Abstract
The primary purpose of this study was to investigate the effect of dual-tasking on cognitive performance and gait parameters in patients with idiopathic Parkinson’s disease (PD) without dementia. The impact of cognitive task complexity on cognition and walking was also examined. Eighteen patients with PD (ages 53–88, 10 women; Hoehn and Yahr stage I-II) and 18 older adults (ages 61–84; 10 women) completed two neuropsychological measures of executive function/attention (the Stroop Test and Wisconsin Card Sorting Test). Cognitive performance and gait parameters related to functional mobility of stride were measured under single (cognitive task only) and dual-task (cognitive task during walking) conditions with different levels of difficulty and different types of stimuli. In addition, dual-task cognitive costs were calculated. Although cognitive performance showed no significant difference between controls and PD patients during single or dual-tasking conditions, only the patients had a decrease in cognitive performance during walking. Gait parameters of patients differed significantly from controls at single and dual-task conditions, indicating that patients gave priority to gait while cognitive performance suffered. Dual-task cognitive costs of patients increased with task complexity, reaching significantly higher values then controls in the arithmetic task, which was correlated with scores on executive function/attention (Stroop Color-Word Page). Baseline motor functioning and task executive/attentional load affect the performance of cognitive tasks of PD patients while walking. These findings provide insight into the functional strategies used by PD patients in the initial phases of the disease to manage dual-task interference.
Similar content being viewed by others
References
Muslimovic D, Post B, Speelman JD, Schmand B (2005) Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology 65:1239–1245
Foltynie T, Brayne CE, Robbins TW, Barker RA (2004) The cognitive ability of an incident cohort of Parkinson’s patients in the UK: the CamPaIGN study. Brain 127:550–560
Dubois B, Pillon B (1997) Cognitive deficits in Parkinson’s disease. J Neurol 244:2–8
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
Plotnik M, Dagan Y, Gurevich T, Giladi N, Hausdorff JM (2011) 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
Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G et al (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
Yogev-Seligmann G, Hausdrff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23(3):329–342
Marchese R, Bove M, Abbruzzese G (2003) Effect of cognitive and motor tasks on postural stability in Parkinson’s disease: a posturographic study. Mov Disord 18:652–658
Morris ME, Iansek R, Smithson F, Huxham F (2000) Postural instability in Parkinson’s disease: a comparison with and without an added task. Gait Posture 12:205–216
Hackney ME, Earhart GM (2010) The effects of a secondary task on forward and backward walking in Parkinson’s disease. Neurorehabil Neural Repair 24:88–96
Kelly VE, Eusterbrock AJ, Shumway-Cook A (2012) A review of dual-task walking deficits in people with Parkinson’s disease: motor and cognitive contributions, mechanisms, and clinical implications. Parkinsons Dis. doi:10.1155/2012/918719
Gibb WR, Lees AJ (1988) A comparison of clinical and pathological features of young and old onset Parkinson’s disease. Neurology 38:1402–1406
Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442
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
Gorestein C, Andrade L (1998) Inventário de depressão de Beck: propriedades psicométricas da versão em português. Rev Psiquiatr Clín 25:245–250
Fahn S, Elton RL, Members of the UPDRS Development Committee (1987) The Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Healthcare Information, Florham Park pp 153–163, 293–304
Kongs SK, Thompson LL, Iverson GL, Heaton RK (2000) Wisconsin Card Sorting Test-64 Card Version. Psychological Assessment Resources, Lutz
Strauss E, Sherman EMS, Spreen O (2006) A compendium of neuropsychological tests: administration, norms and commentary. Oxford University Press, New York
Bisiacchi PS, Borella E, Bergamaschi S, Carretti B, Mondini S (2008) Interplay between memory and executive functions in normal and pathological aging. J Clin Exp Neuropsychol 30:723–733
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
Rhodes MG (2004) Age-related differences in performance on the Wisconsin Card Sorting Test: a meta-analytic review. Psychol Aging 19:482–494
Glisky EL, Polster MR, Routhieaux BC (1995) Double dissociation between item and source memory. Neuropsychology 9:229–235
Paolo AM, Tröster AI, Axelrod BN, Koller WC (1995) Construct validity of the WCST in normal elderly and persons with Parkinson’s disease. Arch Clin Neuropsych 10:463–473
Laiacona M, Inzaghi MG, Tanti A, Capitani E (2000) Wisconsin card sorting test: a new global score, with Italian norms, and its relationship with the Weigl sorting test. Neurol Sci 21:279–291
MacLeod CM (1991) Half a century of research on the Stroop effect: an integrative review. Psychol Bull 109:163–203
Kelly VE, Janke AA, Shumway-Cook A (2010) Effects of instructed focus and difficulty on concurrent walking and cognitive task performance in healthy young adults. Exp Brain Res 207:65–73
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
Hollman JH, Kovash FM, Kubik JJ, Linbo RA (2007) Age-related differences in spatiotemporal markers of gait stability during dual task walking. Gait Posture 26:113–119
Cho C, Kunin M, Kudo K, Osaki Y, Olanow CW, Cohen B, Raphan T (2010) Frequency velocity mismatch: a fundamental abnormality in Parkinsonian gait. J Neurophysiol 103:1478–1489
Sabatini AM, Martelloni C, Scapellato S, Cavallo F (2005) Assessment of walking features from foot inertial sensing. IEEE Trans Biomed Eng 52(3):486–494
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
Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J Neuroeng Rehabil 2(19)
Maylor EA, Wing AM (1996) Age differences in postural stability are increased by additional cognitive demands. J Gerontol Psychol Sci 51(B):143–154
Lindenberger U, Marsiske M, Baltes PB (2000) Memorizing while walking: increase in dual-task costs from young adulthood to old age. Psychol Aging 15:417–436
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
Franzén E, Paquette C, Gurfinkel VS, Cordo PJ, Nutt JG, Horak FB (2009) Reduced performance in balance, walking and turning tasks is associated with increased neck tone in Parkinson’s disease. Exp Neurol 219:430–438
Morris M, 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 20:40–50
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
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
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
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
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
Spildooren J, Vercruysse S, Desloovere K, Vandenberghe W, Kerckhofs E, Nieuwboer A (2010) Freezing of gait in Parkinson’s disease: the impact of dual tasking and turning. Mov Disord 25:2563–2570
Tombu M, Jolicoaeur P (2003) A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform 29:3–18
Ruthruff E, Pashler HE, Klaassen A (2001) Processing bottlenecks in dual-task performance: structural limitation or strategic postponement? Psychon Bull Rev 8:73–80
Bloem BR, Grimbergen YA, Van Dijk JG, Munneke M (2006) The “posture second” strategy: a review of wrong priorities in Parkinson’s disease. J Neurol Sci 248:196–204
Beauchet O, Dubost V, Gonthier R, Kressig RW (2005) Dual-task-related gait changes in transitionally frail older adults: the type of the walking-associated cognitive task matters. Gerontology 51:48–52
Galletly R, Brauer SG (2005) Does the type of concurrent task affect preferred and cued gait in people with Parkinson’s disease? Aust J Physiother 51:175–180
Litvan I, Goldman JG, Tröster AI et al (2012) Diagnostic criteria for mild cognitive impairment in Parkinson’s disease: movement disorder society task force guidelines. Mov Disord 27:349–356
Poletti M, Frosini D, Pagni C et al (2012) Mild cognitive impairment and cognitive-motor relationships in newly diagnosed drug-naive patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 83(6):601–606
Gleason CE, Gangnon RE, Fischer BL, Mahoney JE (2009) Increased risk for falling associated with subtle cognitive impairment: secondary analysis of a randomized clinical trial. Dement Geriatr Cogn Disord 27:557–563
Klepac N, Trkulja V, Relja M, Babić T (2008) Is quality of life in non-demented Parkinson’s disease patients related to cognitive performance? A clinic-based cross-sectional study. Eur J Neurol 15:128–133
Canning CG, Ada L, Woodhouse E (2008) Multiple-task walking training in people with mild to moderate Parkinson’s disease: a pilot study. Clin Rehabil 22:226–233
Yogev-Seligmann G, Giladi N, Brozgol M, Hausdorff JM (2012) A training program to improve gait while dual tasking in patients with Parkinson’s disease: a pilot study. Arch Phys Med Rehabil 93(1):176–181
Brauer SG, Morris ME (2010) Can people with Parkinson’s disease improve dual tasking when walking? Gait Posture 31:229–233
Brauer SG, Woollacott MH, Lamont R, Clewett S, O’Sullivan J, Silburn P, Mellick GD, Morris ME (2011) Single and dual task gait training in people with Parkinson’s disease: a protocol for a randomised controlled trial. BMC Neurol 11(90)
Acknowledgments
This research was supported by the National Institute for Translational Medicine (INCT-TM). I. I. Argimon is a National Council for Scientific and Technological Development (CNPq) research fellow. D. B. Lima is a CAPES Ministry of Education and Culture fellowship and H. B. Oliveira is a FAPERGS fellowship.
Conflicts of interest
The authors also declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Lucia Bartmann Wild and Daiane Borba de Lima contributed equally for the study.
Rights and permissions
About this article
Cite this article
Wild, L.B., de Lima, D.B., Balardin, J.B. et al. Characterization of cognitive and motor performance during dual-tasking in healthy older adults and patients with Parkinson’s disease. J Neurol 260, 580–589 (2013). https://doi.org/10.1007/s00415-012-6683-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00415-012-6683-3