Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories

Abstract

We investigated the contributions of the cerebellum and the motor cortex (M1) to acquisition and retention of human motor memories in a force field reaching task. We found that anodal transcranial direct current stimulation (tDCS) of the cerebellum, a technique that is thought to increase neuronal excitability, increased the ability to learn from error and form an internal model of the field, while cathodal cerebellar stimulation reduced this error-dependent learning. In addition, cathodal cerebellar stimulation disrupted the ability to respond to error within a reaching movement, reducing the gain of the sensory-motor feedback loop. By contrast, anodal M1 stimulation had no significant effects on these variables. During sham stimulation, early in training the acquired motor memory exhibited rapid decay in error-clamp trials. With further training the rate of decay decreased, suggesting that with training the motor memory was transformed from a labile to a more stable state. Surprisingly, neither cerebellar nor M1 stimulation altered these decay patterns. Participants returned 24 hours later and were re-tested in error-clamp trials without stimulation. The cerebellar group that had learned the task with cathodal stimulation exhibited significantly impaired retention, and retention was not improved by M1 anodal stimulation. In summary, non-invasive cerebellar stimulation resulted in polarity-dependent up- or down-regulation of error-dependent motor learning. In addition, cathodal cerebellar stimulation during acquisition impaired the ability to retain the motor memory overnight. Thus, in the force field task we found a critical role for the cerebellum in both formation of motor memory and its retention.

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

“…This may be critically important, since movement trajectory is affected both by the ability of the nervous system to learn from errors that were observed in the previous trials, termed trial-to-trial learning, and respond to errors that are sensed in the current trial, termed within-trial response to error (Ahmadi-Pajouh et al 2012;Franklin et al 2007;Kimura et al 2006;Kimura and Gomi 2009;Wong et al 2009). Some studies suggest that the human motor cortex may play an important role in learning to modulate the within-trial response to error (Kimura et al 2006), although disruption of the human cerebellum also reduces the gain of this feedback pathway (Herzfeld et al 2014a). Here, by eliminating this within-trial feedback, we were able to precisely measure learning from error on each trial.…”

Effects of tDCS on motor learning and memory formation: A consensus and critical position paper

“…In contrast, a dissociative effect emerged when M1 stimulation resulted in improved retention of the newly acquired visuomotor transformation, as subjects receiving this stimulation adapted faster when the perturbation was reintroduced following a washout period. Interestingly, in a force-field reaching task that assesses adaptation to perturbed upper limb dynamics, anodal tDCS applied to the cerebellum increased error-dependent learning and facilitated adaptation, while M1 stimulation had no effect (Herzfeld et al, 2014). Furthermore, anodal tDCS applied over M1 did not improve retention.…”

“…tDCS-related effects on adaptation have also been studied in young healthy adults (Avila et al, 2015;Galea et al, 2011;Herzfeld et al, 2014;Hunter, Sacco, Nitsche, & Turner, 2009;Orban de Xivry et al, 2011) (Table 3). Galea and colleagues (2011) compared the effects of anodal tDCS applied to the cerebellum versus M1 during concurrent adaptation to 30-degree rotation of visual feedback (Galea et al, 2011).…”

Cathodal Transcranial Direct Current Stimulation (tDCS) to the Right Cerebellar Hemisphere Affects Motor Adaptation During Gait

“…Adaptation is an error-driven process aimed at learning responses to non-random stimuli [2], such as the trial-and-error adjustment of movements to meet demands [3]. Adaptation can be quantified via reductions in errors over time during a measured task [4,5], or reduction in variability prior to/during successful learning of a task [6].…”