Complexity of human walking: the attractor complexity index is sensitive to gait synchronization with visual and auditory cues

Background. During steady walking, gait parameters fluctuate from one stride to another with complex fractal patterns and long-range statistical persistence. When a metronome is used to pace the gait (sensorimotor synchronization), long-range persistence is replaced by stochastic oscillations (anti-persistence). Fractal patterns present in gait fluctuations are most often analyzed using detrended fluctuation analysis (DFA). This method requires the use of a discrete times series, such as intervals between consecutive heel strikes, as an input. Recently, a new nonlinear method, the attractor complexity index (ACI), has been shown to respond to complexity changes like DFA. But in contrast to DFA, ACI can be applied to continuous signals, such as body accelerations. The aim of this study was to further compare DFA and ACI in a treadmill experiment that induced complexity changes through sensorimotor synchronization. Methods. Thirty-six healthy adults walked 30 minutes on an instrumented treadmill under three conditions: no cueing, auditory cueing (metronome walking), and visual cueing (stepping stones). The center-of-pressure trajectory was discretized into time series of gait parameters, after which a complexity index (scaling exponent alpha) was computed via DFA. Continuous pressure position signals were used to compute the ACI. Correlations between ACI and DFA were then analyzed. The predictive ability of DFA and ACI to differentiate between cueing and no-cueing conditions was assessed using regularized logistic regressions and areas under the receiver operating characteristic curves (AUROC). Results. DFA and ACI were both significantly different among the cueing conditions. DFA and ACI were correlated (Pearson’s r = 0.78). Logistic regressions showed that DFA and ACI could differentiate between cueing/no cueing conditions with a high degree of confidence (AUROC = 1.0 and 0.96, respectively). Conclusion. Both DFA and ACI responded similarly to changes in cueing conditions and had comparable predictive power. This support the assumption that ACI could be used instead of DFA to assess the long-range complexity of continuous gait signals.

[1]  Peter J Beek,et al.  Online gait event detection using a large force platform embedded in a treadmill. , 2008, Journal of biomechanics.

[2]  Antonio M Lopez,et al.  Validity of four gait models to estimate walked distance from vertical COG acceleration. , 2008, Journal of applied biomechanics.

[3]  Philippe Terrier,et al.  Local dynamic stability of treadmill walking: intrasession and week-to-week repeatability. , 2013, Journal of biomechanics.

[4]  Philippe Terrier,et al.  Journal of Neuroengineering and Rehabilitation Open Access How Useful Is Satellite Positioning System (gps) to Track Gait Parameters? a Review , 2022 .

[5]  Jeffrey M. Hausdorff,et al.  Is walking a random walk? Evidence for long-range correlations in stride interval of human gait. , 1995, Journal of applied physiology.

[6]  S. Teixeira,et al.  Music Therapy and Dance as Gait Rehabilitation in Patients With Parkinson Disease: A Review of Evidence , 2019, Journal of geriatric psychiatry and neurology.

[7]  Rafael C González,et al.  Real-time gait event detection for normal subjects from lower trunk accelerations. , 2010, Gait & posture.

[8]  H E Stanley,et al.  Statistical properties of DNA sequences. , 1995, Physica A.

[9]  T. Chau,et al.  Measures of dynamic stability: Detecting differences between walking overground and on a compliant surface. , 2010, Human movement science.

[10]  Philippe Terrier,et al.  Could Local Dynamic Stability Serve as an Early Predictor of Falls in Patients with Moderate Neurological Gait Disorders? A Reliability and Comparison Study in Healthy Individuals and in Patients with Paresis of the Lower Extremities , 2014, PloS one.

[11]  Jaap H van Dieën,et al.  Sensitivity of trunk variability and stability measures to balance impairments induced by galvanic vestibular stimulation during gait. , 2011, Gait & posture.

[12]  D. Sternad,et al.  Slower speeds in patients with diabetic neuropathy lead to improved local dynamic stability of continuous overground walking. , 2000, Journal of biomechanics.

[13]  A. Daffertshofer,et al.  How to Sync to the Beat of a Persistent Fractal Metronome without Falling Off the Treadmill? , 2015, PloS one.

[14]  Bruce J. West,et al.  FRACTAL PHYSIOLOGY AND CHAOS IN MEDICINE , 1990 .

[15]  Fraser,et al.  Independent coordinates for strange attractors from mutual information. , 1986, Physical review. A, General physics.

[16]  Jaap H van Dieën,et al.  Ambulatory fall-risk assessment: amount and quality of daily-life gait predict falls in older adults. , 2015, The journals of gerontology. Series A, Biological sciences and medical sciences.

[17]  Jonathan B Dingwell,et al.  Adaptability of stride-to-stride control of stepping movements in human walking. , 2016, Journal of biomechanics.

[18]  G. Tack,et al.  Fractal fluctuations in spatiotemporal variables when walking on a self-paced treadmill. , 2017, Journal of biomechanics.

[19]  P. Terrier,et al.  Persistent and anti-persistent pattern in stride-to-stride variability of treadmill walking: influence of rhythmic auditory cueing. , 2012, Human movement science.

[20]  Philippe Terrier,et al.  Kinematic variability, fractal dynamics and local dynamic stability of treadmill walking , 2011, Journal of NeuroEngineering and Rehabilitation.

[21]  Jeffrey M. Hausdorff,et al.  Fractal dynamics in physiology: Alterations with disease and aging , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  P. Beek,et al.  Maximum Lyapunov exponents as predictors of global gait stability: a modelling approach. , 2012, Medical engineering & physics.

[23]  Nicolas Vuillerme,et al.  Local dynamic stability during gait for predicting falls in elderly people: A one-year prospective study , 2018, PloS one.

[24]  L. Allet,et al.  Hip muscle and hand-grip strength to differentiate between older fallers and non-fallers: a cross-sectional validity study , 2017, Clinical interventions in aging.

[25]  Bertrand Léger,et al.  Monitoring of Gait Quality in Patients With Chronic Pain of Lower Limbs , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  M. Rosenstein,et al.  A practical method for calculating largest Lyapunov exponents from small data sets , 1993 .

[27]  P. Terrier Fractal Fluctuations in Human Walking: Comparison Between Auditory and Visually Guided Stepping , 2015, Annals of Biomedical Engineering.

[28]  S. Kim,et al.  Rhythmic Auditory Cueing in Motor Rehabilitation for Stroke Patients: Systematic Review and Meta-Analysis. , 2016, Journal of music therapy.

[29]  F. Takens Detecting strange attractors in turbulence , 1981 .

[30]  Didier Delignières,et al.  Complexity Matching: Restoring the Complexity of Locomotion in Older People Through Arm-in-Arm Walking , 2018, Front. Physiol..

[31]  F. Riva,et al.  Estimating fall risk with inertial sensors using gait stability measures that do not require step detection. , 2013, Gait & posture.

[32]  Tom Chau,et al.  The Effects of Rhythmic Sensory Cues on the Temporal Dynamics of Human Gait , 2012, PloS one.

[33]  J. Dingwell,et al.  Nonlinear time series analysis of normal and pathological human walking. , 2000, Chaos.

[34]  A. Kuo,et al.  Active control of lateral balance in human walking. , 2000, Journal of biomechanics.

[35]  R. Tibshirani Regression Shrinkage and Selection via the Lasso , 1996 .

[36]  J. Hamill,et al.  Energetic Cost and Stability during Human Walking at the Preferred Stride Frequency , 1995 .

[37]  J. Dingwell,et al.  Dynamic stability of passive dynamic walking on an irregular surface. , 2007, Journal of biomechanical engineering.

[38]  J. Dingwell,et al.  Re-interpreting detrended fluctuation analyses of stride-to-stride variability in human walking. , 2010, Gait & posture.

[39]  Luis Mochizuki,et al.  Gait Stability and Aging , 2017 .

[40]  H. Abarbanel,et al.  Determining embedding dimension for phase-space reconstruction using a geometrical construction. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[41]  P. Terrier,et al.  GPS analysis of human locomotion: further evidence for long-range correlations in stride-to-stride fluctuations of gait parameters. , 2005, Human movement science.

[42]  Zainy M. H. Almurad,et al.  Evenly spacing in Detrended Fluctuation Analysis , 2016 .

[43]  S. Finch Lyapunov Exponents , 2007 .

[44]  Sina Mehdizadeh,et al.  The largest Lyapunov exponent of gait in young and elderly individuals: A systematic review. , 2018, Gait & posture.

[45]  Jeffrey M. Hausdorff,et al.  Footswitch system for measurement of the temporal parameters of gait. , 1995, Journal of biomechanics.

[46]  A. Daffertshofer,et al.  Tightening Up the Control of Treadmill Walking: Effects of Maneuverability Range and Acoustic Pacing on Stride-to-Stride Fluctuations , 2019, Front. Physiol..

[47]  Philippe Terrier,et al.  Effect of age on the variability and stability of gait: a cross-sectional treadmill study in healthy individuals between 20 and 69 years of age. , 2014, Gait & posture.

[48]  K. Torre,et al.  Fractal dynamics of human gait: a reassessment of the 1996 data of Hausdorff et al. , 2009, Journal of applied physiology.

[49]  P. Terrier,et al.  Non-linear dynamics of human locomotion: effects of rhythmic auditory cueing on local dynamic stability , 2012, Front. Physiol..

[50]  J. Dingwell,et al.  Dynamic stability of human walking in visually and mechanically destabilizing environments. , 2011, Journal of biomechanics.

[51]  P. Terrier Step-to-Step Variability in Treadmill Walking: Influence of Rhythmic Auditory Cueing , 2012, PloS one.

[52]  P. Terrier,et al.  Maximum Lyapunov exponent revisited: Long-term attractor divergence of gait dynamics is highly sensitive to the noise structure of stride intervals. , 2018, Gait & posture.

[53]  Ryan L. Meidinger,et al.  Fractal analysis of gait in people with Parkinson's disease: three minutes is not enough. , 2019, Gait & posture.

[54]  P. Beek,et al.  Assessing the stability of human locomotion: a review of current measures , 2013, Journal of The Royal Society Interface.