Elsevier

NeuroImage

Volume 98, September 2014, Pages 147-158
NeuroImage

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

https://doi.org/10.1016/j.neuroimage.2014.04.076Get rights and content

Highlights

  • We applied tDCS to the brain during force field learning.

  • Anodal stimulation of the cerebellum increased learning from error.

  • Cathodal cerebellar stimulation impaired learning from error and feedback control.

  • Cathodal cerebellar stimulation during acquisition impaired subsequent overnight retention.

  • Anodal motor cortex stimulation had no effect on learning from error and retention.

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.

Introduction

When we interact with a novel object, we learn through trial and error to control that object, producing a motor memory that can be recalled the next time the object is encountered. Force field learning has been used as an experimental paradigm to uncover some of the processes that the brain relies on to accomplish this feat. In a typical experiment, the participant holds the handle of a robotic arm and makes a reaching movement, experiencing novel forces that displace the hand, resulting in error. This error engages short- and long-latency feedback pathways, producing a within-movement motor response to the error. In the subsequent reach the brain predicts some of the novel forces from the onset of the movement, resulting in partial compensation for the robot-induced forces. This trial-to-trial change in the motor commands has a specific pattern: the within-movement error feedback response is shifted earlier in time to produce a predictive response (Thoroughman and Shadmehr, 1999). With training, some of the modifications to the motor commands become a motor memory, as exemplified by the observation that the memory is disengaged when the robot handle is released (Kluzik et al., 2008), and is recalled days (Criscimagna-Hemminger and Shadmehr, 2008, Joiner and Smith, 2008) or months (Shadmehr and Brashers-Krug, 1997) later when the robot handle is grasped.

Formation of this motor memory appears independent of human medial temporal lobe structures (Shadmehr et al., 1998), but dependent on the integrity of the cerebellum (Criscimagna-Hemminger et al., 2010, Donchin et al., 2012, Smith and Shadmehr, 2005), and the motor cortex (Arce et al., 2010b, Li et al., 2001, Orban de Xivry et al., 2011a, Orban de Xivry et al., 2011b, Orban de Xivry et al., 2013, Richardson et al., 2006). In particular, a study in humans demonstrated that reversible disruption of the thalamic projections of the cerebellum to the cortex produced within-subject impairments in the ability to learn the force field task (Chen et al., 2006). Therefore, the current evidence points to the cerebellum as one of the structures that plays a critical role in the acquisition of this motor memory.

Here, we used transcranial direct current stimulation (tDCS) to alter function of the cerebellum and quantified the effect of this disruption on the ability to learn the force field task. tDCS of the cerebellum is thought to affect the excitability of Purkinje cells (Galea et al., 2009). Anodal cerebellar stimulation, which is thought to elevate the excitability of Purkinje cells, has been shown to increase rates of adaptation in visuomotor (Block and Celnik, 2013, Galea et al., 2010) and gait (Jayaram et al., 2012) tasks, whereas cathodal cerebellar stimulation, which is thought to reduce Purkinje cell excitability, has been shown to decrease rates of gait adaptation (Jayaram et al., 2012). By contrast, anodal stimulation of the motor cortex (M1) had no effect on the rate of visuomotor adaptation, the size of after-effects, or the rate of de-adaptation upon removal of the perturbation (Galea et al., 2011). However, immediately after adaptation and removal of anodal M1 tDCS, those in the stimulation group showed a reduced rate at which the resulting memory decayed in the absence of visual feedback (Galea et al., 2011). These findings led Galea et al. (2011) to propose that whereas the cerebellum may be critical for learning from error, the motor cortex plays a role in retention of the resulting memory. By contrast with the findings of Galea et al. (2011), Hunter et al. (2009) applied anodal stimulation to the motor cortex in a force field task and observed a larger reduction in signed kinematic errors during adaptation than in a sham tDCS condition, suggesting that motor cortical stimulation increased learning from error. Therefore, whereas current evidence suggests that stimulation of the human cerebellum can affect learning from error, it is unclear whether stimulation of the motor cortex affects learning from error and/or retention.

Here, we compared the effects of cerebellar and M1 stimulation on the process of acquisition and retention of motor memories in a force field paradigm. Given previous observations in other motor learning paradigms, we expected that M1 stimulation would not affect the rate of learning from error, whereas anodal cerebellar stimulation would increase this rate and cathodal cerebellar stimulation would decrease the rate of learning. In addition, to specifically test the hypothesis that anodal stimulation of M1 enhances retention of motor memories (Galea et al., 2011), we tested the effects of M1 anodal stimulation on both short-term retention (via blocks of error-clamp trials during the training blocks), and long-term retention (at 24 hours following completion of training).

Section snippets

Materials and methods

Fifty healthy self-reported right-handed volunteers (21 females; mean age ± STD of 24 ± 4.7 years, range 18–38 years) with no known neurological or psychiatric disorders participated in our study. All participants were naive to the purpose of the experiment and gave written informed consent. The study was approved by the Johns Hopkins School of Medicine Institutional Review Board. Participants were screened prior to enrollment in the study to ensure that they did not have conditions that would

Results

In our experiment, short blocks of field trials alternated with short blocks of error-clamp trials (Fig. 1A). The two day experiment enabled us to measure three separate components of learning: 1) in field trials of Day 1 we assayed error-dependent learning by quantifying how the motor output improved from one trial to the next, 2) in error-clamp trials of Day 1 we assayed the stability of the developing memory by quantifying how the motor output decayed within blocks in the absence of error,

Discussion

We performed a two day experiment to measure effects of non-invasive brain stimulation on the ability to learn to reach in a force field. We found that increasing the excitability of the cerebellum via anodal tDCS increased the rate of learning, while decreasing cerebellar excitability via cathodal tDCS impaired the ability to respond to sensory feedback and decreased the rate of learning. On Day 1, training resulted in a motor output that decayed in the absence of error. This decay was fast in

Acknowledgments

This work was supported by grants from the NIH (NS37422) and the Human Frontiers Science Program. A.M.H. is currently with the Department of Neurology, Johns Hopkins School of Medicine. D.P. was supported by a Rotary International Ambassadorial Scholarship. J.O'S. was supported by a Royal Society Dorothy Hodgkin Fellowship and Research Grant.

Conflict of interest

The authors declare no competing financial interests.

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    D.J.H. and D.P. contributed equally to this research.

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