Evidence for motor learning in Parkinson's disease: Acquisition, automaticity and retention of cued gait performance after training with external rhythmical cues

Abstract

People with Parkinson's disease (PD) have difficulty learning new motor skills. Evidence suggests external stimuli (cues) may enhance learning; however, this may be specific to cued rather than non-cued performance. We aimed to test effects of cued training on motor learning in PD. We defined motor learning as acquisition (single task), automaticity (dual task) and retention of single- and dual-task performance (follow-up). 153 subjects with PD received 3 weeks cued gait training as part of a randomised trial (the RESCUE trial). We measured changes in cued gait performance with three external rhythmical cues (ERC) (auditory, visual and somatosensory) during single and dual tasks after training and 6 weeks follow-up. Gait was tested without cues to compare specificity of learning (transfer). Subjects were ‘on’ medication and were cued at preferred step frequency during assessment. Accelerometers recorded gait and walking speed, step length and step frequency were determined from raw data. Data were analysed with SAS using linear regression models. Walking speed and step length significantly increased with all cues after training during both single- and dual-task gait and these effects were retained. Training effects were not specific to cued gait and were observed in dual-task step length, and walking speed however was more limited in single-task non-cued gait. These results support the use of ERC to enhance motor learning in PD as defined by increased acquisition, automaticity and retention. They also highlight the potential for sustained improvement in walking and complex task performance.

Introduction

Research has highlighted a role for the basal ganglia in learning, raising questions regarding the capacity for people with Parkinson's disease (PD) to acquire and retain motor skills (Doyon, 2008). Motor skills and sequences of movement are acquired through a process of implicit learning, becoming automatic with practice and performed with little conscious awareness as opposed to explicit learning which refers to acquisition of factual knowledge. Automatic movements have functional benefits, allowing dual- and multiple-task performance, and are impaired in PD (Bond and Morris, 2000, O'Shea et al., 2002, Rochester et al., 2004). The main method of managing the symptoms of Parkinson's disease (PD) is through levodopa therapy providing highly effective symptomatic treatment. However, after a variable period of time, motor complications develop that cannot be adequately controlled with medication. These complications include unpredictable and extended ‘off’ periods, dyskinesias, poor gait and balance which contribute to reduced mobility and increased risk of falls. Rehabilitation strategies that result in sustained change in function in PD may therefore offer an important contribution to patient management. Knowledge of motor learning is therefore critical for the optimal design of rehabilitation interventions (Abbruzzese et al., 2009).

Motor skill acquisition, automaticity and retention are considered hallmarks of motor learning. Learning a motor skill has two phases in which the skill is acquired over a short time scale (a few hours) and then consolidated (retained) into long-term memory with practice over several weeks (Karni et al., 1995). During the early stage attention is required and with repeated practice this is reduced such that performance can occur automatically with relatively little attention. Whilst a recent meta-analysis concluded that implicit sequence learning was impaired in PD (Siegert et al., 2006) others have reported that it was possible but attenuated compared to controls (Wu and Hallett, 2008, Wilkinson and Jananshahi, 2007, Mentis et al., 2003, Carbon and Eidelberg, 2006). In PD the fast stage of learning where skills are acquired may be preserved; however, transference of skills into later stages of learning with increased automaticity and retention of skill is less efficient compared to age matched controls (Doyon et al., 1998, Wu and Hallett, 2008, Wilkinson and Jananshahi, 2007, Muslimovic et al., 2007).

Motor learning studies demonstrate that there is capacity for people with PD to learn a variety of motor tasks ranging from upper limb movement to functional tasks (Smiley-Oyen et al., 2006, Jessop et al., 2006; Mak and Hui-Chan, 2008). A common feature of these studies is the use of augmented feedback such as auditory pacing cues or visual cues for training. External information in the form of visual or auditory stimuli improves motor performance and motor learning in normal subjects (Heremans et al., 2009, Semjen et al., 2000). Augmented visual feedback also facilitated motor learning in a novel upper limb task in PD (Verschueren et al., 1997). Interestingly in this study, the effects were not retained in the absence of sensory information, highlighting the possibility that learning in PD is context specific with external feedback being incorporated into the motor program (Verschueren et al., 1997). The study by Verschueren et al. (1997) also highlights an important point in relation to methods of evaluating training as some studies test the effect of training with the cue and others test without the cue and therefore measure transfer of skill. This is an important distinction as cue specific learning (described by Verschueren et al., 1997) may be missed.

External cues have received much interest as a rehabilitation tool to improve function such as gait in PD (for review, see Rubinstein et al., 2002, Lim et al., 2005, Nieuwboer et al., 2008). External cues have been defined as temporal (e.g., auditory tones to step in time to) or spatial (lines on the ground to step on or over) stimuli associated with the ongoing facilitation of movement (Nieuwboer et al., 2007). In PD, where practice was given in a single training session external cues improved walking speed and step length (Morris et al., 1996, Rochester et al., 2007, Baker et al., 2007, Hausdorff et al., 2007). Dual-task walking speed and step length also improve suggesting that gait had become more automatic (Rochester et al., 2005, Rochester et al., 2007, Baker et al., 2007). Furthermore a one off-training session with external cues had a short-term carryover effect to non-cued gait (up to 2 h) (Morris et al., 1996, Rochester et al., 2005, Rochester et al., 2007, Baker et al., 2007, Baker et al., 2008, Hausdorff et al., 2007), which may indicate the early stages of learning or heightened attention. These studies measure cued gait and underscore the potential for cueing training as a motor learning paradigm. However they also raise the question as to whether a longer period of training may facilitate the later phase of motor learning in PD to enhance automaticity and retention.

Clinical studies have shown that externally cued practice over more extended periods (3–6 weeks) show significant benefits of training with a range of different external cues on gait, balance and transfers (Thaut et al., 1996, Nieuwboer et al., 2007, Mak and Hui-Chan, 2008, Sidaway et al., 2006). Cued training has also been shown to be more effective than other interventions such as non-cued exercise (Mak et al., 2007; Marchese et al., 2000). Evidence for retention is inconclusive however with some studies reporting retention of between 2 and 4 weeks (Mak and Hui-ChanMak and Hui-Chan, 2008, Sidaway et al., 2006) whilst others of longer duration (6 weeks) do not (Nieuwboer et al., 2007). In all of these studies, training effects were measured without the external cue; therefore, they primarily concentrated on generalisation to a range of functional skills and motor symptoms. It may be that learning in PD is cue specific as reported by Verschueren et al. (1997) and the effect of training on cued performance is therefore not clear to date.

As stated above, we have shown that gait training with external rhythmical cues (ERC) (the RESCUE trial) (Nieuwboer et al., 2007) improved a variety of functional tests relating to a broad range of mobility outcomes. These effects were not retained at 6 weeks; however, the method of assessment could be insensitive to learning effects specific to cued performance. We were therefore also interested in the specificity of training with ERC on cued gait performance, which we evaluated using a specially designed protocol that measured cued single- and dual-task gait performance (Rochester et al., 2007). We used three different ERC modalities (visual, auditory and somatosensory) and found ERC (especially auditory) immediately enhanced dual-task gait performance before training and had a short-term carryover to non-cued gait but these effects were not retained when measured 3 weeks later (Rochester et al., 2007). Here we extend our findings to report the effect of training with ERC on cued gait performance during single- and dual-task gait and retention of performance. These are new data and have not been previously reported. In this study we defined motor learning as acquisition, automaticity and retention of skill. We hypothesized that an extended period of training with ERCs would further enhance cued gait performance during single (acquisition) and dual tasks (automaticity) and would be retained. We also tested training effects during non-cued single- and dual-task gait to see learning was specific to cued trials only.