Auditory Cue Based on the Golden Ratio Can Improve Gait Patterns in People with Parkinson's Disease

Valeria Belluscio, Marco Iosa, Giuseppe Vannozzi, Stefano Paravati, Antonella Peppe, Valeria Belluscio, Marco Iosa, Giuseppe Vannozzi, Stefano Paravati, Antonella Peppe

Abstract

The harmonic structure of walking relies on an irrational number called the golden ratio (ϕ): in healthy subjects, it coincides with the stride-to-stance ratio, and it is associated with a smooth gait modality. This smoothness is lost in people with Parkinson's disease (PD), due to deficiencies in the execution of movements. However, external auditory cues seem to facilitate movement, by enabling the timing of muscle activation, and helping in initiating and modulating motor output. Based on a harmonic fractal structure of gait, can the administration of an auditory cue based on individual's ϕ-rhythm improve, in acute, gait patterns in people with PD? A total of 20 participants (16 males, age 70.9 ± 8.4 years, Hoehn and Yahr stage-II) were assessed through stereophotogrammetry: gait spatio-temporal parameters, and stride-to-stance ratio were computed before, during, and after the ϕ-rhythm administration. Results show improvements in terms of stride length (p = 0.018), walking speed (p = 0.014), and toe clearance (p = 0.013) when comparing gait patterns before and after the stimulus. Furthermore, the stride-to-stance ratio seems to correlate with almost all spatio-temporal parameters, but it shows the main changes in the before-during rhythm comparison. In conclusion, ϕ-rhythm seems an effective cue able to compensate for defective internal rhythm of the basal ganglia in PD.

Keywords: external rhythm; fractal; gait analysis; internal rhythm; locomotion; motor adaptation; physiological rhythm; walking.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Marker positioning based on Modified Davis Protocol. Letters R and L at the beginning of the acronyms correspond to the body side (right and left). SHO: acromio-clavicular joint; ASI: anterior superior iliac spine; THI: thigh; KNE: lateral epicondyle; TIB: tibiae; ANK: lateral malleoli; TOE: second metatarsal head; C7: 7th cervical vertebrae; T11: 11th thoracic vertebrae; ELB: elbow; WRB: wrist bar pinkie side; HEE: calcaneus.
Figure 2
Figure 2
Schematics of study design. T0 = before GR administration. T1= during GR administration. T2 = after GR administration.
Figure 3
Figure 3
Walking speed. T0 = before Golden Ratio administration; T1 = during Golden Ratio administration; T2 = after Golden Ratio administration; * indicates statistically significant differences.
Figure 4
Figure 4
Stride length, toe clearance and maximum height of malleoli are reported; T0 = before GR administration; T1 = during GR administration; T2 = after GR administration; MA = more affected side; LA = less affected side; * indicates statistically significant differences.

References

    1. Dauer W., Przedborski S. Parkinson’s disease: Mechanisms and models. Neuron. 2003;39:889–909. doi: 10.1016/S0896-6273(03)00568-3.
    1. Jankovic J. Parkinson’s disease: Clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry. 2008;79:368–376. doi: 10.1136/jnnp.2007.131045.
    1. Morris M.E., Iansek R., Matyas T.A., Summers J.J. Stride length regulation in Parkinson’s disease: Normalization strategies and underlying mechanisms. Brain. 1996;119:551–568. doi: 10.1093/brain/119.2.551.
    1. Peppe A., Chiavalon C., Pasqualetti P., Crovato D., Caltagirone C. Does gait analysis quantify motor rehabilitation efficacy in Parkinson’s disease patients? Gait Posture. 2007;26:452–462. doi: 10.1016/j.gaitpost.2006.11.207.
    1. Luria A.R. The Frontal Lobes and the Regulation of Behavior. Academic Press, Inc.; Cambridge, MA, USA: 1973.
    1. Takahashi H., Takada Y., Nagai N., Urano T., Takada A. Serotonergic neurons projecting to hippocampus activate locomotion. Brain Res. 2000;869:194–202. doi: 10.1016/S0006-8993(00)02385-4.
    1. Iosa M., Morone G., Fusco A., Marchetti F., Caltagirone C., Paolucci S., Peppe A. Loss of fractal gait harmony in Parkinson’s Disease. Clin. Neurophysiol. 2016;127:1540–1546. doi: 10.1016/j.clinph.2015.11.016.
    1. Nombela C., Hughes L.E., Owen A.M., Grahn J.A. Into the groove: Can rhythm influence Parkinson’s disease? Neurosci. Biobehav. Rev. 2013;37:2564–2570. doi: 10.1016/j.neubiorev.2013.08.003.
    1. Ebersbach G., Sojer M., Valldeoriola F., Wissel J., Müller J., Tolosa E., Poewe W. Comparative analysis of gait in Parkinson’s disease, cerebellar ataxia and subcortical arteriosclerotic encephalopathy. Brain. 1999;122:1349–1355. doi: 10.1093/brain/122.7.1349.
    1. Asai Y., Nomura T., Sato S., Tamaki A., Matsuo Y., Mizukura I., Abe K. A coupled oscillator model of disordered interlimb coordination in patients with Parkinson’s disease. Biol. Cybern. 2003;88:152–162. doi: 10.1007/s00422-002-0371-9.
    1. Muthukrishnan N., Abbas J.J., Shill H.A., Krishnamurthi N. Cueing paradigms to improve gait and posture in parkinson’s disease: A narrative review. Sensors. 2019;19:5468. doi: 10.3390/s19245468.
    1. Thaut M.H., McIntosh G.C., Rice R.R., Miller R.A., Rathbun J., Brault J.M. Rhythmic auditory stimulation in gait training for Parkinson’s disease patients. Mov. Disord. 1996;11:193–200. doi: 10.1002/mds.870110213.
    1. Thaut M.H. The future of music in therapy and medicine. Ann. N. Y. Acad. Sci. 2005;1060:303–308. doi: 10.1196/annals.1360.023.
    1. McIntosh G.C., Brown S.H., Rice R.R., Thaut M.H. Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry. 1997;62:22–26. doi: 10.1136/jnnp.62.1.22.
    1. Ashoori A., Eagleman D.M., Jankovic J. Effects of auditory rhythm and music on gait disturbances in Parkinson’s disease. Front. Neurol. 2015;6:234. doi: 10.3389/fneur.2015.00234.
    1. Hausdorff J.M., Lowenthal J., Herman T., Gruendlinger L., Peretz C., Giladi N. Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease. Eur. J. Neurosci. 2007;26:2369–2375.
    1. Lim I., van Wegen E., de Goede C., Deutekom M., Nieuwboer A., Willems A., Jones D., Rochester L., Kwakkel G. Effects of external rhythmical cueing on gait in patients with Parkinson’s disease: A systematic review. Clin. Rehabil. 2005;19:695–713. doi: 10.1191/0269215505cr906oa.
    1. Rochester L., Hetherington V., Jones D., Nieuwboer A., Willems A.M., Kwakkel G., Van Wegen E. 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. 2005;86:999–1006. doi: 10.1016/j.apmr.2004.10.040.
    1. Spaulding S.J., Barber B., Colby M., Cormack B., Mick T., Jenkins M.E. Cueing and gait improvement among people with Parkinson’s disease: A meta-analysis. Arch. Phys. Med. Rehabil. 2013;94:562–570. doi: 10.1016/j.apmr.2012.10.026.
    1. Willems A.M., Nieuwboer A., Chavret F., Desloovere K., Dom R., Rochester L., Jones D., Kwakkel G., Van Wegen E. The use of rhythmic auditory cues to influence gait in patients with Parkinson’s disease, the differential effect for freezers and non-freezers, an explorative study. Disabil. Rehabil. 2006;28:721–728. doi: 10.1080/09638280500386569.
    1. Iosa M., Fusco A., Marchetti F., Morone G., Caltagirone C., Paolucci S., Peppe A. The golden ratio of gait harmony: Repetitive proportions of repetitive gait phases. Biomed Res. Int. 2013 doi: 10.1155/2013/918642.
    1. Bilney B., Morris M., Webster K. Concurrent related validity of the GAITRite† walkway system for quantification of the spatial and temporal parameters of gait. Gait Posture. 2003;17:68–74. doi: 10.1016/S0966-6362(02)00053-X.
    1. Steinert A., Sattler I., Otte K., Röhling H., Mansow-Model S., Müller-Werdan U. Using new camera-based technologies for gait analysis in older adults in comparison to the established GAITrite system. Sensors. 2020;20:125.
    1. Cohen J. Statistical Power Analysis. Curr. Dir. Psychol. Sci. 1992;1:98–101. doi: 10.1111/1467-8721.ep10768783.
    1. Folstein M.F., Folstein S.E., McHugh P.R. Mini-Mental State: A practical method for grading the cognitive state of patients fro clinicians. J. Psychiatr. 1975;12:162–167. doi: 10.3744/snak.2003.40.2.021.
    1. Goetz C.G., Tilley B.C., Shaftman S.R., Stebbins G.T., Fahn S., Martinez-Martin P., Poewe W., Sampaio C., Stern M.B., Dodel R., et al. Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov. Disord. 2008;23:2129–2170. doi: 10.1002/mds.22340.
    1. Tinetti M.E. Performance-Oriented Assessment of Mobility Problems in Elderly Patients. J. Am. Geriatr. Soc. 1986;34:119–126. doi: 10.1111/j.1532-5415.1986.tb05480.x.
    1. Jenkinson C., Fitzpatrick R., Peto V., Greenhall R., Hyman N. The Parkinson’s disease questionnaire (PDQ-39): Development and validation of a Parkinson’s disease summary index score. Age Ageing. 1997;26:353–357. doi: 10.1093/ageing/26.5.353.
    1. Powell L.E., Moore D.S., Ellis R., Kosma M., Fabre J.M., McCarter K.S., Wood R.H. The Activities-specific Balance Confidence ( ABC ) Scale * The Activities-specific Balance Confidence (ABC) Scale. Res. Q. Exerc. Sport. 2011;50:545–554.
    1. Davis R.B., Õunpuu S., Tyburski D., Gage J.R. A gait analysis data collection and reduction technique. Hum. Mov. Sci. 1991;10:575–587. doi: 10.1016/0167-9457(91)90046-Z.
    1. Iosa M., Morone G., Paolucci S. Phi in physiology, psychology and biomechanics: The golden ratio between myth and science. BioSystems. 2018;165:31–39. doi: 10.1016/j.biosystems.2018.01.001.
    1. Alcock L., Galna B., Lord S., Rochester L. Characterisation of foot clearance during gait in people with early Parkinson׳s disease: Deficits associated with a dual task. J. Biomech. 2016;49:2763–2769. doi: 10.1016/j.jbiomech.2016.06.007.

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