Dynamic Modulation of Cerebellar Excitability for Abrupt, But Not Gradual, Visuomotor Adaptation

Abstract

The cerebellum is critically important for error driven adaptive motor learning, as evidenced by the fact that cerebellar patients do not adapt well to sudden predictable perturbations. However, recent work has shown that cerebellar patients adapt much better if the perturbation is gradually introduced. Here we explore physiological mechanisms that underlie this distinction between abrupt and gradual motor adaptation in humans. We used Transcranial Magnetic Stimulation (TMS) to evaluate whether neural mechanisms within the cerebellum contribute to either process during a visuomotor reach adaptation. When a visuomotor rotation was introduced abruptly, cerebellar excitability changed early in learning, and approached baseline levels near the end of the adaptation block. However, we observed no modulation of cerebellar excitability when we presented the visuomotor rotation gradually during learning. Similarly, we did not observe cerebellar modulation during trial-by-trial adaptation to random visuomotor displacements or during reaches without perturbations. This suggests that the cerebellum is most active during the early-phases of adaptation when large perturbations are successfully compensated.

Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration

“…Our finding are consistent with an earlier study that used force-field perturbation tasks and found that performance of the cerebellar patients was impaired in the abrupt protocol, but less affected in the gradual protocol (Criscimagna-Hemminger et al 2010). Our results, however, stand in contrast to a study that found similar impairments in the gradual and abrupt protocols in a visuomotor rotation task (Schlerf et al 2012). Gibo et al (2013) observed improvements in the gradual protocol, but only for some directions of reaching.…”

“…In contrast to these results, in a visuomotor rotation paradigm, Schlerf et al (2012) reported that individuals with cerebellar damage showed similar adaptation deficits in abrupt and gradual perturbation protocols. In a force field paradigm, Gibo et al (2013) reported that the benefit from the gradual protocol was present in some reach directions, but not others.…”

“…In a visuomotor reach adaptation paradigm, there are changes in the excitability of the human cerebellum during an abrupt protocol, but these changes are smaller in the gradual protocol (Schlerf et al 2012). Disruption of the human motor cortex impairs adaptation in the force field paradigm during an abrupt protocol, but the same disruption appears to spare adaptation during a gradual protocol in force fields (Orban de Xivry et al 2011) and visuomotor rotations (Hadipour-Niktarash et al 2007).…”

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

“…For instance, projections from the cerebellum to the motor cortex are modulated during abrupt adaptation but not during gradual adaptation (Schlerf et al 2012). Nevertheless, contradictory data from cerebellar patients do not allow us to assess the role of the cerebellum in the abrupt and gradual conditions (CriscimagnaHemminger et al 2010;Gibo et al 2013;Izawa et al 2012;Smith and Shadmehr 2005).…”

Laterality Differences in Cerebellar–Motor Cortex Connectivity

“…As a physiological measure, it is sensitive to behaviors such as locomotor adaptation ) and reach adaptation (Schlerf et al 2012). The majority of studies have focused on the connectivity between the cerebellum and M1 in the dominant hand.…”