Creating order from chaos: Walking on cue with rhythmic auditory stimulation

COMMENTARY

By Conor Sheridan & Lucas D. Crosby

One, two, three, four. You count along to a metronome’s tones, matching your foot steps to the rhythmic symphony with seemingly little effort. You are engaging in rhythmic auditory stimulation (RAS) – a technique used in rehabilitation to facilitate movements that are biologically rhythmic (1). In simplest terms, RAS is the use of rhythmic cues (e.g., musical beats) to which humans synchronize their movements to assist with the performance of rhythmic actions (e.g., walking).

During the 2017 International Society of Posture and Gait Research (ISPGR) World Congress, an exciting topic of discussion was a new form of auditory stimulation for the rehabilitation of gait (walking pattern) called variable-tempo RAS (vRAS). In contrast to the more commonly used fixed-tempo RAS (fRAS), which delivers a constant beat, vRAS employs an ever-changing beat of rhythmic cues. Two studies presented during ISPGR investigated this new form of RAS: the first used variable-tempo auditory cues to manipulate healthy gait (2), and the second used variable-tempo visual cues to retrain gait post-stroke (3). In the second study, participants with stroke showed improvements in gait pattern at a post-training follow-up, despite a lack of improvement during training trials (3). As described at ISPGR, future research aims to investigate the underlying mechanisms contributing to these enhancements and the potential implications of vRAS for the improvement of asymmetrical post-stroke gait.

As this research emerges, it is worth considering whether or not this new vRAS has advantages for gait rehabilitation over the more commonly used fRAS. This article aims to explore the potential differences between vRAS and fRAS as a gait intervention. To understand how human gait may benefit from RAS, one must first appreciate the basics of gait dynamics.

While the way humans walk can be considered mostly symmetrical, stride-to-stride variations are inherent to a healthy gait (4), providing adaptability and stability (5). In some cases, such as stride time, having less variability is better as it demonstrates greater stability. In other cases, such as step width, a moderate level (or optimal pattern) of variability reflects a more adaptable gait (6). Researchers measure variation using two methods: (a) calculating the deviation of individual strides from an overall mean (i.e., standard deviation), and (b) examining fractal index. The fractal index is a measure of the optimal range for healthy stride variation patterns. An individual’s overall walking pattern is made up of groups of strides that vary, but are related to and dependent upon one another (i.e., a single stride affects subsequent strides and is dependent on preceding strides). An optimal fractal index signifies the presence of long-term memory in the locomotor control system (5).

Analyzing stride-to-stride dynamics of gait unearths an array of subtleties in the development of movement and movement pathology. For instance, children at age three outwardly appear to have a mature gait; however, it is not until after age seven that they present with an optimal pattern of stride dynamics (7). In Huntington’s disease, damage to brain areas responsible for rhythmic control of movement causes a more random pattern of stride-to-stride fluctuations (8). These fluctuations demonstrate a lack of movement control necessary to generate the long-term stride-to-stride correlations observed in healthy adults (5).

For over 20 years, RAS has been widely used in rehabilitation to modulate disordered gait expressed in neurologic conditions such as Parkinson’s disease (PD), Huntington’s disease, traumatic brain injury, and stroke (1,9). Gait modulation occurs when a person synchronizes their stepping movements to a steady metronome beat through entrainment. This process happens when physiological (e.g., heart rate or breathing) or behavioural (e.g., movement) rhythms synchronize to an external rhythm. A common example of entrainment is the urge many people feel to nod or tap along to the beat of their favourite song.

The steady beat involved in fRAS is used to help restore gait to a more symmetrical rhythm, and is effective at retraining gait in individuals with many neurologic conditions (1). After stroke for instance, improvements such as increased use of the paretic leg are observed even after walking only a single trial with fRAS entrainment (10). Following fRAS training, people with stroke demonstrate increased walking speed, improved cadence and stride length, and enhanced inter-leg symmetry (11,12). Moreover, in individuals with PD, gait improvements are maintained for at least two months following fRAS training (18 sessions across six weeks) (13). So far, fRAS shows a multitude of benefits in a variety of gait-related disorders.

Due to the importance of inherent stride variations and the fact that everyday gait requires dynamic changes in inherently fast-moving environments (5), such as in a busy shopping centre or on a crowded subway platform, some researchers have suggested that training with fRAS may have limited benefits (14,15). For instance, fRAS may work to organize gait around a single tempo rather than retaining its inherent, non-random stride-to-stride variation. At face value, fRAS can reduce stride time variability in individuals with PD; however, when the underlying fluctuation patterns are analyzed, patients do not appear to demonstrate a healthy fractal index (14). This distinction further emphasizes the independence of both methods of assessing stride-to-stride variability: standard deviation and fractal indexing. Thus, fRAS has demonstrated flaws in restoring optimal variability in both healthy (15) and Parkinsonian gait (14). Consequently, vRAS has been proposed for gait rehabilitation in individuals with neurologic conditions (5,14,16).

Recently, vRAS has gained traction with the development of the WalkMate system (17). This system plays auditory cues through headphones that continuously adjust to an individual’s walking tempo, resulting in mutual entrainment – that is, synchrony between the walking steps and auditory cues (17). Foot sensors collect information about walking tempo, and a computer uses that information to adjust the auditory cues accordingly. This system has the added benefit of more accurately simulating the dynamic fluctuation of healthy everyday gait, thus facilitating more adaptable retraining (15,16,18,19). In individuals with PD, vRAS has led to greater stride-to-stride variability (representing optimal healthy dynamic gait) compared to fRAS conditions, which lowered stride-to-stride variability away from healthy gait patterns (14).

While some promising results are emerging for vRAS, there is no clear evidence of lasting effects, such as those described for fRAS. To our knowledge, only one study has reported some lasting effects using variable-tempo visual cues for treadmill gait entrainment in healthy adults (20). Until recently, vRAS was infeasible for low mobility populations due to the high step count (>500 strides) required to perform complex analyses of optimal variability estimations. Guidelines now exist to apply this technique to data with shorter time series (100-200 strides), expanding its applicability in the gait rehabilitation field (21). In the future, randomized controlled trials with post-training follow-up periods in low mobility neurologic populations could examine if vRAS has long-lasting effects.

The effectiveness of both RAS methods is challenged when we explore the rhythmic abilities of different individuals. Researchers measure beat perception and production abilities using the Beat Alignment Task (22). Not everyone can easily synchronize their movements to a beat, and many are poor at this task. While mostly anecdotal (23), some empirical evidence suggests rhythmic abilities vary in the healthy population (24,25). With neurologic conditions, such as PD (26) and stroke (27), rhythmic perception can also be impaired. Therefore, when using RAS training for an individual with poor rhythmic abilities, there may actually be a detrimental effect on gait. The cognitive resources required to attend to the rhythmic cue could hinder the benefits of RAS entrainment (28).

Conferences like ISPGR provide gait rehabilitation researchers with invaluable platforms to present their creative ideas to the world. Some of the research that was showcased at ISPGR 2017 suggests that vRAS can restore healthy stride dynamics to populations with neurological impairments. Yet, this modality lacks evidence of the long-term benefits fRAS provides to patients. In addition to examining the lasting effects of vRAS, future research should investigate the combined use of both techniques to facilitate a synergistic therapeutic effect. For example, patients with low mobility could begin treatment with fRAS to first improve step length and rate, and then transition to vRAS to restore the optimal stride variability observed in healthy populations. Major strides in the future of gait rehabilitation research will rely on the imagination of those eager to step forward and create new rehabilitation techniques.

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