Biologically-variable rhythmic auditory cues are superior to isochronous cues in fostering natural gait variability in Parkinson’s disease

doi:10.1016/j.gaitpost.2016.09.020

Gait & Posture

Volume 51, January 2017, Pages 64-69

https://doi.org/10.1016/j.gaitpost.2016.09.020 Get rights and content

Highlights

•
Loss of long-range correlation in PD gait is a symptom of advanced disease.
•
Isochronous cueing is known to improve average gait parameters but removes the long-range correlation even in early stage patients.
•
Embedding physiological variability in the stimulus avoids this side effect of cueing.

Abstract

Introduction

Rhythmic auditory cueing improves certain gait symptoms of Parkinson's disease (PD). Cues are typically stimuli or beats with a fixed inter-beat interval. We show that isochronous cueing has an unwanted side-effect in that it exacerbates one of the motor symptoms characteristic of advanced PD. Whereas the parameters of the stride cycle of healthy walkers and early patients possess a persistent correlation in time, or long-range correlation (LRC), isochronous cueing renders stride-to-stride variability random. Random stride cycle variability is also associated with reduced gait stability and lack of flexibility.

Method

To investigate how to prevent patients from acquiring a random stride cycle pattern, we tested rhythmic cueing which mimics the properties of variability found in healthy gait (biological variability). PD patients (n = 19) and age-matched healthy participants (n = 19) walked with three rhythmic cueing stimuli: isochronous, with random variability, and with biological variability (LRC). Synchronization was not instructed.

Results

The persistent correlation in gait was preserved only with stimuli with biological variability, equally for patients and controls (p's < 0.05). In contrast, cueing with isochronous or randomly varying inter-stimulus/beat intervals removed the LRC in the stride cycle. Notably, the individual's tendency to synchronize steps with beats determined the amount of negative effects of isochronous and random cues (p's < 0.05) but not the positive effect of biological variability.

Conclusion

Stimulus variability and patients’ propensity to synchronize play a critical role in fostering healthier gait dynamics during cueing. The beneficial effects of biological variability provide useful guidelines for improving existing cueing treatments.

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.

References (32)

S.J. Spaulding et al.
Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis
Arch. Phys. Med. Rehabil.
(2013)
N.N. Byl et al.
The neural consequences of repetition: clinical implications of a learning hypothesis
J. Hand Ther.
(1997)
T. Herman et al.
Gait instability and fractal dynamics of older adults with a cautious gait: why do certain older adults walk fearfully?
Gait Posture
(2005)
J. Sowiński et al.
Poor synchronization to the beat may result from deficient auditory-motor mapping
Neuropsychologia
(2013)
J.M. Hausdorff
Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking
Hum. Mov. Sci.
(2007)
D.H. Gates et al.
Possible biomechanical origins of the long-range correlations in stride intervals of walking
Physica A
(2007)
G.C. McIntosh et al.
Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease
J. Neurol. Neurosurg. Psychiatry
(1997)
P. Arias et al.
Effects of rhythmic sensory stimulation (auditory, visual) on gait in Parkinson’s disease patients
Exp. Brain Res.
(2008)
J.M. Hausdorff et al.
Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease
Eur. J. Neurosci.
(2007)
S. Dalla Bella et al.
Effects of musically cued gait training in Parkinson’s disease: beyond a motor benefit
Ann. N. Y. Acad. Sci.
(2015)

I. Lim et al.

Does cueing training improve physical activity in patients with Parkinson’s disease?

Neurorehabil. Neural Repair

(2010)

K. Doya et al.

A computational model of birdsong learning by auditory experience and auditory feedback

K.S. Chaisanguanthum et al.

Motor variability arises from a slow random walk in neural state

J. Neurosci.

(2014)

M. Merzenich

How The New Science Of Brain Plasticity Can Change Your Life

(2013)

A.L. Goldberger et al.

Fractal dynamics in physiology: alterations with disease and aging

Proc. Natl. Acad. Sci. U. S. A.

(2002)

L.A. Lipsitz et al.

Loss of “complexity” and aging

JAMA

(1992)

Cited by (51)

Synchronization performance affects gait variability measures during cued walking
2022, Gait and Posture
Incorporating variability within gait rehabilitation offers a promising approach to restore functional capacity. However, it’s success requires adequate synchronization, a parameter that lacks report in most of the literature regarding cued gait training.
How changes to synchronization performance during fractal-like and isochronous cueing impacts gait variability measures?
We asked twelve young male participants to walk in synchronization to two different temporally structure cueing (isochronous [ISO] and fractal [FRC]). We have also manipulated the cueing’s tempo by increasing and decreasing it by 5% to manipulate synchronization, resulting in six conditions (stimuli [ISO,FRC] x tempo [SLOW, NORMAL, FAST]). The normal condition was set from an uncued trial through the participant’s self-paced stride time. Synchronization performance (ASYNC) and gait variability (fractal scaling and coefficient of variation) were calculated from stride time data ( -ISIs,CV-ISIs). Repeated measures analysis of variance or Aligned Rank Transform were conducted to determine significant differences between metronome tempo and stimuli for the dependent variables
Our results showed a FAST tempo decreases synchronization performance (ASYNC) and leads to lower -ISIs, for both ISO and FRC stimuli. This indicates that when an individual exhibits poor synchronization during cued gait training, his/her gait variability patterns will not follow the temporal structure of the presented metronome. Specifically, if the individual poorly synchronizes to the cues, the gait patterns become more random, a condition typically observed in older adults and neurological patients, which runs contrary to the hypothesis when using fractal-like metronomes.
This study provides supporting evidence that measuring synchronization performance in cued training is fundamental for a proper clinical interpretation of its effects. This is particularly relevant for the recent and ongoing clinical research using fractal-like metronomes since the expected gait patterns are dependent on the synchronization performance. Randomized control trials must incorporate synchronization performance related measures.
Benefits of nonlinear analysis indices of walking stride interval in the evaluation of neurodegenerative diseases
2021, Human Movement Science
Indices characterising the long-range temporal structure of walking stride interval (SI) variability such as Hurst exponent (H) and fractal dimension (D) may be used in addition to indices measuring the amount of variability like the coefficient of variation (CV). We assess the added value of the former indices in a clinical neurological context. Our aim is to demonstrate that they provide a clinical significance in aging and in frequent neurodegenerative diseases such as Parkinson's disease, Huntington, and amyotrophic lateral sclerosis.
Indices assessing the temporal structure of variability are mainly dependent on SI time series length and algorithms used, making quantitative comparisons between different studies difficult or even impossible. Here, we recompute these indices from available SI time series, either from our lab or from online databases. More precisely, we recompute CV, H, and D in a unified way. The average SI is also added to the measured parameters.
We confirm that variability indices are relevant indicators of aging process and neurodegenerative diseases. While CV is sensitive to aging process and pathology, it does not discriminate between specific neurodegenerative diseases. H, which measures predictability of SI, significantly decreases with age but increases in patients suffering from amyotrophic lateral sclerosis. D, catching complexity of SI, is correlated with total functional capacity in patients with Huntington's disease.
We conclude that the computation of H complements the clinical diagnosis of walking in patients with neurodegenerative diseases and we recommend it as a relevant supplement to classical CV or averaged SI. Since H and D indices did not lead to the same observations, suggesting the multi-fractal nature of SI dynamics, we recommend to open clinical gait analysis to the evaluation of more parameters.
Fractal auditory stimulation has greater benefit for people with Parkinson's disease showing more random gait pattern
2020, Gait and Posture
Citation Excerpt :
If fractal variations reflect locomotor system’s health and adaptive capacity, as suggested by theories of complex adaptive systems [19–21], gait rehabilitation should aim to increase the persistence of stride-to-stride variations. Stride-to-stride variations can be manipulated toward more randomness or more persistence when the inter-beat intervals present random or persistent variations, respectively [22–24]. People with PD are able to synchronize with fractal RAS, and to shift their stride-to-stride variations away from randomness toward more persistence.
Healthy gait dynamics are characterized by the presence of fractal, persistent stride-to-stride variations, which become more random with Parkinson’s disease (PD). Rhythmic auditory stimulation with fractal beat-to-beat variations can change gait dynamics in people with PD toward more persistence.
How does gait in people with PD change when synchronizing steps with fractal melodic metronomes with different step-to-beat ratios, and which stimulus do they prefer?
In this cross-sectional study, 15 people with PD and 15 healthy older adults walked over-ground in three conditions: self-paced, paced by a fractal auditory stimulus with a 1:1 step-to-beat ratio (‘metronome’), and fractal auditory stimulus with a 1:2 step-to-beat ratio (‘music’). Gait dynamics were recorded with instrumented insoles, and detrended fluctuation analysis (DFA) was applied to the series of stride time intervals. Stimuli preference was assessed using Likert-like scales and open-ended questions. ANOVAs were used to compare mean, coefficient of variation, α-DFA, and the responses from the continuous Likert scales. Pearson correlations were used to assess the relationship between ‘music’ and ‘metronome’ enjoyment or difficulty with gait outcomes, and to determine the association between baseline α-DFA and changes due to the stimuli.
Our major findings are that (i) stride-to-stride variations were more persistent with the ‘metronome’ compared to baseline for both groups, (ii) the effect was greater for people with lower α-DFA at baseline (i.e., more random stride-to-stride variations), and (iii) both groups found the ‘metronome’ less difficult to synchronize with.
This study showed that people with PD and healthy older adults walk with higher statistical persistence in their stride-to-stride variations when instructed to synchronize their steps with a fractal stimulus. Participants with lower persistence at baseline benefited the most from the fractal ‘metronome’, highlighting the importance to develop patient-centered tests and interventions.
Sensorimotor synchronization during gait is altered by the addition of variability to an external cue
2020, Human Movement Science
Sensorimotor synchronization has been used in the rehabilitation of gait, yet much remains unknown regarding the optimal use of this technique. The purpose of this study was to test the hypothesis that adding small amounts of variability to the motion of a vertically oscillating treadmill would affect the behavior of healthy walkers. Sixteen young adults walked on a treadmill and pneumatically actuated platform for one control trial (no oscillation) and eight trials in which the walking surface oscillated in the vertical direction under different conditions of variability. During the oscillation trials, the mean frequency of oscillation was equal to the preferred step frequency of the participant, but each individual cycle period was allowed to vary within a pre-determined range from 0% (no variability) to ±25% (high variability) of the mean cycle period. The amount of variance of each cycle period within each condition was drawn randomly from a white noise generator. Synchronization was improved when a small amount of noise was added to the platform motion but synchronization significantly decreased at higher levels of noise. Coefficient of variation of stride duration was relatively unchanged at lower levels of variability, but increased significantly at higher levels of variability. Statistical persistence of stride duration was significantly reduced during all trials with vertical oscillation relative to normal walking, but was not significantly altered by variability in the treadmill oscillation. These results suggest that the addition of a small amount of random variability to the cycle period of an oscillator may enhance sensorimotor synchronization of gait to an external signal. These data may have implications for the use of synchronization in a therapeutic setting.
Why do we move to the beat? A multi-scale approach, from physical principles to brain dynamics
2020, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
The temporal structure of cueing appears to influence the temporal dynamics of gait. Dotov et al. (2017) demonstrated that cueing with isochronous or randomly varying inter-stimulus/beat intervals removed the LRC in the stride cycle. In contrast, persistent correlation in gait was unaffected with stimuli which mimicked the properties of variability found in healthy gait.
Humans’ ability to synchronize movement with auditory rhythms relies on motor networks, such as cortical areas, basal ganglia and the cerebellum, which also participate in rhythm perception and movement production. Current research has provided insights into the dependence of this action-perception coupling upon the entrainment of neuronal activity by external rhythms. At a physical level, advances on wearable robotics have enriched our understanding of the dynamical properties of the locomotor system showing evidence of mechanical entrainment. Here we defend the view that modelling brain and locomotor oscillatory activities as dynamical systems, at both neural and physical levels, provides a unified theoretical framework for the understanding of externally driven rhythmic entrainment of biological systems. To better understand the underlying mechanisms of this multi-level entrainment during locomotion, we review in a common framework the core questions related to the dynamic properties of biological oscillators and the neural bases of auditory-motor synchronization. Illustrations of our approach, using personalized auditory stimulation, to gait rehabilitation in Parkinson disease and to manipulation of runners’ kinematics are presented.
Cognitive effects of rhythmic auditory stimulation in Parkinson's disease: A P300 study
2019, Brain Research
Citation Excerpt :
Although the mechanisms underlying AMS effects on temporal encoding are still unclear, the BG, involved in both motor and rhythm perception, are thought to contribute to this embodied timing coding during “active AMS”. Interestingly, PD patients benefit more from such a “passive AMS” than “active AMS” during gait training (Dotov et al., 2017; Hove et al., 2012). The present study, therefore, investigated whether active versus passive AMS influences the aforementioned effect of temporal predictability in PD patients.
Rhythmic auditory stimulation (RAS) may compensate dysfunctions of the basal ganglia (BG), involved with intrinsic evaluation of temporal intervals and action initiation or continuation. In the cognitive domain, RAS containing periodically presented tones facilitates young healthy participants’ attention allocation to anticipated time points, indicated by better performance and larger P300 amplitudes to periodic compared to random stimuli. Additionally, active auditory-motor synchronization (AMS) leads to a more precise temporal encoding of stimuli via embodied timing encoding than stimulus presentation adapted to the participants’ actual movements.
Here we investigated the effect of RAS and AMS in Parkinson’s disease (PD). 23 PD patients and 23 healthy age-matched controls underwent an auditory oddball task. We manipulated the timing (periodic/random/adaptive) and setting (pedaling/sitting still) of stimulation. While patients elicited a general timing effect, i.e., larger P300 amplitudes for periodic versus random tones for both, sitting and pedaling conditions, controls showed a timing effect only for the sitting but not for the pedaling condition. However, a correlation between P300 amplitudes and motor variability in the periodic pedaling condition was obtained in control participants only. We conclude that RAS facilitates attentional processing of temporally predictable external events in PD patients as well as healthy controls, but embodied timing encoding via body movement does not affect stimulus processing due to BG impairment in patients. Moreover, even with intact embodied timing encoding, such as healthy elderly, the effect of AMS depends on the degree of movement synchronization performance, which is very low in the current study.

View all citing articles on Scopus

¹: Present address: Circuito Mario de la Cueva 20, Insurgentes Cuicuilco, Ciudad de México, D.F México.

View full text

Full length articleBiologically-variable rhythmic auditory cues are superior to isochronous cues in fostering natural gait variability in Parkinson’s disease

Highlights

Abstract

Introduction

Method

Results

Conclusion

Introduction

Section snippets

Participants

Results

Discussion

Conclusion

Financial disclosure

Arch. Phys. Med. Rehabil.

J. Hand Ther.

Gait Posture

Neuropsychologia

Hum. Mov. Sci.

Physica A

Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease

J. Neurol. Neurosurg. Psychiatry

Effects of rhythmic sensory stimulation (auditory, visual) on gait in Parkinson’s disease patients

Exp. Brain Res.

Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease

Eur. J. Neurosci.

Effects of musically cued gait training in Parkinson’s disease: beyond a motor benefit

Ann. N. Y. Acad. Sci.

Does cueing training improve physical activity in patients with Parkinson’s disease?

Neurorehabil. Neural Repair

A computational model of birdsong learning by auditory experience and auditory feedback

Motor variability arises from a slow random walk in neural state

J. Neurosci.

How The New Science Of Brain Plasticity Can Change Your Life

Fractal dynamics in physiology: alterations with disease and aging

Proc. Natl. Acad. Sci. U. S. A.

Loss of “complexity” and aging

JAMA

Full length article
Biologically-variable rhythmic auditory cues are superior to isochronous cues in fostering natural gait variability in Parkinson’s disease