3) whereas the execution of well learned sequential movements invo...

Motor skill learning depends on protein synthesis in the dorsal striatum after training

“…Imaging studies show changes in the activation of the dorsal striatum (Lehericy et al 2005) and electrophysiological experiments in animals show evidence for reorganization of corticostriatal circuits during early stages of motor skill learning (Brasted and Wise 2004;Costa et al 2004, Yin et al 2009). …”

“…The sensorimotor cortex interacts with the basal ganglia (Pisani et al 2005;Costa 2007), the cerebellum and other sensory as well as associative cortical areas . Imaging studies in humans demonstrate activation of the striatum during skill learning (Seitz et al 1990; Lehericy et al 2005;Wachter et al 2009). These studies also suggest that striatal circuits undergo plastic modifications as neuronal activation shifts from the associative, rostrodorsal region to the sensorimotor, caudoventral region of the putamen (Lehericy et al 2005) in association with learning a new finger tapping sequence.…”

“…Imaging studies in humans demonstrate activation of the striatum during skill learning (Seitz et al 1990; Lehericy et al 2005;Wachter et al 2009). These studies also suggest that striatal circuits undergo plastic modifications as neuronal activation shifts from the associative, rostrodorsal region to the sensorimotor, caudoventral region of the putamen (Lehericy et al 2005) in association with learning a new finger tapping sequence. Evidence for this shift of activation was also found in non-human primates using single cell recordings (Miyachi et al 2002).…”

Probabilistic inference under time pressure leads to a cortical-to-subcortical shift in decision evidence integration

“…Some studies, additionally, have reported enhanced post-learning subcortical processing (Doyon et al, 2009;Lehericy et al, 2005;Van Turennout et al, 2003), although the results are rather mixed (see Ashby et al, 2010 for a detailed discussion). To examine changes in cortical and subcortical activity over time, we divided our experiment into four different sets (120 trials/set, 2 sets/phase), each consisting of a complete set of unique stimulus combinations, and conducted an additional GLM analysis.…”

The Crossed Projection to the Striatum in Two Species of Monkey and in Humans: Behavioral and Evolutionary Significance

“…also raised by McGuire et al (1991). The anterior portion of the striatum, connected with prefrontal and premotor structures, is activated bilaterally during the acquisition of unilateral motor tasks, while the posterior part, involved in sensorimotor functions, is activated at advanced stages of learning (Lehéricy et al 2005). The learning and execution of movements might require the temporal coordination, with minimal delays between the hemispheres that the bilateral projection affords.…”