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

Abstract

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.

Motor learning in childhood reveals distinct mechanisms for memory retention and re-learning

“…Likewise, the caudate, putamen and pallidum all show protracted development during childhood (Østby et al 2009), and there is evidence that the basal ganglia plays a role in motor adaptation and the formation of longer-term motor memories (Marinelli et al 2009;Bédard and Sanes 2011). In individuals with Parkinson's disease, re-learning (savings) of an upper extremity movement is attenuated (Marinelli et al 2009;Bédard and Sanes 2011), similar to the young children in this study. However, savings of split-belt walking was recently found to be intact in Parkinson's disease (Roemmich et al 2014).…”

“…This timeline corresponds with the protracted maturation of the cerebellum-whole cerebellar volume does not peak until the early teenage years (Caviness et al 1996;Tiemeier et al 2010). Likewise, the caudate, putamen and pallidum all show protracted development during childhood (Østby et al 2009), and there is evidence that the basal ganglia plays a role in motor adaptation and the formation of longer-term motor memories (Marinelli et al 2009;Bédard and Sanes 2011). In individuals with Parkinson's disease, re-learning (savings) of an upper extremity movement is attenuated (Marinelli et al 2009;Bédard and Sanes 2011), similar to the young children in this study.…”

Formation of model-free motor memories during motor adaptation depends on perturbation schedule

“…Such a reward prediction error could be used either to build the model-free motor memory through reinforcement learning (Darshan et al 2014;Izawa and Shadmehr 2011;Madelain et al 2011) independently of the adaptation of an internal model (Izawa et al 2012) or to tag the model-free motor memory in order to facilitate its recall when another reward prediction error is experienced (Shmuelof et al 2012). The involvement of reward prediction would also be consistent with the absence of savings observed in Parkinson's disease patients (Bédard and Sanes 2011;Leow et al 2012Leow et al , 2013Marinelli et al 2009). …”

Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

“…A further piece of evidence in support of the recall hypothesis is that Parkinson's disease (PD) patients are typically unimpaired in initial adaptation to a perturbation (Stern et al 1988;Gutierrez-Garralda et al 2013;Leow et al 2013;Mongeon et al 2013) but show impaired savings during readaptation (Marinelli et al 2009;Bédard and Sanes 2011;Leow et al 2013). This dissociation suggests that initial adaptation and savings depend on different processes.…”