Gait and cognition in Parkinson’s disease: implications for rehabilitation

Robert Iansek; Mary Danoudis; Nicholas Bradfield

doi:10.1515/revneuro-2013-0006

Article

Gait and cognition in Parkinson’s disease: implications for rehabilitation

Robert Iansek
Robert Iansek is Professor of Geriatric Neurology at Monash University in Melbourne, and Director of the Victorian Comprehensive Parkinson Program (VCPP) as well as Director of Clinical Research Centre for Movement Disorders & Gait at the Kingston Centre, Southern Health in Melbourne. He is a Neurologist by training and has over 25 years neurophysiological research experience, having published over 150 articles, books, and videos. His main research interests’ concern basal ganglia function and malfunctions in Parkinson’s disease, cortical gait control mechanisms and rehabilitation in Parkinson’s disease. Professor Iansek was instrumental in the development and use of multi disciplinary rehabilitation for people with Parkinson’s disease and its implementation in both the public and private health systems in Australia.
, Mary Danoudis
Mary Danoudis is a research physiotherapist and clinician working with people with Parkinson’s disease at the Clinical Research Centre for Movement Disorders and Gait, Kingston Centre, Monash Health. Her research expertise is in rehabilitation for Parkinson’s disease and understanding changes in the brain responsible for walking disorders. She has a Research Masters in Physiotherapy.
and Nicholas Bradfield
Dr Nicholas Bradfield is a clinical neuropsychologist and lecturer in behavioural neuroscience. He completed his doctoral thesis examining the effects of repetitive Transcranial Magnetic Stimulation on the dorsolateral prefrontal cortex using functional Magnetic Resonance Imaging. He currently works in movement disorders, aged psychiatry, trauma, consultation liaison and neurosurgery. His special interests include dementia, Parkinson’s disease, frontotemporal dementia and the anatomy of the prefrontal cortex and the hippocampus.

Published/Copyright: May 6, 2013

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From the journal Reviews in the Neurosciences Volume 24 Issue 3

Abstract

An increasing awareness of the interaction between gait and cognition has occurred over recent time. This interaction is even more prominent in Parkinson’s disease (PD), where the alteration of striatal dopamine deficiency places a greater emphasis on cognition to compensate for the gait disturbances seen in PD. This dissertation aims to provide an insight into this interaction in PD and demonstrate how normal gait control mechanisms are altered in PD to more cognitive control. Evidence will be provided which demonstrates a shift between attention and automatic gait control mechanisms toward attention. In addition, it will be demonstrated that, because of the cognitive dysfunction that also occurs in PD, the capacity to normalize gait still remains impaired and becomes more subject to the effects of external environmental influences. Further, a rationale will be provided to utilize this interaction in a more beneficial manner, to assist the attention control mechanisms to return gait towards normal. This latter approach is applicable to all aspects of gait disorders in PD and forms a basis for possible intervention therapies.

Keywords: attention; basal ganglia; cognition; gait; Parkinson’s disease

Corresponding author: Robert Iansek, Clinical Research Centre for Movement Disorders and Gait, Kingston Centre, Warrigal Road, Cheltenham, VIC 3192, Australia

About the authors

Robert Iansek

Robert Iansek is Professor of Geriatric Neurology at Monash University in Melbourne, and Director of the Victorian Comprehensive Parkinson Program (VCPP) as well as Director of Clinical Research Centre for Movement Disorders & Gait at the Kingston Centre, Southern Health in Melbourne. He is a Neurologist by training and has over 25 years neurophysiological research experience, having published over 150 articles, books, and videos. His main research interests’ concern basal ganglia function and malfunctions in Parkinson’s disease, cortical gait control mechanisms and rehabilitation in Parkinson’s disease. Professor Iansek was instrumental in the development and use of multi disciplinary rehabilitation for people with Parkinson’s disease and its implementation in both the public and private health systems in Australia.

Mary Danoudis

Mary Danoudis is a research physiotherapist and clinician working with people with Parkinson’s disease at the Clinical Research Centre for Movement Disorders and Gait, Kingston Centre, Monash Health. Her research expertise is in rehabilitation for Parkinson’s disease and understanding changes in the brain responsible for walking disorders. She has a Research Masters in Physiotherapy.

Nicholas Bradfield

Dr Nicholas Bradfield is a clinical neuropsychologist and lecturer in behavioural neuroscience. He completed his doctoral thesis examining the effects of repetitive Transcranial Magnetic Stimulation on the dorsolateral prefrontal cortex using functional Magnetic Resonance Imaging. He currently works in movement disorders, aged psychiatry, trauma, consultation liaison and neurosurgery. His special interests include dementia, Parkinson’s disease, frontotemporal dementia and the anatomy of the prefrontal cortex and the hippocampus.

References

Alexander, G.E., Delong, M.R., and Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381.10.1146/annurev.ne.09.030186.002041Search in Google Scholar

Baddeley, A. (1986). Working memory (Oxford: Clarendon Press).Search in Google Scholar

Ballard, C.G., Aarsland, D., McKeith, I., O’Brien, J., Gray, A., Cormack, F., Burn, D., Cassidy, T., Starfeldt, R., Larsen. J.P., et al. (2002). Fluctuations in attention: PD dementia vs DLB with parkinsonism. Neurology 59, 1714–1720.10.1212/01.WNL.0000036908.39696.FDSearch in Google Scholar

Bernstein, N.A. (1967). The Co-ordination and regulation of movements (London: Pergamon Press Ltd.).Search in Google Scholar

Bohnen, N.I., Kaufer, D.I., Hendrickson, R., Ivanco, L.S., Lopresti, B.J., and Constantine, G.M. (2006). Cognitive correlates of cortical cholinergic denervation in Parkinson’s disease and parkinsonian dementia. J. Neurol. 253, 242–247.10.1007/s00415-005-0971-0Search in Google Scholar

Bohnen, N.I., Muller, M.L., Koeppe, R.A., Studenski, S.A., Kilbourn, M.A., Frey, K.A., and Albin, R.L. (2009). History of falls in Parkinson disease is associated with reduced cholinergic activity. Neurology 73, 1670–1676.10.1212/WNL.0b013e3181c1ded6Search in Google Scholar

Bond, J.M. and Morris, M. (2000). Goal-directed secondary motor tasks: Their effects on gait in subjects with Parkinson disease. Arch. Phys. Med. Rehabil. 81, 110–116.10.1016/S0003-9993(00)90230-2Search in Google Scholar

Bondi, M.W., Kaszniak, A.W., Bayles, K.A., and Vance, K.T. (1993). Contributions of frontal system dysfunction to memory and perceptual abilities in Parkinson’s disease. Neuropsychology 17, 89–102.10.1037/0894-4105.7.1.89Search in Google Scholar

Brønnick, K. (2010). Cognitive profiles in Parkinson’s disease dementia. Cognitive impairment and dementia in Parkinson’s disease. M. Emre, ed. (Oxford: Oxford University Press), pp. 27–43.10.1093/med/9780199564118.003.004Search in Google Scholar

Brønnick, K.S., Nordby, H., Larsen, J.P., and Aarsland, D. (2010). Disturbance of automatic auditory change detection in dementia associated with Parkinson’s disease: A mismatch negativity study. Neurobiol. Aging 31, 104–113.10.1016/j.neurobiolaging.2008.02.021Search in Google Scholar PubMed

Brotchie, P., Iansek, R., and Horne, M.K. (1991). Motor function of the monkey globus pallidus. Brain 114, 1667–1683.10.1093/brain/114.4.1667Search in Google Scholar PubMed

Caccappolo, E. and Marder, K. (2010). Cognitive impairment in non-demented patients with Parkinson’s Disease. Cognitive impairment and dementia in Parkinson’s disease. M. Emre, ed. (Oxford: Oxford University Press), pp. 179–198.10.1093/med/9780199564118.003.015Search in Google Scholar

Camicioli, R., Oken, B.S., Sexton, G., Kaye, J.A., and Nutt, J.G. (1998). Verbal fluency task affects gait in Parkinson’s disease with motor freezing. J. Geriatr. Psychiatry Neurol. 11, 181–185.10.1177/089198879901100403Search in Google Scholar

Chee, R., Murphy, A., Danoudis, M., Georgiou-Karistianis, N., and Iansek, R. (2009). Gait freezing in Parkinson’s disease and the stride length sequence effect interaction. Brain 132, 2151–2160.10.1093/brain/awp053Search in Google Scholar

Cunnington, R., Iansek, R., Bradshaw, J., and Phillips, J. (1995). Movement-related potentials in Parkinson’s disease. Brain 118, 935–950.10.1093/brain/118.4.935Search in Google Scholar

Cunnington, R., Bradshaw, J.L., and Iansek, R. (1996). The role of the supplementary motor area in the control of voluntary movement. Hum. Mov. Sci. 15, 627–647.10.1016/0167-9457(96)00018-8Search in Google Scholar

Cunnington, R., Iansek, R., and Bradshaw, J.L. (1999). Movement-related potentials in Parkinson’s disease: external cues and attentional strategies. Mov. Disord. 14, 63–68.10.1002/1531-8257(199901)14:1<63::AID-MDS1012>3.0.CO;2-VSearch in Google Scholar

Cunnington, R., Windischberger, C., Deecke, L., and Moser, E. (2002). The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 15, 373–385.10.1006/nimg.2001.0976Search in Google Scholar

de Laat, K.F., Tuladhar, A.M., van Norden, A.G.W., Norris, D.G., Zwiers, M.P., and de Leeuw, F.-E. (2011). Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain 134, 73–83.10.1093/brain/awq343Search in Google Scholar

Deiber, M., Passingham, R., Colebatch, J., Friston, K., Nixon, P., and Frackowiak, R. (1991). Cortical areas and the selection of movement: a study with positron emission tomography. Exp. Brain Res. 84, 393–402.10.1007/BF00231461Search in Google Scholar

Egerton, T., Danoudis, M., Huxham, F., and Iansek, R. (2011). Central gait control mechanisms and the stride length cadence relationship. Gait Posture 34, 178–182.10.1016/j.gaitpost.2011.04.006Search in Google Scholar

Emre, M. (2010). General features, mode of onset and course of dementia in Parkinson’s disease. Cognitive impairment and dementia in Parkinson’s disease. M. Emre, ed. (Oxford: Oxford University Press), pp. 15–26.10.1093/med/9780199564118.003.003Search in Google Scholar

Emre, M., Aarsland, D., Brown, R., Burn, D.J., Duyckaerts, C., Mizuno, Y., Broe, G.A., Cummings, J., Dickson, D.W., Gauthier, S., et al. (2007). Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov. Disord. 22, 1689–1707.10.1002/mds.21507Search in Google Scholar

Fukuyama, H., Ouchi, Y., Matsuzaki, S., Nagahama, Y., Yamauchi, H., Ogawa, M., Kimura, J., and Shibasaki, H. (1997). Brain functional activity during gait in normal subjects: a SPECT study. Neurosci. Lett. 228, 183–186.10.1016/S0304-3940(97)00381-9Search in Google Scholar

Hallett, M. (2008). The intrinsic and extrinsic aspects of freezing of gait. Mov. Disord. 23(S2), S439–S443.10.1002/mds.21836Search in Google Scholar

Helkala, E.-L., Laulumaa, V., Soininen, H., and Riekkinen, P.J. (1988). Recall and recognition memory in patients with Alzheimer’s and Parkinson’s diseases. Ann. Neurol. 24, 214–217.10.1002/ana.410240207Search in Google Scholar

Higginson, C.I., King, D.S., Levine, D., Wheelock, V.L., Khamphay, N.O., and Sigvardt, K.A. (2003). The relationship between executive function and verbal memory in Parkinson’s disease. Brain Cogn. 52, 343–352.10.1016/S0278-2626(03)00180-5Search in Google Scholar

Ho, A.K., Iansek, R., and Bradshaw, J.L. (1999). Regulation of parkinsonian speech volume: the effect of interlocuter distance. J. Neurol. Neurosurg. Psychiatry 67, 199–202.10.1136/jnnp.67.2.199Search in Google Scholar

Hughes, A.J., Daniel, S.E., Blankson, S., and Lees, A.J. (1993). A clinicopathologic study of 100 cases of Parkinson’s disease. Arch. Neurol. 50, 140–148.10.1001/archneur.1993.00540020018011Search in Google Scholar

Huxham, F., Baker, R., Morris, M.E., and Iansek, R. (2008). Footstep adjustments used to turn during walking in Parkinson’s disease. Mov. Disord. 23, 817–823.10.1002/mds.21932Search in Google Scholar

Iansek, R., Huxham, F., and McGinley, J. (2006). The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Mov. Disord. 21, 1419–1424.10.1002/mds.20998Search in Google Scholar

Kehagia, A.A., Barker, R.A., and Robbins, T.W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurology 9, 1200–1213.10.1016/S1474-4422(10)70212-XSearch in Google Scholar

Kwakkel, G., de Goede, C.J.T., and van Wegen, E.E.H. (2007). Impact of physical therapy for Parkinson’s disease: a critical review of the literature. Parkinsonism Relat. Disord. 13(Suppl. 3), S478–S487.10.1016/S1353-8020(08)70053-1Search in Google Scholar

Luria, A.R. (1980). Higher cortical functions in man, 2nd ed. (New York: Basic Books).10.1007/978-1-4615-8579-4Search in Google Scholar

Machado, L., Devine, A., and Wyatt, N. (2009). Distractibility with advancing age and Parkinson’s disease. Neuropsychologia 47, 1756–1764.10.1016/j.neuropsychologia.2009.02.018Search in Google Scholar

Mattila, P.M., Rinne, J.O., Helenius, H., Dickson, D.W., and Röyttä, M. (2000). Alpha-synuclein-immunoreactive cortical Lewy bodies are associated with cognitive impairment in Parkinson’s disease. Acta Neuropathol. 100, 285–290.10.1007/s004019900168Search in Google Scholar

McLennan, J.E., Nakano, K., Tyler, H.R., and Schwab, R.S. (1972). Micrographia in Parkinson’s disease. J. Neurol. Sci. 15, 141–152.10.1016/0022-510X(72)90002-0Search in Google Scholar

Morris, M.E. (2000). Movement disorders in people with Parkinson disease: a model for physical therapy. Phys. Ther. 80, 578–597.10.1093/ptj/80.6.578Search in Google Scholar

Morris, M.E., Iansek, R., Matyas, T.A., and Summers, J.J. (1994). The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 117, 1169–1181.10.1093/brain/117.5.1169Search in Google Scholar PubMed

Morris, M., Iansek, R., Matyas, T., and Summers, J. (1998). Abnormalities in the stride length-cadence relation in parkinsonian gait. Mov. Disord. 13, 61–69.10.1002/mds.870130115Search in Google Scholar PubMed

Morris, M., Iansek, R., McGinley, J., Matyas, T., and Huxham, F. (2005). Three dimensional gait biomechanics in Parkinson’s disease: Evidence for a centrally mediated amplitude regulation disorder. Mov. Disord. 20, 40–50.10.1002/mds.20278Search in Google Scholar PubMed

Mosimann, U.P., Mather, G., Wesnes, K.A., O’Brien, J.T., Burn, D.J., and McKeith, I.G. (2004). Visual perception in Parkinson disease dementia and dementia with Lewy bodies. Neurology 63, 2091–2096.10.1212/01.WNL.0000145764.70698.4ESearch in Google Scholar

O’Shea, S., Morris, M.E., and Iansek, R. (2002). Dual task interference during gait in people with Parkinson disease: effects of motor versus cognitive secondary tasks. Phys. Ther. 82, 888–897.10.1093/ptj/82.9.888Search in Google Scholar

Olanow, C.W., Stern, M.B., and Sethi, K. (2009). The scientific and clinical basis for the treatment of Parkinson disease. Neurology 72, S1–S136.Search in Google Scholar

Owen, A.M. (2004). Cognitive dysfunction in Parkinson’s disease: The role of frontostriatal circuitry. Neuroscientist 10, 525–537.10.1177/1073858404266776Search in Google Scholar PubMed

Piggot, M.A. and Perry, E.K. (2010). Neurochemical pathology of Parkinson’s disease dementia. Cognitive impairment and dementia in Parkinson’s disease. M. Emre, ed. (Oxford: Oxford University Press), pp. 153–170.10.1093/med/9780199564118.003.013Search in Google Scholar

Revuelta, G.J. and Lippa, C. (2010). Pathological correlates of dementia in Parkinson’s disease. Cognitive impairment and dementia in Parkinson’s disease. M. Emre, ed. (Oxford: Oxford University Press), pp. 171–178.10.1093/med/9780199564118.003.014Search in Google Scholar

Rinne, J.O., Rummukainen, J., Paljhi, L., and Rinne, U.K. (1989). Dementia in Parkinson’s disease is related to neuronal loss in the medial substantia nigra. Arch. Neurol. 26, 47–50.10.1002/ana.410260107Search in Google Scholar PubMed

Rochester, L., Nieuwboer, A., Baker, K., Hetherington, V., Willems, A.M., Chavret, F., Kwakkel, G., Van Wegen, E., Lim, I., and 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. 14, 1243–1248.10.1007/s00702-007-0756-ySearch in Google Scholar PubMed

Schaafsma, J.D., Balash, Y., Gurevich, T., Bartels, A.L., Hausdorff, J.M., and Giladi, N. (2003). Characterization of freezing of gait subtypes and the response of each to levodopa in Parkinson’s disease. Eur. J. Neurol. 10, 391–398.10.1046/j.1468-1331.2003.00611.xSearch in Google Scholar PubMed

Shin, J., Choi, S., Lee, J.E., Lee, H.S., Sohn, Y.H., and Lee, P.H. (2012). Subcortical white matter hyperintensities within the cholinergic pathways of Parkinson’s disease patients according to cognitive status. J. Neurol. Neurosurg. Psychiatry 83, 315–321.10.1136/jnnp-2011-300872Search in Google Scholar PubMed

Shoushtarian, M., Murphy, A., and Iansek, R. (2011). Examination of central gait control mechanisms in Parkinson’s disease using movement-related potentials. Mov. Disord. 26, 2347–2353.10.1002/mds.23844Search in Google Scholar PubMed

Snijders, A.H., Leunissen, I., Bakker, M., Overeem, S., Helmich, R.C., Bloem, B.R., and Toni, I. (2011). Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134, 59–72.10.1093/brain/awq324Search in Google Scholar PubMed

Stam, C.J., Visser, S.L., Op de Coul, A.A.W., De Sonneville, L.M.J., Schellens, R.L.L.A., Brunia, C.H.M., de Smet, J.S., and Gielen, G. (1993). Disturbed frontal regulation of attention in Parkinson’s disease. Brain 116, 1139–1158.10.1093/brain/116.5.1139Search in Google Scholar PubMed

Stella, F., Gobbi, L.T., Gobbi, S., Oliani, M.M., Tanaka, K., and Pieruccini-Faria, F. (2007). Early impairment of cognitive functions in Parkinson’s disease. Arq. Neuropsiquiatr. 65, 406–410.10.1590/S0004-282X2007000300008Search in Google Scholar

Thevathasan, W., Cole, M.H., Graepel, C.L., Hyam, J.A., Jenkinson, N., Brittain, J.-S., Coyne, T.J., Silburn, P.A., Aziz, T.Z., Kerr, G., et al. (2012). A spatiotemporal analysis of gait freezing and the impact of pedunculopontine nucleus stimulation. Brain 135, 1446–1454.10.1093/brain/aws039Search in Google Scholar PubMed PubMed Central

Weintraub, D., Moberg, P.J., Culbertson, W.C., Duda, J.E., and Stern, M.B. (2004). Evidence for impaired encoding and retrieval memory profiles in Parkinson disease. Cogn. Behav. Neurol. 17, 195–200.Search in Google Scholar

Werheid, K., Koch, I., Reichert, K., and Brass, M. (2007). Impaired self-initiated task preparation during task switching in Parkinson’s disease. Neuropsychologia 45, 273–281.10.1016/j.neuropsychologia.2006.07.007Search in Google Scholar PubMed

Wu, T. and Hallett, M. (2005). A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain 128, 2250–2259.10.1093/brain/awh569Search in Google Scholar PubMed

Wu, T., Kansaku, K., and Hallett, M. (2004). How self-initiated memorized movements become automatic: a functional MRI study. J. Neurophysiol. 91, 1690–1698.10.1152/jn.01052.2003Search in Google Scholar PubMed

Wu, T., Chan, P., and Hallett, M. (2010). Effective connectivity of neural networks in automatic movements in Parkinson’s disease. Neuroimage 49, 2581–2587.10.1016/j.neuroimage.2009.10.051Search in Google Scholar PubMed PubMed Central

Yogev-Seligmann, G., Hausdorff, J.M., and Giladi, N. (2008). The role of executive function and attention in gait. Mov. Disord. 23, 329–342.10.1002/mds.21720Search in Google Scholar PubMed PubMed Central

Received: 2013-3-8

Accepted: 2013-3-31

Published Online: 2013-05-06

Published in Print: 2013-06-01

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https://doi.org/10.1515/revneuro-2013-0006

Keywords for this article

attention; basal ganglia; cognition; gait; Parkinson’s disease