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Gait asymmetry in patients with Parkinson’s disease and elderly fallers: when does the bilateral coordination of gait require attention?

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Abstract

While it is known that certain pathologies may impact on left–right symmetry of gait, little is known about the mechanisms that contribute to gait symmetry or how high in the hierarchy of the control of gait symmetry is regulated in humans. To assess the contribution of cognitive function to gait symmetry, we measured gait asymmetry (GA) in three subject groups, patients with Parkinson’s disease (PD, n = 21), idiopathic elderly fallers (n = 15), and healthy elderly controls (n = 11). All subjects walked under two walking conditions: usual walking and dual tasking (cognitive loading) condition. For each subject, the swing time (SW) was calculated and averaged across strides for the left and right feet (SWL and SWR). GA was defined as: \( 100 \times {\left| {\ln ({\text{SWR}}/{\text{SWL}})} \right|.} \) For both the PD patients and the elderly fallers GA values were significantly higher during the usual walking condition, as compared with the control group (< 0.01). In addition, for both the PD patients and the elderly fallers, GA significantly increased when they walked and performed a dual task, compared with the usual walking condition (< 0.003). In contrast, dual tasking did not affect the GA of the healthy controls (= 0.518). GA was associated with gait speed and gait variability, but no correlations were found between GA and the asymmetry of the classic PD motor symptoms. Thus, the results suggest that the ability to generate a steady, rhythmic walk with a bilaterally coordinated gait does not rely heavily on mental attention and cognitive resources in healthy older adults. In contrast, however, when gait becomes impaired and less automatic, GA apparently relies on cognitive input and attention.

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References

  • Auriel E, Hausdorff JM, Herman T, Simon ES, Giladi N (2006) Effects of methylphenidate on cognitive function and gait in patients with Parkinson’s disease: a pilot study. Clin Neuropharmacol 29:15–17

    Article  PubMed  CAS  Google Scholar 

  • Baltadjieva R, Giladi N, Gruendlinger L, Peretz C, Hausdorff JM (2006) Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson’s disease. Eur J Neurosci (in press)

  • Bazner H, Oster M, Daffertshofer M, Hennerici M (2000) Assessment of gait in subcortical vascular encephalopathy by computerized analysis: a cross-sectional and longitudinal study. J Neurol 247:841–849

    Article  PubMed  CAS  Google Scholar 

  • Blin O, Ferrandez AM, Serratrice G (1990) Quantitative analysis of gait in Parkinson patients: increased variability of stride length. J Neurol Sci 98:91–97

    Article  PubMed  CAS  Google Scholar 

  • Bloem BR, Valkenburg VV, Slabbekoorn M, Gert vD (2001) The multiple tasks test.Strategies in Parkinson’s disease. Exp Brain Res 137:478–486

    Article  PubMed  CAS  Google Scholar 

  • Bloem BR, Steijns JA, Smits-Engelsman BC (2003) An update on falls. Curr Opin Neurol 16:15–26

    Article  PubMed  Google Scholar 

  • Bond JM, Morris M (2000) Goal-directed secondary motor tasks: their effects on gait in subjects with Parkinson disease. Arch Phys Med Rehabil 81:110–116

    PubMed  CAS  Google Scholar 

  • Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG (1998) Verbal fluency task affects gait in Parkinson’s disease with motor freezing. J Geriatr Psychiatry Neurol 11:181–185

    PubMed  CAS  Google Scholar 

  • Dietz V (2002) Do human bipeds use quadrupedal coordination? Trends Neurosci 25:462–467

    Article  PubMed  Google Scholar 

  • Dietz V, Zijlstra W, Duysens J (1994) Human neuronal interlimb coordination during split-belt locomotion. Exp Brain Res 101:513–520

    Article  PubMed  CAS  Google Scholar 

  • Dwolatzky T, Whitehead V, Doniger GM, Simon ES, Schweiger A, Jaffe D, Chertkow H (2003) Validity of a novel computerized cognitive battery for mild cognitive impairment. BMC Geriatr 3:4

    Google Scholar 

  • Fahn S, Elton R, Members of the UPDRS development committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne D, Goldstein M (eds) Recent developments in Parkinson’s disease. MacMillan Health Care Information, Florham Park, pp 153–163

  • 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 12:189–198

    Article  PubMed  CAS  Google Scholar 

  • Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger L, Hausdorff JM (2005) Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson’s disease. Mov Disord 20:1109–1114

    Article  PubMed  Google Scholar 

  • Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39

    Article  PubMed  CAS  Google Scholar 

  • Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brookhardt J, Mountcastle G (eds) Handbook of physiology. American Physiological Society, Bethesda, pp 1179–1236

    Google Scholar 

  • Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J NeuroEng Rehabil 2. DOI 10.1186/1743-0003-2-19

  • Hausdorff JM, Cudkowicz ME, Firtion R, Wei JY, Goldberger AL (1998) Gait variability and basal ganglia disorders: stride-to-stride variations of gait cycle timing in Parkinson’s disease and Huntington’s disease. Mov Disord 13:428–437

    Article  PubMed  CAS  Google Scholar 

  • Hausdorff JM, Rios D, Edelberg HK (2001) Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 82:1050–1056

    Article  PubMed  CAS  Google Scholar 

  • Hausdorff JM, Yogev G, Springer S, Simon ES, Giladi N (2005) Walking is more like catching than tapping: gait in the elderly as a complex cognitive task. Exp Brain Res 164:541–548

    Article  PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    Article  PubMed  CAS  Google Scholar 

  • Jensen L, Prokop T, Dietz V (1998) Adaptational effects during human split-belt walking: influence of afferent input. Exp Brain Res 118:126–130

    Article  PubMed  CAS  Google Scholar 

  • Kjaerulff O, Kiehn O (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16:5777–5794

    PubMed  CAS  Google Scholar 

  • Lin PY, Yang YR, Cheng SJ, Wang RY (2006) The relation between ankle impairments and gait velocity and symmetry in people with stroke. Arch Phys Med Rehabil 87:562–568

    Article  PubMed  Google Scholar 

  • Lundin-Olsson L, Nyberg L, Gustafson Y (1997) “Stops walking when talking” as a predictor of falls in elderly people. Lancet 349:617

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687–717

    PubMed  CAS  Google Scholar 

  • Miller RA, Thaut MH, McIntosh GC, Rice RR (1996) Components of EMG symmetry and variability in parkinsonian and healthy elderly gait. Electroencephalogr Clin Neurophysiol 101:1–7

    Article  PubMed  CAS  Google Scholar 

  • Morris ME, Iansek R, Matyas TA, Summers JJ (1994a) Ability to modulate walking cadence remains intact in Parkinson’s disease. J Neurol Neurosurg Psychiatry 57:1532–1534

    Article  CAS  Google Scholar 

  • Morris ME, Iansek R, Matyas TA, Summers JJ (1994b) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117(Pt 5):1169–1181

    Article  Google Scholar 

  • Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119(Pt 2):551–568

    Article  PubMed  Google Scholar 

  • O’Shea S, Morris ME, Iansek R (2002) Dual task interference during gait in people with Parkinson disease: effects of motor versus cognitive secondary tasks. Phys Ther 82:888–897

    PubMed  Google Scholar 

  • Pashler H (1994) Dual-task interference in simple tasks: data and theory. Psychol Bull 116:220–244

    Article  PubMed  CAS  Google Scholar 

  • Plotnik M, Giladi N, Balash Y, Peretz C, Hausdorff JM (2005) Is freezing of gait in Parkinson’s disease related to asymmetric motor function? Ann Neurol 57:656–663

    Article  PubMed  Google Scholar 

  • Sadeghi H, Allard P, Prince F, Labelle H (2000) Symmetry and limb dominance in able-bodied gait: a review. Gait Posture 12:34–45

    Article  PubMed  CAS  Google Scholar 

  • Schaafsma JD, Giladi N, Balash Y, Bartels AL, Gurevich T, Hausdorff JM (2003) Gait dynamics in Parkinson’s disease: relationship to parkinsonian features, falls and response to levodopa. J Neurol Sci 212:47–53

    Article  PubMed  Google Scholar 

  • Schmidt RA, Lee TD (1999) Motor control and learning. Human Kinetics, Champaign

    Google Scholar 

  • Sheridan PL, Solomont J, Kowall N, Hausdorff JM (2003) Influence of executive function on locomotor function: divided attention increases gait variability in Alzheimer’s disease. J Am Geriatr Soc 51:1633–1637

    Article  PubMed  Google Scholar 

  • Skinner HB, Effeney DJ (1985) Gait analysis in amputees. Am J Phys Med 64:82–89

    PubMed  CAS  Google Scholar 

  • Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM (2006) Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Mov Disord 21:950–957

    Article  PubMed  Google Scholar 

  • 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 [Epub ahead of print]

  • Verghese J, Buschke H, Viola L, Katz M, Hall C, Kuslansky G, Lipton R (2002) Validity of divided attention tasks in predicting falls in older individuals: a preliminary study. J Am Geriatr Soc 50:1572–1576

    Article  PubMed  Google Scholar 

  • Wall JC, Turnbull GI (1986) Gait asymmetries in residual hemiplegia. Arch Phys Med Rehabil 67:550–553

    PubMed  CAS  Google Scholar 

  • Woollacott M, Shumway-Cook A (2002) Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16:1–14

    Article  PubMed  Google Scholar 

  • Yang JF, Lamont EV, Pang MY (2005) Split-belt treadmill stepping in infants suggests autonomous pattern generators for the left and right leg in humans. J Neurosci 25:6869–6876

    Article  PubMed  CAS  Google Scholar 

  • Yang YR, Chen YC, Lee CS, Cheng SJ, Wang RY (2006) Dual-task-related gait changes in individuals with stroke. Gait Posture [Epub ahead of print]

  • Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM (2005) Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 22:1248–1256

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the National Parkinson Foundation, the Parkinson’s Disease Foundation, and by National Institutes of Health grants AG-14100, RR-13622, HD-39838 and AG-08812. We thank Shmuel Springer, Talia Herman and Leor Gruendlinger for invaluable assistance and the participants for their time and effort.

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Correspondence to Jeffrey M. Hausdorff.

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Yogev, G., Plotnik, M., Peretz, C. et al. Gait asymmetry in patients with Parkinson’s disease and elderly fallers: when does the bilateral coordination of gait require attention?. Exp Brain Res 177, 336–346 (2007). https://doi.org/10.1007/s00221-006-0676-3

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  • DOI: https://doi.org/10.1007/s00221-006-0676-3

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