Learning and consolidation of visuo-motor adaptation in Parkinson's disease

Department of Physiology & Pharmacology, CUNY Medical School, New York, NY 100031, USA.
Parkinsonism & Related Disorders (Impact Factor: 3.97). 05/2008; 15(1):6-11. DOI: 10.1016/j.parkreldis.2008.02.012
Source: PubMed


We have previously shown in normal subjects that motor adaptation to imposed visual rotation is significantly enhanced when tested few days later. This occurs through a process of sleep-dependent memory consolidation. Here we ascertained whether patients with Parkinson's disease (PD) learn, improve, and retain new motor skills in the same way as normal subjects. We tested 16 patients in early stages of PD and 21 control subjects over two days. All subjects performed reaching movements on a digitizing tablet. Vision of the limb was precluded with an opaque screen; hand paths were shown on the screen with the targets' position. Unbeknownst to the subjects, the hand path on the screen was rotated by 30 degrees . In experiment 1, patients taking dopaminergic treatment and controls adapted to rotation with targets appearing in an unpredictable order. In experiment 2, drug-naïve patients and controls adapted to rotation in a less challenging task where target's appearance was predictable. Patients and controls made similar movements and adapted to rotation in the same way. However, when tested again over the following days, controls' performance significantly improved compared to training, while patients' performance did not. This lack of consolidation, which is present in the early stages of the disease and is independent from therapy, may be due to abnormal homeostatic processes that occur during sleep.

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Available from: Marco Bove, Oct 04, 2015
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    • "With regards to the pattern of within and between session performance, it appears that different processes may be underlying these different stages of motor skill learning. A similar pattern of intact learning within sessions, but impaired retention between-sessions, has been reported previously in individuals with PD (Bédard and Sanes, 2011; Leow et al., 2012; Marinelli et al., 2009; Mochizuki-Kawai et al., 2004). In terms of processes, it has been argued that the cortico-cerebellar circuit along with the hippocampus and frontal regions are primarily involved in early stages of learning and therefore, may support initial skill learning, but that the striatal system is particularly critical for long-term retention of motor skills after initial training (Albouy et al., 2013; Doyon et al., 2009; Mochizuki-Kawai et al., 2004). "
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    ABSTRACT: Previous research suggests that different aspects of tool knowledge are mediated by different memory systems. It is believed that tool attributes (e.g., function, color) are represented as declarative memory while skill learning is supported by procedural memory. It has been proposed that other aspects (e.g., skilled tool use) may rely on an interaction of both declarative and procedural memory. However, the specific form of procedural memory underlying skilled tool use and the nature of interaction between declarative and procedural memory systems remain unclear. In the current study, individuals with Parkinson's disease (PD) and healthy controls were trained over 2 sessions, 3 weeks apart, to use a set of novel complex tools. They were also tested on their ability to recall tool attributes as well as their ability to demonstrate grasp and use of the tools to command. Results showed that, compared to controls, participants with PD showed intact motor skill acquisition and tool use to command within sessions, but failed to retain performance across sessions. In contrast, people with PD showed equivalent recall of tool attributes and tool grasping relative to controls, both within and across sessions. Current findings demonstrate that the frontal-striatal network, compromised in PD, mediates long-term retention of motor skills. Intact initial skill learning raises the possibility of compensation from declarative memory for frontal-striatal dysfunction. Lastly, skilled tool use appears to rely on both memory systems which may reflect a cooperative interaction between the two systems. Current findings regarding memory representations of tool knowledge and skill learning may have important implications for delivery of rehabilitation programs for individuals with PD.
    Neuropsychologia 11/2014; 66. DOI:10.1016/j.neuropsychologia.2014.11.005 · 3.30 Impact Factor
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    • "The idea of instance-reliant learning can account for the phenomenon of savings by suggesting that the instances obtained during the initial learning period are available to facilitate relearning, even after the algorithm developed during initial training may no longer be available due to unlearning or forgetting. The basal ganglia may also be involved in instance–reliant learning, because studies have reported that despite their intact ability to adapt to novel visuomotor conditions, parkinsonian patients show lack of savings (Marinelli et al., 2009; Bédard & Sanes, 2011; Leow, Loftus, & Hammond, 2012). It is plausible that parkinsonian patients can adapt to the novel condition as well as controls by employing algorithmic learning, whereas their savings is absent because instance–reliant learning is impaired in these patients. "
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    ABSTRACT: Learning a visumotor adaptation task with one arm typically facilitates subsequent performance with the other. The extent of transfer across the arms, however, is generally much smaller than that across different conditions within the same arm. This may be attributed to a possibility that intralimb transfer involves both algorithmic and instance–reliant learning, whereas interlimb transfer only involves algorithmic learning. Here, we investigated whether prolonged training with one arm could facilitate subsequent performance with the other arm to a greater extent, by examining the effect of varying lengths of practice trials on the extent of interlimb transfer. We had 18 subjects adapt to a 30° visuomotor rotation with the left arm first (training), then with the right arm (transfer). During the training session, the subjects reached toward multiple targets for 160, 320 or 400 trials; during the transfer session, all subjects performed the same task for 160 trials. Our results revealed substantial initial transfer from the left to the right arm in all three conditions. However, neither the amount of initial transfer nor the rate of adaptation during the transfer session was significantly different across the conditions, indicating that the extent of transfer was similar regardless of the length of initial training. Our findings suggest that interlimb transfer of visuomotor adaptation may only occur through algorithmic learning, which is effector independent, and that prolonged training may only have beneficial effects when instance–reliant learning, which is effector dependent, is also involved in the learning process.
    Brain and Cognition 10/2014; 91:95–99. DOI:10.1016/j.bandc.2014.09.004 · 2.48 Impact Factor
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    • "Reinforcement processes that are known to be impaired in Parkinson's disease (Frank, 2005) were found to impair both savings (Marinelli et al., 2008; B edard & Sanes, 2011; Leow et al., 2012, 2013) and anterograde interference (Leow et al., 2013). Furthermore , savings was evident despite adaptation to opposing perturbations when target locations were separated such that the ideally adapted movements for the opposing perturbations had a common reinforced direction (Huang et al., 2011). "
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    ABSTRACT: Retention of motor adaptation is evident in savings, where initial learning improves subsequent learning, and anterograde interference, where initial learning impairs subsequent learning. Previously, we proposed that use-dependent movement biases induced by movement repetition contribute to anterograde interference, but not to savings. Here, we evaluate this proposal by limiting or extending movement repetition while stimulating the motor cortex (M1) with anodal transcranial direct current stimulation (tDCS), a brain stimulation technique known to increase use-dependent plasticity when applied during movement repetition. Participants first adapted to a counterclockwise rotation of visual feedback imposed either abruptly (extended repetition) or gradually (limited repetition) in a first block (A1), during which either sham or anodal tDCS (2 mA) was applied over M1. Anterograde interference was then assessed in a second block (B) with a clockwise rotation, and savings in a third block (A2) with a counterclockwise rotation. Anodal M1 tDCS elicited more anterograde interference than sham stimulation with extended but not with limited movement repetition. Conversely, anodal M1 tDCS did not affect savings with either limited or extended repetition of the adapted movement. Crucially, the effect of anodal M1 tDCS on anterograde interference did not require large errors evoked by an abrupt perturbation schedule, as anodal M1 tDCS combined with extended movement repetition within a gradual perturbation schedule similarly increased anterograde interference but not savings. These findings demonstrate that use-dependent plasticity contributes to anterograde interference but not to savings.
    European Journal of Neuroscience 08/2014; 40(8). DOI:10.1111/ejn.12699 · 3.18 Impact Factor
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