The nature of dual-task interference during gait in incident Parkinson’s disease

Dual-task interference during gait is a common phenomenon in older adults and people with Parkinson's disease (PD). Dual-task performance is driven by cognitive processes involving executive function, attention and working memory which underpin resource capacity and allocation. The underlying processes that contribute to dual-task interference are poorly understood, and confounded by methodological differences. The aim of this study was to explore the nature of dual-task interference in PD with respect to age-matched controls. We examined 121 people with early PD and 189 controls and controlled for baseline task demand on both tasks allowing between-group differences to be attributed to dual-task interference rather than differences in baseline performance. We also compared a wide range of gait characteristics to evaluate the pattern of interference. Participants walked for two minutes at a preferred pace under single- and dual-task (test of working memory capacity-digit span recall) conditions. In a subgroup task demand was increased (digit span+1) (n=55 control, n=44 PD) to assess the influence of resource capacity. Finally the association between dual-task interference with motor and cognitive characteristics was examined to evaluate resource capacity and allocation. PD and controls responded similarly to the dual-task for all gait characteristics except for step width and step width variability and this was the same when task demand increased (dual+1). Control participants took wider steps (p=0.006) and step width variability increased significantly for controls (p=0.001) but not PD. Interference was specific to the gait characteristic rather than a global pattern of impairment. Digit span error rates were not significantly different between groups during dual-task performance. There were no significant correlations with dual-task interference and global cognition, motor deficit, and executive function for either group. Effects of dual-tasks on gait performance are twofold and specific to the gait characteristic. They reflect an age-related reduction in gait performance (especially forward progression) in PD and controls possibly due to reduced resource capacity; and secondly, show postural stability during walking in early PD is disproportionately affected highlighting a PD-specific dual-task co-ordination deficit. Further work is required to identify the cognitive, executive and motor correlates of dual-task interference from which inferences about underlying cognitive processes can be made. These findings inform an understanding of dual-task impairment in early PD and suggest that management should target postural control under dual-task conditions from the early stages.

[1]  Bastiaan R. Bloem,et al.  Assessment of dual tasking has no clinical value for fall prediction in Parkinson’s disease , 2012, Journal of Neurology.

[2]  S. Studenski,et al.  Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed , 2005, Journal of NeuroEngineering and Rehabilitation.

[3]  G. Kwakkel,et al.  Walking speed during single and dual tasks in Parkinson's disease: Which characteristics are important? , 2008, Movement disorders : official journal of the Movement Disorder Society.

[4]  Thomas Foltynie,et al.  The distinct cognitive syndromes of Parkinson's disease: 5 year follow-up of the CamPaIGN cohort. , 2009, Brain : a journal of neurology.

[5]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[6]  T. Brandt,et al.  Differential effects of absent visual feedback control on gait variability during different locomotion speeds , 2012, Experimental Brain Research.

[7]  J. Evans,et al.  Walking and talking: an investigation of cognitive—motor dual tasking in multiple sclerosis , 2009, Multiple sclerosis.

[8]  B. Bloem,et al.  The “posture second” strategy: A review of wrong priorities in Parkinson's disease , 2006, Journal of the Neurological Sciences.

[9]  W. Zijlstra,et al.  Do Dual Tasks Have an Added Value Over Single Tasks for Balance Assessment in Fall Prevention Programs? A Mini-Review , 2008, Gerontology.

[10]  S. Swinnen,et al.  Neural Basis of Aging: The Penetration of Cognition into Action Control , 2005, The Journal of Neuroscience.

[11]  Thomas Brandt,et al.  Aging of human supraspinal locomotor and postural control in fMRI , 2012, Neurobiology of Aging.

[12]  C. Clarke,et al.  Systematic review of levodopa dose equivalency reporting in Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[13]  S. Studenski,et al.  Stance time and step width variability have unique contributing impairments in older persons. , 2008, Gait & posture.

[14]  U. Nayak,et al.  The effect of age on variability in gait. , 1984, Journal of gerontology.

[15]  Jeffrey M. Hausdorff,et al.  The role of executive function and attention in gait , 2008, Movement disorders : official journal of the Movement Disorder Society.

[16]  B. Bloem,et al.  Postural control in Parkinson patients: A proprioceptive problem? , 2011, Experimental Neurology.

[17]  K. Wesnes Assessing cognitive function in clinical trials: latest developments and future directions. , 2002, Drug discovery today.

[18]  O. Bock,et al.  Age-Related Deficits of Dual-Task Walking: A Review , 2012, Neural plasticity.

[19]  Jeffrey M. Hausdorff,et al.  Effects of Cognitive Challenge on Gait Variability in Patients with Parkinson’s Disease , 2003, Journal of geriatric psychiatry and neurology.

[20]  M. Hallett,et al.  Neural correlates of dual task performance in patients with Parkinson’s disease , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[21]  P. Rabbitt,et al.  Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. , 1994, Dementia.

[22]  William W. McDonald,et al.  Depression rating scales in Parkinson's disease: Critique and recommendations , 2007, Movement disorders : official journal of the Movement Disorder Society.

[23]  M. Plotnik,et al.  Bilateral coordination of gait and Parkinson’s disease: the effects of dual tasking , 2009, Journal of Neurology, Neurosurgery, and Psychiatry.

[24]  R. Barker,et al.  The spectrum of nonmotor symptoms in early Parkinson disease , 2013, Neurology.

[25]  C. Annweiler,et al.  Stops walking when talking: a predictor of falls in older adults? , 2009, European journal of neurology.

[26]  S. Sala,et al.  Dual Task Performance in Parkinson’s Disease , 2013, Behavioural neurology.

[27]  R H Logie,et al.  Dual task effects of walking when talking in Alzheimer's disease. , 2004, Revue neurologique.

[28]  L. E. Powell,et al.  The Activities-specific Balance Confidence (ABC) Scale. , 1995, The journals of gerontology. Series A, Biological sciences and medical sciences.

[29]  Jeannette R. Mahoney,et al.  fNIRS study of walking and walking while talking in young and old individuals. , 2011, The journals of gerontology. Series A, Biological sciences and medical sciences.

[30]  Martina Mancini,et al.  Framework for understanding balance dysfunction in Parkinson's disease , 2013, Movement disorders : official journal of the Movement Disorder Society.

[31]  Jeffrey M. Hausdorff,et al.  Dual tasking, gait rhythmicity, and Parkinson's disease: Which aspects of gait are attention demanding? , 2005, The European journal of neuroscience.

[32]  F. Horak,et al.  Milestones in gait, balance, and falling , 2011, Movement disorders : official journal of the Movement Disorder Society.

[33]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[34]  A. Kuo,et al.  Active control of lateral balance in human walking. , 2000, Journal of biomechanics.

[35]  M. McDaniel,et al.  The relationship between working memory capacity and executive functioning: evidence for a common executive attention construct. , 2010, Neuropsychology.

[36]  Lynn Rochester,et al.  Moving forward on gait measurement: Toward a more refined approach , 2013, Movement disorders : official journal of the Movement Disorder Society.

[37]  Jeffrey M. Hausdorff Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. , 2007, Human movement science.

[38]  Alan D Baddeley,et al.  Is there a specific executive capacity for dual task coordination? Evidence from Alzheimer's disease. , 2004, Neuropsychology.

[39]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[40]  Mark Latt,et al.  Reliability of the GAITRite walkway system for the quantification of temporo-spatial parameters of gait in young and older people. , 2004, Gait & posture.

[41]  Jeffrey M. Hausdorff,et al.  The contribution of postural control and bilateral coordination to the impact of dual tasking on gait , 2013, Experimental Brain Research.

[42]  Lynn Rochester,et al.  Is gait variability reliable in older adults and Parkinson's disease? Towards an optimal testing protocol. , 2013, Gait & posture.

[43]  R. W. Watson,et al.  A central executive deficit in patients with Parkinson's disease. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[44]  D. Burn,et al.  Executive dysfunction and attention contribute to gait interference in 'off' state Parkinson's Disease. , 2010, Gait & posture.

[45]  G. Kwakkel,et al.  Attending to the task: interference effects of functional tasks on walking in Parkinson's disease and the roles of cognition, depression, fatigue, and balance. , 2004, Archives of physical medicine and rehabilitation.

[46]  Lynn Rochester,et al.  Independent domains of gait in older adults and associated motor and nonmotor attributes: validation of a factor analysis approach. , 2013, The journals of gerontology. Series A, Biological sciences and medical sciences.

[47]  C. Zampieri,et al.  Dual task performance in Parkinson's disease: a sensitive predictor of impairment and disability. , 2013, Parkinsonism & related disorders.

[48]  Differences in dual-task performance and prefrontal cortex activation between younger and older adults , 2013, BMC Neuroscience.

[49]  Lynn Rochester,et al.  Gait variability in Parkinson’s disease: an indicator of non-dopaminergic contributors to gait dysfunction? , 2011, Journal of Neurology.

[50]  T. Shallice,et al.  The cognitive and neuroanatomical correlates of multitasking , 2000, Neuropsychologia.

[51]  J. Jankovic,et al.  Movement Disorder Society‐sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS‐UPDRS): Scale presentation and clinimetric testing results , 2008, Movement disorders : official journal of the Movement Disorder Society.

[52]  G. Kwakkel,et al.  Everyday walking with Parkinson's disease: Understanding personal challenges and strategies , 2008, Disability and rehabilitation.

[53]  W. Gibb,et al.  The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[54]  Nir Giladi,et al.  Do we always prioritize balance when walking? Towards an integrated model of task prioritization , 2012, Movement disorders : official journal of the Movement Disorder Society.

[55]  Jeffrey M. Hausdorff,et al.  Cognitive contributions to gait and falls: Evidence and implications , 2013, Movement disorders : official journal of the Movement Disorder Society.

[56]  A. Shumway-cook,et al.  A Review of Dual-Task Walking Deficits in People with Parkinson's Disease: Motor and Cognitive Contributions, Mechanisms, and Clinical Implications , 2011, Parkinson's disease.

[57]  Stephan P. Swinnen,et al.  Age-related differences in attentional cost associated with postural dual tasks: Increased recruitment of generic cognitive resources in older adults , 2013, Neuroscience & Biobehavioral Reviews.

[58]  Roee Holtzer,et al.  The relationship between attention and gait in aging: facts and fallacies. , 2012, Motor control.

[59]  L. Chiari,et al.  Anticipatory postural adjustments prior to step initiation are hypometric in untreated Parkinson’s disease: an accelerometer‐based approach , 2009, European journal of neurology.