Skip to main content
Top
Published in: Experimental Brain Research 2/2011

01-01-2011 | Research Article

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

Authors: Meir Plotnik, Yaacov Dagan, Tanya Gurevich, Nir Giladi, Jeffrey M. Hausdorff

Published in: Experimental Brain Research | Issue 2/2011

Login to get access

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.
Literature
go back to reference Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ (2009) Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 15:110–115CrossRefPubMed Allcock LM, Rowan EN, Steen IN, Wesnes K, Kenny RA, Burn DJ (2009) Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat Disord 15:110–115CrossRefPubMed
go back to reference Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958CrossRefPubMed Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958CrossRefPubMed
go back to reference 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 15:83–93CrossRefPubMed 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 15:83–93CrossRefPubMed
go back to reference Colosimo C, De Michele M (1999) Motor fluctuations in Parkinson’s disease: pathophysiology and treatment. Eur J Neurol 6:1–21CrossRefPubMed Colosimo C, De Michele M (1999) Motor fluctuations in Parkinson’s disease: pathophysiology and treatment. Eur J Neurol 6:1–21CrossRefPubMed
go back to reference D’Elia LF, Satz P, Uchiyama CL, White T (1996) Color trails test. Psychological Assessment Resources, Florida D’Elia LF, Satz P, Uchiyama CL, White T (1996) Color trails test. Psychological Assessment Resources, Florida
go back to reference 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 2:117–124CrossRefPubMed 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 2:117–124CrossRefPubMed
go back to reference 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 21:28–36CrossRefPubMed 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 21:28–36CrossRefPubMed
go back to reference 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 3:4CrossRefPubMed 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 3:4CrossRefPubMed
go back to reference 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 24:33–44CrossRefPubMed 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 24:33–44CrossRefPubMed
go back to reference 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 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
go back to reference 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 12:189–198CrossRefPubMed 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 12:189–198CrossRefPubMed
go back to reference Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39CrossRefPubMed Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39CrossRefPubMed
go back to reference 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) 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)
go back to reference Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113CrossRefPubMed Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113CrossRefPubMed
go back to reference 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 13:428–437CrossRefPubMed 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 13:428–437CrossRefPubMed
go back to reference 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 149:187–194PubMed 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 149:187–194PubMed
go back to reference Hausdorff JM, Peng CK, Goldberger AL, Stoll AL (2004) Gait unsteadiness and fall risk in two affective disorders: a preliminary study. BMC Psychiatry 4:39CrossRefPubMed Hausdorff JM, Peng CK, Goldberger AL, Stoll AL (2004) Gait unsteadiness and fall risk in two affective disorders: a preliminary study. BMC Psychiatry 4:39CrossRefPubMed
go back to reference 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 63:1335–1343PubMed 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 63:1335–1343PubMed
go back to reference Hedden T, Gabrieli JD (2010) Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Neuroimage 51:421–431CrossRefPubMed Hedden T, Gabrieli JD (2010) Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Neuroimage 51:421–431CrossRefPubMed
go back to reference 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 20:190–199CrossRefPubMed 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 20:190–199CrossRefPubMed
go back to reference 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 65:1086–1092PubMed 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 65:1086–1092PubMed
go back to reference Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMed Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442PubMed
go back to reference Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75:116–124CrossRefPubMed Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn PA (2010) Predictors of future falls in Parkinson disease. Neurology 75:116–124CrossRefPubMed
go back to reference 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 64:700–706PubMed 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 64:700–706PubMed
go back to reference 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 34:277–283CrossRefPubMed 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 34:277–283CrossRefPubMed
go back to reference 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 31:169–174CrossRefPubMed 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 31:169–174CrossRefPubMed
go back to reference Morris ME, Iansek R, Matyas TA, Summers JJ (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117(Pt 5):1169–1181CrossRefPubMed Morris ME, Iansek R, Matyas TA, Summers JJ (1994) The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117(Pt 5):1169–1181CrossRefPubMed
go back to reference Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119(2):551–568CrossRefPubMed Morris ME, Iansek R, Matyas TA, Summers JJ (1996) Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 119(2):551–568CrossRefPubMed
go back to reference Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53–83CrossRefPubMed Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53–83CrossRefPubMed
go back to reference 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 30:63–71CrossRefPubMed 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 30:63–71CrossRefPubMed
go back to reference 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–S450CrossRefPubMed 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–S450CrossRefPubMed
go back to reference 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 57:656–663CrossRefPubMed 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 57:656–663CrossRefPubMed
go back to reference 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 181:561–570CrossRefPubMed 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 181:561–570CrossRefPubMed
go back to reference Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006CrossRefPubMed Plotnik M, Giladi N, Hausdorff JM (2008) Bilateral coordination of walking and freezing of gait in Parkinson’s disease. Eur J Neurosci 27:1999–2006CrossRefPubMed
go back to reference Plotnik M, Giladi N, Hausdorff JM (2009) Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking. J Neurol Neurosurg Psychiatry 80:347–350CrossRefPubMed Plotnik M, Giladi N, Hausdorff JM (2009) Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking. J Neurol Neurosurg Psychiatry 80:347–350CrossRefPubMed
go back to reference Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148PubMed Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148PubMed
go back to reference Riley DE, Lang AE (1993) The spectrum of levodopa-related fluctuations in Parkinson’s disease. Neurology 43:1459–1464PubMed Riley DE, Lang AE (1993) The spectrum of levodopa-related fluctuations in Parkinson’s disease. Neurology 43:1459–1464PubMed
go back to reference 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 85:1578–1585CrossRefPubMed 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 85:1578–1585CrossRefPubMed
go back to reference 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 114:1243–1248CrossRefPubMed 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 114:1243–1248CrossRefPubMed
go back to reference 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 23:2312–2318CrossRefPubMed 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 23:2312–2318CrossRefPubMed
go back to reference 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 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
go back to reference Srygley JM, Mirelman A, Herman T, Giladi N, Hausdorff JM (2009) When does walking alter thinking? Age and task associated findings. Brain Res 1253:92–99CrossRefPubMed Srygley JM, Mirelman A, Herman T, Giladi N, Hausdorff JM (2009) When does walking alter thinking? Age and task associated findings. Brain Res 1253:92–99CrossRefPubMed
go back to reference 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 56:1244–1251CrossRefPubMed 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 56:1244–1251CrossRefPubMed
go back to reference 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 64:896–901PubMed 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 64:896–901PubMed
go back to reference 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 17:37–49CrossRefPubMed 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 17:37–49CrossRefPubMed
go back to reference 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 22:1248–1256CrossRefPubMed 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 22:1248–1256CrossRefPubMed
go back to reference 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 177:336–346CrossRefPubMed 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 177:336–346CrossRefPubMed
go back to reference Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342CrossRefPubMed Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342CrossRefPubMed
Metadata
Title
Effects of cognitive function on gait and dual tasking abilities in patients with Parkinson’s disease suffering from motor response fluctuations
Authors
Meir Plotnik
Yaacov Dagan
Tanya Gurevich
Nir Giladi
Jeffrey M. Hausdorff
Publication date
01-01-2011
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 2/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-010-2469-y

Other articles of this Issue 2/2011

Experimental Brain Research 2/2011 Go to the issue