Experimental Brain Research

, Volume 208, Issue 2, pp 169–179 | Cite as

Effects of cognitive function on gait and dual tasking abilities in patients with Parkinson’s disease suffering from motor response fluctuations

  • Meir Plotnik
  • Yaacov Dagan
  • Tanya Gurevich
  • Nir Giladi
  • Jeffrey M. Hausdorff
Research Article


Recent studies have demonstrated that cognitive loading aggravates the gait impairments that are typically seen in Parkinson’s disease (PD). To better understand the relationship between cognition and gait in PD, we evaluated 30 subjects with PD who suffer from motor response fluctuations. The subjects were clinically and cognitively assessed using standard clinical (e.g., Unified Parkinson’s Disease Rating Scale) and cognitive tests while in the “ON” period of the medication cycle. In addition, the subjects wore force-sensitive insoles to quantify the timing of the gait cycles during 80-m walks at a self-selected, comfortable pace during three randomly presented gait conditions: (1) usual-walking, (2) dual tasking (DT), performing serial 3 subtractions (DT_S3), and (3) DT_S7. Stride length, gait speed, gait variability and bilateral coordination of gait were affected by DT, compared to the usual-walking (P < 0.001) as was gait asymmetry (P = 0.024). Stepwise regression analyses showed that a subset of the cognitive performance scores accounted for the changes seen in the gait parameters during DT, e.g., set shifting capabilities as expressed by the Trial Making Test Scores (P < 0.001). Affect (e.g., anxiety) was not associated with DT-related gait changes. For most gait features, DT had a large impact on the DT_S3 condition with only minimal additional effect in the DT_S7 condition. These results demonstrate that the complex cognitive–motor interplay in the control of gait in patients with PD who suffer from motor response fluctuations has a profound and marked effect during DT conditions on gait variability, asymmetry and bilateral coordination, even in the “ON” state when patients are likely to be most active, mobile and vulnerable to the negative effects of dual tasking.


Parkinson’s disease Gait Cognition Attention Gait variability Bilateral coordination 



We thank the patients and staff of the Movement Disorders Unit at the Tel-Aviv Sourasky Medical Center for invaluable assistance. We thank Ms. Jennifer Srygley and Mr. Leor Grundlinger for their help with data handling. This study was supported in part by the Parkinson’s disease Foundation (PDF), the National Parkinson’s Foundation (NPF) and by the Israeli Ministries of Health and Veteran Affairs (Grant #3000004385).


  1. Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ (2009) Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 15:110–115CrossRefPubMedGoogle Scholar
  2. Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958CrossRefPubMedGoogle Scholar
  3. Brauer SG, Woollacott M, Shumway-Cook A (2002) The influence of a concurrent cognitive task on the compensatory stepping response to a perturbation in balance-impaired and healthy elders. Gait Posture 15:83–93CrossRefPubMedGoogle Scholar
  4. Colosimo C, De Michele M (1999) Motor fluctuations in Parkinson’s disease: pathophysiology and treatment. Eur J Neurol 6:1–21CrossRefPubMedGoogle Scholar
  5. D’Elia LF, Satz P, Uchiyama CL, White T (1996) Color trails test. Psychological Assessment Resources, FloridaGoogle Scholar
  6. Doniger GM, Zucker DM, Schweiger A, Dwolatzky T, Chertkow H, Crystal H, Simon ES (2005) Towards practical cognitive assessment for detection of early dementia: a 30-minute computerized battery discriminates as well as longer testing. Curr Alzheimer Res 2:117–124CrossRefPubMedGoogle Scholar
  7. Doniger GM, Dwolatzky T, Zucker DM, Chertkow H, Crystal H, Schweiger A, Simon ES (2006) Computerized cognitive testing battery identifies mild cognitive impairment and mild dementia even in the presence of depressive symptoms. Am J Alzheimers Dis Other Demen 21:28–36CrossRefPubMedGoogle Scholar
  8. Dubois B, Pillon B (1997) Cognitive deficits in Parkinson’s disease. J Neurol 244:2–8CrossRefPubMedGoogle Scholar
  9. 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 3:4CrossRefPubMedGoogle Scholar
  10. Dwolatzky T, Whitehead V, Doniger GM, Simon ES, Schweiger A, Jaffe D, Chertkow H (2004) Validity of the Mindstreams computerized cognitive battery for mild cognitive impairment. J Mol Neurosci 24:33–44CrossRefPubMedGoogle Scholar
  11. Fahn S, Elton R, Members of the UPDRS Developmental Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, MCCDGM (eds) Recent developments in Parkinson’s disease. NJ, Florham Park, pp 153–163Google Scholar
  12. 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
  13. Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39CrossRefPubMedGoogle Scholar
  14. Hackney ME, Earhart GM (2009) The effects of a secondary task on forward and backward walking in Parkinson’s disease. Neurorehabil Neural Repair (in press)Google Scholar
  15. Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113CrossRefPubMedGoogle Scholar
  16. 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 13:428–437CrossRefPubMedGoogle Scholar
  17. Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson’s disease subjects with freezing of gait. Exp Brain Res 149:187–194PubMedGoogle Scholar
  18. Hausdorff JM, Peng CK, Goldberger AL, Stoll AL (2004) Gait unsteadiness and fall risk in two affective disorders: a preliminary study. BMC Psychiatry 4:39CrossRefPubMedGoogle Scholar
  19. Hausdorff JM, Schweiger A, Herman T, Yogev-Seligmann G, Giladi N (2008) Dual-task decrements in gait: contributing factors among healthy older adults. J Gerontol A Biol Sci Med Sci 63:1335–1343PubMedGoogle Scholar
  20. Hedden T, Gabrieli JD (2010) Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Neuroimage 51:421–431CrossRefPubMedGoogle Scholar
  21. Hely MA, Morris JG, Reid WG, Trafficante R (2005) Sydney Multicenter Study of Parkinson’s disease: non-L-dopa-responsive problems dominate at 15 years. Mov Disord 20:190–199CrossRefPubMedGoogle Scholar
  22. Herman T, Mirelman A, Giladi N, Schweiger A, Hausdorff JM (2010) Executive control deficits as a prodrome to falls in healthy older adults: a prospective study linking thinking, walking, and falling. J Gerontol A Biol Sci Med Sci 65:1086–1092PubMedGoogle Scholar
  23. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMedGoogle Scholar
  24. Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75:116–124CrossRefPubMedGoogle Scholar
  25. Latt MD, Menz HB, Fung VS, Lord SR (2009) Acceleration patterns of the head and pelvis during gait in older people with Parkinson’s disease: a comparison of fallers and nonfallers. J Gerontol A Biol Sci Med Sci 64:700–706PubMedGoogle Scholar
  26. Lemke MR, Wendorff T, Mieth B, Buhl K, Linnemann M (2000) Spatiotemporal gait patterns during over ground locomotion in major depression compared with healthy controls. J Psychiatr Res 34:277–283CrossRefPubMedGoogle Scholar
  27. Lord S, Rochester L, Hetherington V, Allcock LM, Burn D (2010) Executive dysfunction and attention contribute to gait interference in ‘off’ state Parkinson’s disease. Gait Posture 31:169–174CrossRefPubMedGoogle Scholar
  28. Morris ME, Iansek R, Matyas TA, Summers JJ (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117(Pt 5):1169–1181CrossRefPubMedGoogle Scholar
  29. Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119(2):551–568CrossRefPubMedGoogle Scholar
  30. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53–83CrossRefPubMedGoogle Scholar
  31. Paleacu D, Shutzman A, Giladi N, Herman T, Simon ES, Hausdorff JM (2007) Effects of pharmacological therapy on gait and cognitive function in depressed patients. Clin Neuropharmacol 30:63–71CrossRefPubMedGoogle Scholar
  32. Plotnik M, Hausdorff JM (2008) The role of gait rhythmicity and bilateral coordination of stepping in the pathophysiology of freezing of gait in Parkinson’s disease. Mov Disord 23(Suppl):S444–S450CrossRefPubMedGoogle Scholar
  33. 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 57:656–663CrossRefPubMedGoogle Scholar
  34. Plotnik M, Giladi N, Hausdorff JM (2007) A new measure for quantifying the bilateral coordination of human gait: effects of aging and Parkinson’s disease. Exp Brain Res 181:561–570CrossRefPubMedGoogle Scholar
  35. Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006CrossRefPubMedGoogle Scholar
  36. Plotnik M, Giladi N, Hausdorff JM (2009) Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking. J Neurol Neurosurg Psychiatry 80:347–350CrossRefPubMedGoogle Scholar
  37. Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148PubMedGoogle Scholar
  38. Riley DE, Lang AE (1993) The spectrum of levodopa-related fluctuations in Parkinson’s disease. Neurology 43:1459–1464PubMedGoogle Scholar
  39. Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G, Van Wegen E (2004) Attending to the task: interference effects of functional tasks on walking in Parkinson’s disease and the roles of cognition, depression, fatigue, and balance. Arch Phys Med Rehabil 85:1578–1585CrossRefPubMedGoogle Scholar
  40. Rochester L, Nieuwboer A, Baker K, Hetherington V, Willems AM, Chavret F, Kwakkel G, Van Wegen E, Lim I, Jones D (2007) The attentional cost of external rhythmical cues and their impact on gait in Parkinson’s disease: effect of cue modality and task complexity. J Neural Transm 114:1243–1248CrossRefPubMedGoogle Scholar
  41. Rochester L, Nieuwboer A, Baker K, Hetherington V, Willems AM, Kwakkel G, Van Wegen E, Lim I, Jones D (2008) Walking speed during single and dual tasks in Parkinson’s disease: which characteristics are important? Mov Disord 23:2312–2318CrossRefPubMedGoogle Scholar
  42. Spielberger CD, Gorsuch R, Lushene R, Vagg P, Jacobs G (1983) Self-evaluation questionnaire (form Y). Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Palo AltoGoogle Scholar
  43. Srygley JM, Mirelman A, Herman T, Giladi N, Hausdorff JM (2009) When does walking alter thinking? Age and task associated findings. Brain Res 1253:92–99CrossRefPubMedGoogle Scholar
  44. Verghese J, Robbins M, Holtzer R, Zimmerman M, Wang C, Xue X, Lipton RB (2008) Gait dysfunction in mild cognitive impairment syndromes. J Am Geriatr Soc 56:1244–1251CrossRefPubMedGoogle Scholar
  45. Verghese J, Holtzer R, Lipton RB, Wang C (2009) Quantitative gait markers and incident fall risk in older adults. J Gerontol A Biol Sci Med Sci 64:896–901PubMedGoogle Scholar
  46. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17:37–49CrossRefPubMedGoogle Scholar
  47. 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 22:1248–1256CrossRefPubMedGoogle Scholar
  48. Yogev G, Plotnik M, Peretz C, Giladi N, Hausdorff JM (2007) Gait asymmetry in patients with Parkinson’s disease and elderly fallers: when does the bilateral coordination of gait require attention? Exp Brain Res 177:336–346CrossRefPubMedGoogle Scholar
  49. Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Meir Plotnik
    • 1
    • 2
    • 3
  • Yaacov Dagan
    • 1
    • 4
  • Tanya Gurevich
    • 1
    • 5
  • Nir Giladi
    • 1
    • 5
  • Jeffrey M. Hausdorff
    • 1
    • 6
    • 7
  1. 1.Movement Disorders Unit, Department of Neurology, Laboratory for Gait and NeurodynamcisTel-Aviv Sourasky Medical CenterTel-AvivIsrael
  2. 2.Department of Physiology and Pharmacology, Sackler Faculty of MedicineTel-Aviv UniversityTel AvivIsrael
  3. 3.The Gonda Brain Research CenterBar Ilan UniversityRamat GanIsrael
  4. 4.Department of RehabilitationSheba Medical CenterRamat GanIsrael
  5. 5.Department of Neurology, Sackler Faculty of MedicineTel-Aviv UniversityTel AvivIsrael
  6. 6.Department of Physical Therapy, Sackler Faculty of MedicineTel-Aviv UniversityTel AvivIsrael
  7. 7.Department of MedicineHarvard Medical SchoolBostonUSA

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