Annals of Biomedical Engineering

, Volume 44, Issue 9, pp 2785–2793 | Cite as

Fractal Fluctuations in Human Walking: Comparison Between Auditory and Visually Guided Stepping

  • Philippe TerrierEmail author


In human locomotion, sensorimotor synchronization of gait consists of the coordination of stepping with rhythmic auditory cues (auditory cueing, AC). AC changes the long-range correlations among consecutive strides (fractal dynamics) into anti-correlations. Visual cueing (VC) is the alignment of step lengths with marks on the floor. The effects of VC on the fluctuation structure of walking have not been investigated. Therefore, the objective was to compare the effects of AC and VC on the fluctuation pattern of basic spatiotemporal gait parameters. Thirty-six healthy individuals walked 3 × 500 strides on an instrumented treadmill with augmented reality capabilities. The conditions were no cueing (NC), AC, and VC. AC included an isochronous metronome. For VC, projected stepping stones were synchronized with the treadmill speed. Detrended fluctuation analysis assessed the correlation structure. The coefficient of variation (CV) was also assessed. The results showed that AC and VC similarly induced a strong anti-correlated pattern in the gait parameters. The CVs were similar between the NC and AC conditions but substantially higher in the VC condition. AC and VC probably mobilize similar motor control pathways and can be used alternatively in gait rehabilitation. However, the increased gait variability induced by VC should be considered.


Human locomotion Motor control Sensorimotor synchronization Gait variability Auditory cueing Visual cueing Long-range correlations 



Auditory cueing


No cueing


Visual cueing


Detrended fluctuation analysis


Coefficient of variation



The author warmly thanks Emilie Du Fay de Lavallaz for his valuable support in bibliographical research and Vincent Bonvin for his help in data collection. The study was funded by the Swiss accident insurance company SUVA, by the Clinique Romande de Réadaptation (CRR), and by the Institute for Research in Rehabilitation (IRR). The IRR is funded by the State of Valais and the City of Sion. Study funders had no role in the collection, analysis, and interpretation of data; in the writing of the manuscript; and in the decision to submit the manuscript for publication.

Supplementary material

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  1. 1.
    Accardo, A., M. Affinito, M. Carrozzi, and F. Bouquet. Use of the fractal dimension for the analysis of electroencephalographic time series. Biol. Cybern. 77:339–350, 1997.CrossRefPubMedGoogle Scholar
  2. 2.
    Azulay, J.-P., S. Mesure, B. Amblard, O. Blin, I. Sangla, and J. Pouget. Visual control of locomotion in Parkinson’s disease. Brain 122:111–120, 1999.CrossRefPubMedGoogle Scholar
  3. 3.
    Bauby, C. E., and A. D. Kuo. Active control of lateral balance in human walking. J. Biomech. 33:1433–1440, 2000.CrossRefPubMedGoogle Scholar
  4. 4.
    Chang, M. D., S. Shaikh, and T. Chau. Effect of treadmill walking on the stride interval dynamics of human gait. Gait Posture 30:431–435, 2009.CrossRefPubMedGoogle Scholar
  5. 5.
    Delignieres, D., and K. Torre. Fractal dynamics of human gait: a reassessment of the 1996 data of Hausdorff et al. J. Appl. Physiol. 106:1272–1279, 2009.CrossRefPubMedGoogle Scholar
  6. 6.
    Dingwell, J. B., and J. P. Cusumano. Re-interpreting detrended fluctuation analyses of stride-to-stride variability in human walking. Gait Posture 32:348–353, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Dingwell, J. B., and J. P. Cusumano. Identifying stride-to-stride control strategies in human treadmill walking. PLoS ONE 10:e0124879, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Dingwell, J. B., and L. C. Marin. Kinematic variability and local dynamic stability of upper body motions when walking at different speeds. J. Biomech. 39:444–452, 2006.CrossRefPubMedGoogle Scholar
  9. 9.
    Dingwell, J. B., J. John, and J. P. Cusumano. Do humans optimally exploit redundancy to control step variability in walking? PLoS Comput. Biol. 6:e1000856, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Eke, A., P. Herman, L. Kocsis, and L. Kozak. Fractal characterization of complexity in temporal physiological signals. Physiol. Meas. 23:R1, 2002.CrossRefPubMedGoogle Scholar
  11. 11.
    Hamacher, D., F. Herold, P. Wiegel, D. Hamacher, and L. Schega. Brain activity during walking: a systematic review. Neurosci. Biobehav. R. 57:310–327, 2015.CrossRefGoogle Scholar
  12. 12.
    Hausdorff, J. M. Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum. Mov. Sci. 26:555–589, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Hausdorff, J. M. Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hausdorff, J. M., C. K. Peng, Z. Ladin, J. Y. Wei, and A. L. Goldberger. Is walking a random walk? Evidence for long-range correlations in stride interval of human gait. J. Appl. Physiol. 78:349–358, 1995.PubMedGoogle Scholar
  15. 15.
    Hausdorff, J. M., A. Lertratanakul, M. E. Cudkowicz, A. L. Peterson, D. Kaliton, and A. L. Goldberger. Dynamic markers of altered gait rhythm in amyotrophic lateral sclerosis. J. Appl. Physiol. 88:2045–2053, 2000.PubMedGoogle Scholar
  16. 16.
    Hausdorff, J. M., J. Lowenthal, T. Herman, L. Gruendlinger, C. Peretz, and N. Giladi. Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease. Eur. J. Neurosci. 26:2369–2375, 2007.CrossRefPubMedGoogle Scholar
  17. 17.
    Heeren, A., M. W. van Ooijen, A. C. Geurts, B. L. Day, T. W. Janssen, P. J. Beek, M. Roerdink, and V. Weerdesteyn. Step by step: a proof of concept study of C-Mill gait adaptability training in the chronic phase after stroke. J. Rehabil. Med. 45:616–622, 2013.CrossRefPubMedGoogle Scholar
  18. 18.
    Jordan, K., J. H. Challis, and K. M. Newell. Walking speed influences on gait cycle variability. Gait Posture 26:128–134, 2007.CrossRefPubMedGoogle Scholar
  19. 19.
    Lewis, G. N., W. D. Byblow, and S. E. Walt. Stride length regulation in Parkinson’s disease: the use of extrinsic, visual cues. Brain 123(Pt 10):2077–2090, 2000.CrossRefPubMedGoogle Scholar
  20. 20.
    Mandelbrot, B. B. Les objets fractals: forme, hasard et dimension. Flammarion 10:422–437, 1975.Google Scholar
  21. 21.
    Mandelbrot, B. B., and J. W. Van Ness. Fractional Brownian motions, fractional noises and applications. SIAM Rev 10:422–437, 1968.CrossRefGoogle Scholar
  22. 22.
    Maraun, D., H. W. Rust, and J. Timmer. Tempting long-memory—on the interpretation of DFA results. Nonlinear Proc. Geophys. 11:495–503, 2004.CrossRefGoogle Scholar
  23. 23.
    Marmelat, V., K. Torre, P. J. Beek, and A. Daffertshofer. Persistent fluctuations in stride intervals under fractal auditory stimulation. PLoS ONE 9:e91949, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Miall, R. C., and D. M. Wolpert. Forward models for physiological motor control. Neural Netw. 9:1265–1279, 1996.CrossRefPubMedGoogle Scholar
  25. 25.
    Nascimento, L. R., C. Q. de Oliveira, L. Ada, S. M. Michaelsen, and L. F. Teixeira-Salmela. Walking training with cueing of cadence improves walking speed and stride length after stroke more than walking training alone: a systematic review. J. Physiother. 61:10–15, 2015.CrossRefPubMedGoogle Scholar
  26. 26.
    O’Connor, S. M., H. Z. Xu, and A. D. Kuo. Energetic cost of walking with increased step variability. Gait Posture 36:102–107, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Owings, T. M., and M. D. Grabiner. Variability of step kinematics in young and older adults. Gait Posture 20:26–29, 2004.CrossRefPubMedGoogle Scholar
  28. 28.
    Peng, C.-K., S. V. Buldyrev, S. Havlin, M. Simons, H. E. Stanley, and A. L. Goldberger. Mosaic organization of DNA nucleotides. Phys. Rev. E 49:1685, 1994.CrossRefGoogle Scholar
  29. 29.
    Peng, C. K., S. Havlin, H. E. Stanley, and A. L. Goldberger. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 5:82–87, 1995.CrossRefPubMedGoogle Scholar
  30. 30.
    Peper, C. L. E., M. J. de Dreu, and M. Roerdink. Attuning one’s steps to visual targets reduces comfortable walking speed in both young and older adults. Gait Posture 41:830–834, 2015.CrossRefPubMedGoogle Scholar
  31. 31.
    Repp, B. H. Sensorimotor synchronization: a review of the tapping literature. Psychon. Bull. Rev. 12:969–992, 2005.CrossRefPubMedGoogle Scholar
  32. 32.
    Repp, B. H., and Y.-H. Su. Sensorimotor synchronization: a review of recent research (2006–2012). Psychon. Bull. Rev. 20:403–452, 2013.CrossRefPubMedGoogle Scholar
  33. 33.
    Roerdink, M., B. H. Coolen, B. H. Clairbois, C. J. Lamoth, and P. J. Beek. Online gait event detection using a large force platform embedded in a treadmill. J. Biomech. 41:2628–2632, 2008.CrossRefPubMedGoogle Scholar
  34. 34.
    Roerdink, M., A. Daffertshofer, V. Marmelat, and P. J. Beek. How to sync to the beat of a persistent fractal metronome without falling off the treadmill? PLoS ONE 10:e0134148, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Rossignol, S., R. Dubuc, and J. P. Gossard. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86:89–154, 2006.CrossRefPubMedGoogle Scholar
  36. 36.
    Sejdic, E., Y. Fu, A. Pak, J. A. Fairley, and T. Chau. The effects of rhythmic sensory cues on the temporal dynamics of human gait. PLoS ONE 7:e43104, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Sidaway, B., J. Anderson, G. Danielson, L. Martin, and G. Smith. Effects of long-term gait training using visual cues in an individual with Parkinson disease. Phys. Ther. 86:186–194, 2006.PubMedGoogle Scholar
  38. 38.
    Terrier, P. Step-to-step variability in treadmill walking: influence of rhythmic auditory cueing. PLoS ONE 7:e47171, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Terrier, P., and O. Dériaz. Kinematic variability, fractal dynamics and local dynamic stability of treadmill walking. J. Neuroeng. Rehabil. 8:12, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Terrier, P., and O. Dériaz. Persistent and anti-persistent pattern in stride-to-stride variability of treadmill walking: influence of rythmic auditory cueing. Hum. Mov. Sci. 31:1585–1597, 2012.CrossRefPubMedGoogle Scholar
  41. 41.
    Terrier, P., and O. Dériaz. Nonlinear dynamics of human locomotion: effects of rhythmic auditory cueing on local dynamic stability. Front. Physiol. 4:230, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Terrier, P., V. Turner, and Y. Schutz. GPS analysis of human locomotion: further evidence for long-range correlations in stride-to-stride fluctuations of gait parameters. Hum. Mov. Sci. 24:97–115, 2005.CrossRefPubMedGoogle Scholar
  43. 43.
    Torre, K., D. Delignieres, and L. Lemoine. Detection of long-range dependence and estimation of fractal exponents through ARFIMA modelling. Brit. J. Math. Stat. Psychol. 60:85–106, 2007.CrossRefGoogle Scholar
  44. 44.
    van Ooijen, M. W., A. Heeren, K. Smulders, A. C. Geurts, T. W. Janssen, P. J. Beek, V. Weerdesteyn, and M. Roerdink. Improved gait adjustments after gait adaptability training are associated with reduced attentional demands in persons with stroke. Exp. Brain Res. 233:1007–1018, 2015.CrossRefPubMedGoogle Scholar
  45. 45.
    van Wegen, E. E., M. A. Hirsch, M. Huiskamp, and G. Kwakkel. Harnessing Cueing Training for Neuroplasticity in Parkinson Disease. Top. Geriatr. Rehabil. 30:46–57, 2014.CrossRefGoogle Scholar
  46. 46.
    West, B. J., and N. Scafetta. Nonlinear dynamical model of human gait. Phys. Rev. E 67:051917, 2003.CrossRefGoogle Scholar
  47. 47.
    Wittwer, J. E., K. E. Webster, and K. Hill. Music and metronome cues produce different effects on gait spatiotemporal measures but not gait variability in healthy older adults. Gait Posture 37:219–222, 2013.CrossRefPubMedGoogle Scholar
  48. 48.
    Zarrugh, M. Y., F. N. Todd, and H. J. Ralston. Optimization of energy expenditure during level walking. Eur. J. Appl. Physiol. Occup. Physiol. 33:293–306, 1974.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2016

Authors and Affiliations

  1. 1.IRRInstitute for Research in RehabilitationSionSwitzerland
  2. 2.Clinique romande de réadaptation SUVACareSionSwitzerland

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