Basal ganglia-dependent processes in recalling learned visual-motor adaptations

Abstract

Humans learn and remember motor skills to permit adaptation to a changing environment. During adaptation, the brain develops new sensory-motor relationships that become stored in an internal model (IM) that may be retained for extended periods. How the brain learns new IMs and transforms them into long-term memory remains incompletely understood since prior work has mostly focused on the learning process. A current model suggests that basal ganglia, cerebellum, and their neocortical targets actively participate in forming new IMs but that a cerebellar cortical network would mediate automatization. However, a recent study (Marinelli et al. 2009) reported that patients with Parkinson's disease (PD), who have basal ganglia dysfunction, had similar adaptation rates as controls but demonstrated no savings at recall tests (24 and 48 h). Here, we assessed whether a longer training session, a feature known to increase long-term retention of IM in healthy individuals, could allow PD patients to demonstrate savings. We recruited PD patients and age-matched healthy adults and used a visual-motor adaptation paradigm similar to the study by Marinelli et al. (2009), doubling the number of training trials and assessed recall after a short and a 24-h delay. We hypothesized that a longer training session would allow PD patients to develop an enhanced representation of the IM as demonstrated by savings at the recall tests. Our results showed that PD patients had similar adaptation rates as controls but did not demonstrate savings at both recall tests. We interpret these results as evidence that fronto-striatal networks have involvement in the early to late phase of motor memory formation, but not during initial learning.

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 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.…”

“…Alternatively, long-term motor memory might be mediated by an implicit or procedural memory for a component of learning that was initially explicit or declarative. This process of transition from one type of memory to another has been suggested as a general mechanism for skill acquisition (Fitts 1964;Anderson 1982). If visuomotor adaptation serves as an example of the initial, explicit stage of this process, one task that may serve as a model for this process following more practice is adjustment of grip and load forces for lifting objects of unusual densities.…”

Dissecting the Links Between Cerebellum and Dystonia

“…Within traditional motor adaptation paradigms, adaptive learning is assessed by the degree of the after-effect observed during a de-adaptation task and the amount of savings upon a second exposure to the adaptation task (i.e., a readaptation task). In context of the present study, locomotor adaptation is a process during which changes in locomotor output are stabilized over time by the central nervous system's incorporation of feed-forward predictive motor actions and sensorimotor feedback [13][14][15][16][17][18][19]. While locomotor adaptation has previously been induced within the laboratory setting using a variety of different methods, Hoffland et al utilize a locomotor adaptation paradigm using a split-belt treadmill.…”