Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ (2009) Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 15:110–115

    CAS  Article  PubMed  Google Scholar 

  • Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958

    CAS  Article  PubMed  Google Scholar 

  • 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 15:83–93

    CAS  Article  PubMed  Google Scholar 

  • Colosimo C, De Michele M (1999) Motor fluctuations in Parkinson’s disease: pathophysiology and treatment. Eur J Neurol 6:1–21

    CAS  Article  PubMed  Google Scholar 

  • D’Elia LF, Satz P, Uchiyama CL, White T (1996) Color trails test. Psychological Assessment Resources, Florida

    Google Scholar 

  • 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 2:117–124

    CAS  Article  PubMed  Google Scholar 

  • 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 21:28–36

    Article  PubMed  Google Scholar 

  • Dubois B, Pillon B (1997) Cognitive deficits in Parkinson’s disease. J Neurol 244:2–8

    CAS  Article  PubMed  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

    Article  PubMed  Google Scholar 

  • 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 24:33–44

    CAS  Article  PubMed  Google Scholar 

  • 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 153–163

    Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • 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)

  • Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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 149:187–194

    CAS  PubMed  Google Scholar 

  • Hausdorff JM, Peng CK, Goldberger AL, Stoll AL (2004) Gait unsteadiness and fall risk in two affective disorders: a preliminary study. BMC Psychiatry 4:39

    Article  PubMed  Google Scholar 

  • 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 63:1335–1343

    PubMed  Google Scholar 

  • Hedden T, Gabrieli JD (2010) Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Neuroimage 51:421–431

    Article  PubMed  Google Scholar 

  • 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 20:190–199

    Article  PubMed  Google Scholar 

  • 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 65:1086–1092

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75:116–124

    CAS  Article  PubMed  Google Scholar 

  • 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 64:700–706

    PubMed  Google Scholar 

  • 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 34:277–283

    CAS  Article  PubMed  Google Scholar 

  • 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 31:169–174

    Article  PubMed  Google Scholar 

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

    Article  PubMed  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(2):551–568

    Article  PubMed  Google Scholar 

  • Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53–83

    CAS  Article  PubMed  Google Scholar 

  • 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 30:63–71

    CAS  Article  PubMed  Google Scholar 

  • 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–S450

    Article  PubMed  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 

  • 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 181:561–570

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006

    Article  PubMed  Google Scholar 

  • Plotnik M, Giladi N, Hausdorff JM (2009) Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking. J Neurol Neurosurg Psychiatry 80:347–350

    CAS  Article  PubMed  Google Scholar 

  • Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148

    CAS  PubMed  Google Scholar 

  • Riley DE, Lang AE (1993) The spectrum of levodopa-related fluctuations in Parkinson’s disease. Neurology 43:1459–1464

    CAS  PubMed  Google Scholar 

  • 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 85:1578–1585

    Article  PubMed  Google Scholar 

  • 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 114:1243–1248

    CAS  Article  PubMed  Google Scholar 

  • 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 23:2312–2318

    Article  PubMed  Google Scholar 

  • 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 Alto

  • Srygley JM, Mirelman A, Herman T, Giladi N, Hausdorff JM (2009) When does walking alter thinking? Age and task associated findings. Brain Res 1253:92–99

    CAS  Article  PubMed  Google Scholar 

  • 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 56:1244–1251

    Article  PubMed  Google Scholar 

  • 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 64:896–901

    PubMed  Google Scholar 

  • 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 17:37–49

    Article  PubMed  Google Scholar 

  • 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 

  • 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 177:336–346

    Article  PubMed  Google Scholar 

  • Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Meir Plotnik.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Plotnik, M., Dagan, Y., Gurevich, T. et al. Effects of cognitive function on gait and dual tasking abilities in patients with Parkinson’s disease suffering from motor response fluctuations. Exp Brain Res 208, 169–179 (2011). https://doi.org/10.1007/s00221-010-2469-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-010-2469-y

Keywords

  • Parkinson’s disease
  • Gait
  • Cognition
  • Attention
  • Gait variability
  • Bilateral coordination