Full length articleBiologically-variable rhythmic auditory cues are superior to isochronous cues in fostering natural gait variability in Parkinson’s disease
Introduction
Rhythmic auditory cues (e.g., repeated tones or music) can improve gait in Parkinson's disease (PD) [1]. Such non-invasive stimulation leads to an immediate increase of cadence, stride length, and/or speed [2], [3] which might extend to non-cued gait following training [4]. Benefits from cueing may be related to patients’ rhythmic skills [5]. These findings suggest that a portable device can serve as a technological aid in assisting patients in their daily lives and delivering a training program [6]. This use of cueing implies that many of the patients may aim to walk in synchrony with the stimulus. Success of an isochronous stimulus (i.e., tones separated by a constant time interval) is defined in terms of removing all temporal variation. Is it beneficial, however, to repetitively execute a stereotypical movement without any variation?
Computational models suggest that motor variability linked to basal ganglia activity fosters more effective motor learning [7]. Slow variation in a repetitive reaching task in monkeys or in baseball pitching is a part of the process of learning and practicing [8]. At the other extreme, forced long-term stereotypy can lead to loss of behavioral repertoire and even undesirable cortical reorganizations leading to focal dystonia [9]. Thus, variability in training is recommended as a general principle of rehabilitation practice [10].
The temporal properties of variability are particularly important when the motor behavior necessarily involves repetition, such as the case of gait. Typically, however, only an averaged characterization of the gait cycle in terms of mean stride length, speed, and cadence has been used while studying the effects of rhythmic auditory cueing. This fails to reveal the influence of the temporal structure of cueing on the temporal dynamics of gait (i.e., the change of the gait cycle) throughout the trial.
In healthy individuals, the temporal dynamics of gait, expressed in terms of the inter-stride-intervals (ISI), exhibits non-random variability characterized by a persistent trend called long-range correlation (LRC). The LRC property of healthy gait, herein referred to as ‘biological variability’ because of its ubiquitous character in physiological processes [11], [12], is characterized by persistent trends unfolding on multiple temporal scales (i.e., it possesses fractal properties). LRC means that the ISI characterizing a given gait cycle depends on all previous ISIs. A random ISI would not depend on the previous ISIs. LRC is deemed an optimal form of control of physiological processes because LRC is a functionally beneficial combination of stability (persistent control) and variability (flexibility) [11]. It has been associated with tolerance to errors and resistance to perturbations [12], [13]. Biological variability distinguishes faller from non-faller patients with so-called higher-level gait disorder (HLGD) [14]. Thus, the disappearance of LRC with advanced PD [15] is a clinically relevant symptom.
In spite of its beneficial effect on averaged measures, isochronous cueing may exacerbate certain PD symptoms related to the dynamics of these measures. Stimuli with isochronous beats remove LRC in healthy individuals [16] and in PD patients [17]. This could be avoided by embedding biological variability in the stimulus. We tested this strategy in a group of PD patients. The auditory stimuli also varied in terms of their musical complexity (a sequence of tones or music). This was to test the independence of the effect of variability from the characteristics of the auditory stimulus such as pitch, rhythmic features, and motivational factors (music is expected to be more motivating than a metronome) [18].
The interval between the sounds or musical beats was either fixed (standard cueing), non-biologically variable (random uncorrelated noise), or biologically variable (with embedded LRC). The latter was hypothesized to preserve LRC of gait in patients with PD while also maintaining the other beneficial effects expected from standard cueing.
Section snippets
Participants
Nineteen non-demented patients with PD were recruited in the Department of Neurology of a Regional University Hospital of Montpellier, and in the neurological unit of another local hospital (Beau Soleil Clinic). The clinical diagnosis of PD was based on the Queen Square Brain Bank criteria. At the time of testing, all patients scored above the recommended cutoff for dementia (21/30) on the Montreal Cognitive Assessment (MoCA) for screening cognition in PD. Patients were assessed on revised
Results
The analysis of gait parameters at pre-tests showed that patients' stride length was significantly shorter relative to controls (p < 0.01) by 9%. The two groups were comparable in the other gait parameters including LRC (see Table 2).
The effects of cueing conditions are summarized in Table 2. The statistics were based on data averaged across left and right turning trials and across the three stimulus types (metronome, music, AMN) because statistical analyses did not reveal any effects or
Discussion
LRC typical of healthy gait has been linked to increased adaptive stability to perturbations [12], [13], to movement efficiency in terms of kinetic energy re-use [25], and lowered risk of falls [26]. The goal of the present study was to test whether biological variability embedded in the cueing stimulus can overcome the deleterious side-effects of standard isochronous cueing. Our findings confirm two important hypotheses. First, consistent with previous studies [4], patients' gait loses its
Conclusion
The correlation between synchronization and negative impact of isochronous cueing reveals the following dilemma: recommend synchronization but sacrifice natural variability or spare natural variability but diminish the positive effects of synchronizing with the cue. While there might not be an immediate negative consequence of acquiring a more random gait pattern it is safe to assume that the long-term consequences will be substantial. Embedded biological variability should be introduced in
Financial disclosure
The authors do not hold financial interests in the outcome of the current study.
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Present address: Circuito Mario de la Cueva 20, Insurgentes Cuicuilco, Ciudad de México, D.F México.