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Review
, 128 (7), 1127-1141

The Many Facets of Motor Learning and Their Relevance for Parkinson's Disease

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Review

The Many Facets of Motor Learning and Their Relevance for Parkinson's Disease

Lucio Marinelli et al. Clin Neurophysiol.

Abstract

The final goal of motor learning, a complex process that includes both implicit and explicit (or declarative) components, is the optimization and automatization of motor skills. Motor learning involves different neural networks and neurotransmitters systems depending on the type of task and on the stage of learning. After the first phase of acquisition, a motor skill goes through consolidation (i.e., becoming resistant to interference) and retention, processes in which sleep and long-term potentiation seem to play important roles. The studies of motor learning in Parkinson's disease have yielded controversial results that likely stem from the use of different experimental paradigms. When a task's characteristics, instructions, context, learning phase and type of measures are taken into consideration, it is apparent that, in general, only learning that relies on attentional resources and cognitive strategies is affected by PD, in agreement with the finding of a fronto-striatal deficit in this disease. Levodopa administration does not seem to reverse the learning deficits in PD, while deep brain stimulation of either globus pallidus or subthalamic nucleus appears to be beneficial. Finally and most importantly, patients with PD often show a decrease in retention of newly learned skill, a problem that is present even in the early stages of the disease. A thorough dissection and understanding of the processes involved in motor learning is warranted to provide solid bases for effective medical, surgical and rehabilitative approaches in PD.

Keywords: Declarative learning; Dopamine; Exercise; Implicit learning; Levodopa; Plasticity.

Conflict of interest statement

Conflict of interest

The authors report no financial interests or potential conflicts of interest.

Figures

Figure 1
Figure 1. The development of motor skills
The cognitive stage (top) represents the first step of learning a motor task and encompasses the interpretation of verbal instructions (a declarative process), which should be then transformed into an expert motor act. This stage, usually with high performance variability, is fast and, depending on the task and the ability of the subject (born athletes might have a shorter cognitive stage), may last from minutes to hours. The second phase of learning (center), or motor stage, is mostly implicit with small performance improvements and might persist for days up to years, depending upon the intensity and frequency of training. This stage is complete when implicit mechanisms have taken over. In the third stage, autonomous (bottom) the skill has become automatic, as it can be performed automatically, with little attentional resources and less interference from other simultaneous activities. In this stage, a direct condition-action association is established and can be triggered by cues, implicitly. Performance is faster, effortless, precise, effector-specific with details unavailable to awareness.
Figure 2
Figure 2. Schematic representation of the neural bases of visuo-motor sequence learning: from the visuo-cognitive (left panel, white background) to the motor stage (right panel, gray background)
A. On the left, the visuo-cognitive stage, the first step of sequence learning, includes declarative learning for the acquisition and transformation of visual information in a motor act. This requires the planning of movements as a controlled process based on a vision-centered coordinate system. With practice, there is a switch to the motor stage (right) that implies implicit mechanisms and automatic processes and the change of the coordinate system for motor planning from vision- to motor-centered. In this stage, the performance becomes efficient and effector-specific. B. Following the visual input, in the visuo-cognitive stage, the frontal and parietal associative cortices are involved and their action is linked with the associative regions of the basal ganglia and the cerebellum. The passage to the motor stage is mediated by the activity of the pre-SMA, SMA and pre-motor areas. In the motor stage, the motor cortices operate with a link to the motor areas of the basal ganglia and the cerebellum. Dopamine-based reward systems enhance learning in all stages.
Figure 3
Figure 3. The task determines the characteristics of a movement
In the two arm reaching tasks presented in A. and B., the out-and-back movements are directed to the same targets and are “as fast and as accurate as possible with overlapping strokes”. Moreover, the interval between two consecutive targets is the same (1 s). However, the tasks differ in other instructions and characteristics of target presentation. In A., the time of target presentation is predictable, but not its location. Subjects are instructed to move to the target as soon as it appeared, minimizing reaction time but avoiding anticipation. Thus, movement planning occurs after target presentation (vertical solid line), during the reaction or onset time. Response time is the sum of onset time and movement duration. The temporal profile of the movement’s velocity is usually bell-shaped with the peak occurring around 50% of the movement time. The inset a. illustrates an index of spatial accuracy, the hand path area, which reflects adherence to the instructions of “overlapping strokes” and is computed as the area enclosed between the out and back strokes normalized by the squared path length (Moisello et al. 2008). In B., the target location and its appearance time are known in advance. Instructions are to reach the target at the precise time of its appearance, so that movements must be initiated before it. C. Movements performed in the two tasks differ not only in terms of onset (a.) and response times (dotted thick line in b.), but also in terms of movement duration (b.), peak velocity (e.), spatial errors (c.) and hand path area (d.). In summary, movements performed in the unpredictable condition are faster (duration: ~100 ms less than in the predictable condition) and less accurate: all this in order to save time. However, when target is known in advance, movements are slower and more accurate, allowing for energy saving. Sequence learning implies not only changes in the reaction or onset time but also in movement characteristics (duration, velocity and spatial accuracy), going from unpredictable to predictable condition (adapted from Moisello et al., 2009).
Figure 4
Figure 4. Sequence learning SRT task with arm-reaching tasks
We adopted the R-S-S-S-S-R-R-S-R, which is the same structure used in the classical SRT key-press tasks of “implicit learning” where subjects are not informed about the presence of a sequence. The order of target appearance is random in four blocks (R) and a fixed sequence of 16 elements (=eight complete repetitions) in five blocks (S). Instructions are to move as soon and as fast as possible after the stimulus appearance in all the blocks. The main outcome measure of the classical SRT task is based on the response time (the sum of reaction or onset time and movement time) and is computed as the delta between the response time of the last S and R blocks. The arm reaching task was used to parcel out the changes in onset time from those in movement time (Moisello et al. 2009). The results were replicated with finger movements. 1. In the Intentional Sequence Learning, subjects are informed of the presence of a 16-element repeating sequence in the S blocks, they are instructed to learn the order and at the end of each block, they report the sequence order and a verbal score is computed (Moisello et al. 2009). A. Average onset times in S blocks fell toward negative values and were significantly lower (more than 300 ms) than in R blocks. B. Average Movement time increased in the S blocks. In particular, movement time of the correct anticipatory movements increased by more than 50 ms and was significantly higher than those of R blocks. C. The correct anticipatory movements increased to almost 90% across S blocks. Interestingly, at the end of the first S block all subjects correctly report the entire sequence, while anticipatory movements are only 30% and mean onset time decrement is ~100 ms shorter. This suggests that decreases in onset time, the main drive of response time changes, usually follow and do not precede the development of declarative knowledge of the sequence order. 2. In the Incidental Sequence Learning with arm-reaching movements, the presence of a sequence is not mentioned, like the classical SRT tasks with the key-pressing responses. A. Like in the key-pressing tasks, response time decreases by ~30 ms within the four first “S” blocks with a rebound of ~20 ms in the subsequent two “R” blocks. Interestingly, the response time changes are not equally reflected in onset and movement time. B. Onset time is constant in the first five blocks but increases by an average of 15 ms in R6 compared to S5. These changes were confined to three of the 16 elements (varying from 25 to 40 ms, data not shown, see Moisello et al., 2009), suggesting that a partial order of the sequence might have been identified. C. Movement time continuously decreases across all blocks, with significant difference (~ 50 ms) between the first and the blocks starting from S4. Therefore, the reduction in response time over the first five blocks is mostly due to a reduction in movement time, while its change in the R blocks is mostly due to increase in onset time. D. The number of anticipatory movements increases across S blocks, reaching 5.7% in S8 (~8 out of 128 movements). When such movements are excluded from the analysis, R-S differences in onset time almost vanished (B: gray filled circles). These results, which were replicated with a finger press task (Moisello et al. 2011a), suggest that the response time changes during the so-called “implicit” SRT tasks reflects the development of a declarative, although fragmentary, knowledge of the sequence order.

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