Neurological Sciences

, Volume 31, Issue 4, pp 423–430 | Cite as

Three-dimensional motion analysis of the effects of auditory cueing on gait pattern in patients with Parkinson’s disease: a preliminary investigation

  • Alessandro Picelli
  • Maruo Camin
  • Michele Tinazzi
  • Antonella Vangelista
  • Alessandro Cosentino
  • Antonio Fiaschi
  • Nicola SmaniaEmail author
Original Article


Auditory cueing enhances gait in parkinsonian patients. Our aim was to evaluate its effects on spatiotemporal (stride length, stride time, cadence, gait speed, single and double support duration) kinematic (range of amplitude of the hip, knee and ankle joint angles registered in the sagittal plane) and kinetic (maximal values of the hip and ankle joint power) gait parameters using three-dimensional motion analysis. Eight parkinsonian patients performed 12 walking tests: 3 repetitions of 4 conditions (normal walking, 90, 100, and 110% of the mean cadence at preferred pace cued walking). Subjects were asked to uniform their cadence to the cueing rhythm. In the presence of auditory cues stride length, cadence, gait speed and ratio single/double support duration increased. Range of motion of the ankle joint decreased and the maximal values within the pull-off phase of the hip joint power increased. Thus, auditory cues could improve gait modifying motor strategy in parkinsonian patients.


Auditory cueing Gait Motion analysis Parkinson’s disease 


Conflict of interest statement

The authors declare that they have no conflict of interest related to the publication of this manuscript.


  1. 1.
    Meara J, Bhowmick BK (2000) Parkinson’s disease and Parkinsonism in the elderly: introduction. In: Meara J, Koller WC (eds) Parkinson’s disease and Parkinsonism in the elderly, 1st edn. Cambridge University Press, CambridgeGoogle Scholar
  2. 2.
    Morris ME, Iansek R, Matyas TA, Summers JL (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117:1169–1181CrossRefPubMedGoogle Scholar
  3. 3.
    Knuitsson F (1972) An analysis of parkinsonian gait. Brain 95:475–486CrossRefGoogle Scholar
  4. 4.
    Howe TE, Lövgreen B, Cody FW, Ashton VJ, Oldham JA (2003) Auditory cues can modify the gait of persons with early-stage Parkinson’s disease: a method for enhancing parkinsonian walking performance? Clin Rehabil 17:363–367CrossRefPubMedGoogle Scholar
  5. 5.
    Del Olmo MF, Arias P, Furio MC, Pozo MA, Cudeiro J (2006) Evaluation of the effect of training using auditory stimulation on rhythmic movement in parkinsonian patients: a combined motor and [F]-FDG PET study. Parkinsonism Relat Disord 12:155–164CrossRefPubMedGoogle Scholar
  6. 6.
    Lewis G, Byblow W, Walt S (2000) Stride length regulation in Parkinson’s disease: the use of extrinsic, visual cues. Brain 123:2077–2090CrossRefPubMedGoogle Scholar
  7. 7.
    Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119:551–568CrossRefPubMedGoogle Scholar
  8. 8.
    Nieuwboer A, Kwakkel G, Rochester L, Jones D, van Wegen E, Willems AM, Chavret F, Hetherington V, Baker K, Lim I (2006) Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 78:134–140CrossRefGoogle Scholar
  9. 9.
    Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G, Van Wegen E (2005) The effect of external rhythmic cues (auditory and visual) on walking during a functional task in homes of people with Parkinson’s disease. Arch Phys Med Rehabil 86:999–1006CrossRefPubMedGoogle Scholar
  10. 10.
    Sidaway B, Anderson J, Danielson G, Martin L, Smith G (2006) Effects of long-term gait training using visual cues in an individual with Parkinson disease. Phys Ther 86:186–194PubMedGoogle Scholar
  11. 11.
    Suteerawattananon M, Morris GS, Etnyre BR, Jankovic J, Protas EJ (2004) Effects of visual and auditory cues on gait in individuals with Parkinson’s disease. J Neurol Sci 219:63–69CrossRefPubMedGoogle Scholar
  12. 12.
    Baker K, Rochester L, Nieuwboer A (2007) The immediate effect of attentional, auditory, and a combined cue strategy on gait during single and dual tasks in Parkinson’s disease. Arch Phys Med Rehabil 88:1593–1600CrossRefPubMedGoogle Scholar
  13. 13.
    Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P (2009) Rehabilitation treatment of gait in patients with Parkinson’s disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord 24:1139–1143CrossRefPubMedGoogle Scholar
  14. 14.
    Koelewijn T, Bronkhorst A, Theeuwes J (2009) Competition between auditory and visual spatial cues during visual task performance. Exp Brain Res 195:593–602CrossRefPubMedGoogle Scholar
  15. 15.
    Rochester L, Burn DJ, Woods G, Godwin J, Nieuwboer A (2009) Does auditory rhythmical cueing improve gait in people with Parkinson’s disease and cognitive impairment? A feasibility study. Mov Disord 24:839–845CrossRefPubMedGoogle Scholar
  16. 16.
    Ledger S, Galvin R, Lynch D, Stokes EK (2008) A randomised controlled trial evaluating the effect of an individual auditory cueing device on freezing and gait speed in people with Parkinson’s disease. BMC Neurol 8:46CrossRefPubMedGoogle Scholar
  17. 17.
    Akamatsu T, Fukuyama H, Kawamata T (2008) The effects of visual, auditory, and mixed cues on choice reaction in Parkinson’s disease. J Neurol Sci 269:118–125CrossRefPubMedGoogle Scholar
  18. 18.
    Rubinstein TC, Giladi N, Hausdorff JM (2002) The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson’s disease. Mov Disord 17:1148–1160CrossRefPubMedGoogle Scholar
  19. 19.
    McIntosh GC, Brown SH, Rice RR, Thaut MH (1997) Rhythmic auditory motor facilitation of gait patterns in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:22–26CrossRefPubMedGoogle Scholar
  20. 20.
    Morris ME, Iansek R, Summers JJ, Matyas TA (1995) Motor control considerations for the rehabilitation of gait in Parkinson’s disease. In: Glencross DJ, Piek JP (eds) Motor control and sensory motor integration: issue and directions, 1st edn. Elsevier, AmsterdamGoogle Scholar
  21. 21.
    Robertson C, Flowers KA (1990) Motor set in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:583–592CrossRefPubMedGoogle Scholar
  22. 22.
    Azulay JP, Van Deni BC, Mestre D, Blin O, Sangla I, Pouget J, Sterratrice G (1996) Automatic motion analysis of gait in patients with Parkinson disease: effects of levodopa and visual stimulations. Rev Neurol 152:128–134PubMedGoogle Scholar
  23. 23.
    Morris ME, Iansek R, McGinley J, Matyas T, Huxham F (2005) Three dimensional gait biomechanics in Parkinson’s disease: evidence for a centrally mediated amplitude regulation disorder. Mov Disord 1:40–50CrossRefGoogle Scholar
  24. 24.
    Van Wegen E, De Goede C, Lim I, Rietberg M, Nieuwboer A, Willems A, Jones D, Rochester L, Hetherington V, Berendse H, Zijlmans J, Wolters E, Kwakkel G (2006) The effect of rhythmic somatosensory cueing on gait in patients with Parkinson’s disease. J Neurol Sci 248:210–214CrossRefPubMedGoogle Scholar
  25. 25.
    Lim I, van Wegen E, de Goede C, Deutekom M, Nieuwboer A, Willems A, Jones D, Rochester L, Kwakkel G (2005) Effects of external rhythmical cueing on gait in patients with Parkinson’s disease: a systematic review. Clin Rehabil 19:695–713CrossRefPubMedGoogle Scholar
  26. 26.
    Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedGoogle Scholar
  27. 27.
    Berg KO, Wood-Dauphinee SL, Williams JI, Maki B (1992) Measuring balance in the elderly: validation of an instrument. Can J Public Health 83:S7–S11PubMedGoogle Scholar
  28. 28.
    Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  29. 29.
    Davis RB, Õunpuu S, Tyburki D, Cage JR (1991) A gait analysis data collection and reduction technique. Hum Mov Sci 10:575–587CrossRefGoogle Scholar
  30. 30.
    Peppe A, Chiavalon C, Pasqualetti P, Crovato D, Caltagirone C (2007) Does gait analysis quantify motor rehabilitation efficacy in Parkinson’s disease patients? Gait Posture 26:452–462CrossRefPubMedGoogle Scholar
  31. 31.
    Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease, 1st edn. Macmillan, Florham ParkGoogle Scholar
  32. 32.
    Arias P, Cudeiro J (2008) Effects of rhythmic sensory stimulation (auditory, visual) on gait in Parkinson’s disease patients. Exp Brain Res 186:589–601CrossRefPubMedGoogle Scholar
  33. 33.
    Enzensberger W, Oberlander U, Stecker K (1997) Metronome therapy in patients with Parkinson’s disease. Nervenarzt 68:972–977CrossRefPubMedGoogle Scholar
  34. 34.
    Richards CL, Malouin F, Bédard PJ, Cioni M (1992) Changes induced by l-dopa and sensory cues on the gait of parkinsonian patients. In: Wollacot M, Horak F (eds) Posture and gait: control mechanisms, 1st edn. University of Oregon books, EugeneGoogle Scholar
  35. 35.
    Chen Y, Repp BH, Patel A (2002) Spectral decomposition of variability in synchronization and continuation tapping: comparison between auditory and visual pacing feedback conditions. Hum Mov Sci 21:515–532CrossRefPubMedGoogle Scholar
  36. 36.
    Paltsev YI, Elner AM (1967) Change in the functional state of the segmental apparatus of the spinal cord under the influence of sound stimuli and its role in voluntary movement. Biophysics 12:1219–1226Google Scholar
  37. 37.
    Rossignol S, Melvill Jones G (1976) Audio-spinal influences in man studied by the H-reflex and its possible role on rhythmic movement synchronized to sound. Electroencephalogr Clin Neurophysiol 41:83–92CrossRefPubMedGoogle Scholar
  38. 38.
    Dietz V, Leenders KL, Colombo G (1997) Leg muscle activation during gait in Parkinson’s disease:influence of body unloading. Electroencephalogr Clin Neurophysiol 105:400–405CrossRefPubMedGoogle Scholar
  39. 39.
    Cioni M, Richards CL, Malouin F, Bedard PJ, Lemieux R (1997) Characteristics of the electromyographic patterns of lower limb muscles during gait in patients with Parkinson’s disease when OFF and ON l-dopa treatment. Ital J Neurol Sci 18:195–208CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Alessandro Picelli
    • 1
    • 2
  • Maruo Camin
    • 1
    • 2
  • Michele Tinazzi
    • 2
    • 3
  • Antonella Vangelista
    • 2
    • 4
  • Alessandro Cosentino
    • 4
  • Antonio Fiaschi
    • 2
    • 5
  • Nicola Smania
    • 1
    • 2
    • 6
    Email author
  1. 1.Neuromotor and Cognitive Rehabilitation Research CentreUniversity of VeronaVeronaItaly
  2. 2.Department of Neurological and Visual SciencesUniversity of VeronaVeronaItaly
  3. 3.Neurology Unit“Maggiore” HospitalVeronaItaly
  4. 4.Rehabilitation Unit “C. Santi”Polyfunctional Centre Don CalabriaVeronaItaly
  5. 5.IRCCS, S. CamilloVeniceItaly
  6. 6.Rehabilitation Unit“G.B. Rossi” University HospitalVeronaItaly

Personalised recommendations