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Licensed Unlicensed Requires Authentication Published by De Gruyter March 11, 2016

Postural instability and falls in Parkinson’s disease

  • Jacob J. Crouse , Joseph R. Phillips , Marjan Jahanshahi and Ahmed A. Moustafa EMAIL logo

Abstract

Postural instability (PI) is one of the most debilitating motor symptoms of Parkinson’s disease (PD), as it is associated with an increased risk of falls and subsequent medical complications (e.g. fractures), fear of falling, decreased mobility, self-restricted physical activity, social isolation, and decreased quality of life. The pathophysiological mechanisms underlying PI in PD remain elusive. This short review provides a critical summary of the literature on PI in PD, covering the clinical features, the neural and cognitive substrates, and the effects of dopaminergic medications and deep brain stimulation. The delayed effect of dopaminergic medication combined with the success of extrastriatal deep brain stimulation suggests that PI involves neurotransmitter systems other than dopamine and brain regions extending beyond the basal ganglia, further challenging the traditional view of PD as a predominantly single-system neurodegenerative disease.


Corresponding author: Ahmed A. Moustafa, School of Social Sciences and Psychology, Western Sydney University, Sydney, New South Wales, Australia, e-mail: ; and Marcs Institute for Brain and Behaviour, Western Sydney University, Sydney, New South Wales, 2214, Australia

References

Adkin, A.L., Frank, J.S., and Jog, M.S. (2003). Fear of falling and postural control in Parkinson’s disease. Mov. Disord. 18, 496–502.10.1002/mds.10396Search in Google Scholar

Allcock, L.M., Rowan, E.N., Steen, I.N., Wesnes, K., Kenny, R.A., and Burn, D.J. (2009). Impaired attention predicts falling in Parkinson’s disease. Parkinsonism Relat. Disord. 15, 110–115.10.1016/j.parkreldis.2008.03.010Search in Google Scholar

Alves, G., Larsen, J.P., Emre, M., Wentzel-Larsen, T., and Aarsland, D. (2006). Changes in motor subtype and risk for incident dementia in Parkinson’s disease. Mov. Disord. 21, 1123–1130.10.1002/mds.20897Search in Google Scholar

Armand, S., Landis, T., Sztajzel, R., and Burkhard, P.R. (2009). Dyskinesia-induced postural instability in Parkinson’s disease. Parkinsonism Relat. Disord. 15, 359–364.10.1016/j.parkreldis.2008.08.007Search in Google Scholar

Ashburn, A., Stack, E., Pickering, R.M., and Ward, C.D. (2001). A community-dwelling sample of people with Parkinson’s disease: characteristics of fallers and non-fallers. Age Ageing 30, 47–52.10.1093/ageing/30.1.47Search in Google Scholar

Balash, Y., Peretz, C., Leibovich, G., Herman, T., Hausdorff, J.M., and Giladi, N. (2005). Falls in outpatients with Parkinson’s disease: frequency, impact and identifying factors. J. Neurol. 252, 1310–1315.10.1007/s00415-005-0855-3Search in Google Scholar

Beckley, D.J., Panzer, V.P., Remler, M.P., Ilog, L.B., and Bloem, B.R. (1995). Clinical correlates of motor performance during paced postural tasks in Parkinson’s disease. J. Neurol. Sci. 132, 133–138.10.1016/0022-510X(95)00130-TSearch in Google Scholar

Bejjani, B.P., Gervais, D., Arnulf, I., Papadopoulos, S., Demeret, S., Bonnet, A.M., Cornu, P., Damier, P., and Agid, Y. (2000). Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation. J. Neurol. Neurosurg. Psychiatry 68, 595–600.10.1136/jnnp.68.5.595Search in Google Scholar PubMed PubMed Central

Bloem, B.R., Beckley, D.J., van Dijk, J.G., Zwinderman, A.H., Remler, M.P., and Roos, R.A. (1996). Influence of dopaminergic medication on automatic postural responses and balance impairment in Parkinson’s disease. Mov. Disord. 11, 509–521.10.1002/mds.870110506Search in Google Scholar PubMed

Bloem, B.R., Grimbergen, Y.A., Cramer, M., Willemsen, M., and Zwinderman, A.H. (2001). Prospective assessment of falls in Parkinson’s disease. J. Neurol. 248, 950–958.10.1007/s004150170047Search in Google Scholar PubMed

Bloem, B.R., Hausdorff, J.M., Visser, J.E., and Giladi, N. (2004). Falls and freezing of gait in Parkinson’s disease: a review of two interconnected, episodic phenomena. Mov. Disord. 19, 871–884.10.1002/mds.20115Search 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

Bohnen, N.I., Muller, M.L., Kotagal, V., Koeppe, R.A., Kilbourn, M.R., Gilman, S., Albin, R.L., and Frey, K.A. (2012). Heterogeneity of cholinergic denervation in Parkinson’s disease without dementia. J. Cereb. Blood Flow Metab. 32, 1609–1617.10.1038/jcbfm.2012.60Search in Google Scholar

Borel, L. and Alescio-Lautier, B. (2014). Posture and cognition in the elderly: interaction and contribution to the rehabilitation strategies. Neurophysiol. Clin. 44, 95–107.10.1016/j.neucli.2013.10.129Search in Google Scholar

Bronte-Stewart, H.M., Minn, A.Y., Rodrigues, K., Buckley, E.L., and Nashner, L.M. (2002). Postural instability in idiopathic Parkinson’s disease: the role of medication and unilateral pallidotomy. Brain 125, 2100–2114.10.1093/brain/awf207Search in Google Scholar

Burn, D.J., Rowan, E.N., Allan, L.M., Molloy, S., O’Brien, J.T., and McKeith, I.G. (2006). Motor subtype and cognitive decline in Parkinson’s disease, Parkinson’s disease with dementia, and dementia with Lewy bodies. J. Neurol. Neurosurg. Psychiatry 77, 585–589.10.1136/jnnp.2005.081711Search in Google Scholar

Cakit, B.D., Saracoglu, M., Genc, H., Erdem, H.R., and Inan, L. (2007). The effects of incremental speed-dependent treadmill training on postural instability and fear of falling in Parkinson’s disease. Clin. Rehabil. 21, 698–705.10.1177/0269215507077269Search in Google Scholar

Camicioli, R. and Majumdar, S.R. (2010). Relationship between mild cognitive impairment and falls in older people with and without Parkinson’s disease: 1-year prospective cohort study. Gait Posture 32, 87–91.10.1016/j.gaitpost.2010.03.013Search in Google Scholar

Chastan, N., Debono, B., Maltete, D., and Weber, J. (2008). Discordance between measured postural instability and absence of clinical symptoms in Parkinson’s disease patients in the early stages of the disease. Mov. Disord. 23, 366–372.10.1002/mds.21840Search in Google Scholar

Chong, R.K., Horak, F.B., and Woollacott, M.H. (2000). Parkinson’s disease impairs the ability to change set quickly. J. Neuro. Sci. 175, 13.10.1016/S0022-510X(00)00277-XSearch in Google Scholar

Chong, R.K., Morgan, J., Mehta, S.H., Pawlikowska, I., Hall, P., Ellis, A.V., Ibanez-Wong, A.D., Miller, G.M., Baugh, K., and Sethi, K. (2011). Rapid Assessment of Postural Instability in Parkinson’s Disease (RAPID): a pilot study. Eur. J. Neurol. 18, 260–265.10.1111/j.1468-1331.2010.03115.xSearch in Google Scholar PubMed

Chung, K.A., Lobb, B.M., Nutt, J.G., and Horak, F.B. (2010). Effects of a central cholinesterase inhibitor on reducing falls in Parkinson disease. Neurology 75, 1263–1269.10.1212/WNL.0b013e3181f6128cSearch in Google Scholar PubMed PubMed Central

Domellof, M.E., Elgh, E., and Forsgren, L. (2011). The relation between cognition and motor dysfunction in drug-naive newly diagnosed patients with Parkinson’s disease. Mov. Disord. 26, 2183–2189.10.1002/mds.23814Search in Google Scholar PubMed

Gervais-Bernard, H., Xie-Brustolin, J., Mertens, P., Polo, G., Klinger, H., Adamec, D., Broussolle, E., and Thobois, S. (2009). Bilateral subthalamic nucleus stimulation in advanced Parkinson’s disease: five year follow-up. J. Neurol. 256, 225–233.10.1007/s00415-009-0076-2Search in Google Scholar PubMed

Geurts, A.C., Boonstra, T.A., Voermans, N.C., Diender, M.G., Weerdesteyn, V., and Bloem, B.R. (2011). Assessment of postural asymmetry in mild to moderate Parkinson’s disease. Gait Posture 33, 143–145.10.1016/j.gaitpost.2010.09.018Search in Google Scholar PubMed

Gratwicke, J., Jahanshahi, M., and Foltynie, T. (2015). Parkinson’s disease dementia: a neural networks perspective. Brain 138, 1454–1476.10.1093/brain/awv104Search in Google Scholar PubMed PubMed Central

Gray, P. and Hildebrand, K. (2000). Fall risk factors in Parkinson’s disease. J. Neurosci. Nurs. 32, 222–228.10.1097/01376517-200008000-00006Search in Google Scholar PubMed

Grimbergen, Y.A., Munneke, M., and Bloem, B.R. (2004). Falls in Parkinson’s disease. Curr. Opin. Neurol. 17, 405–415.10.1097/01.wco.0000137530.68867.93Search in Google Scholar PubMed

Grimbergen, Y.A., Langston, J.W., Roos, R.A., and Bloem, B.R. (2009). Postural instability in Parkinson’s disease: the adrenergic hypothesis and the locus coeruleus. Exp. Rev. Neurother. 9, 279–290.10.1586/14737175.9.2.279Search in Google Scholar PubMed

Hilker, R., Thomas, A.V., Klein, J.C., Weisenbach, S., Kalbe, E., Burghaus, L., Jacobs, A.H., Herholz, K., and Heiss, W.D. (2005). Dementia in Parkinson disease: functional imaging of cholinergic and dopaminergic pathways. Neurology 65, 1716–1722.10.1212/01.wnl.0000191154.78131.f6Search in Google Scholar PubMed

Holmes, J.D., Jenkins, M.E., Johnson, A.M., Adams, S.G., and Spaulding, S.J. (2010). Dual-task interference: the effects of verbal cognitive tasks on upright postural stability in Parkinson’s disease. Parkinsons Dis. 2010, 696492.10.4061/2010/696492Search in Google Scholar PubMed PubMed Central

Horak, F.B., Frank, J., and Nutt, J. (1996). Effects of dopamine on postural control in parkinsonian subjects: scaling, set, and tone. J. Neurophysiol. 75, 16.10.1152/jn.1996.75.6.2380Search in Google Scholar PubMed

Horak, F.B., Dimitrova, D., and Nutt, J.G. (2005). Direction-specific postural instability in subjects with Parkinson’s disease. Exp. Neurol. 193, 504–521.10.1016/j.expneurol.2004.12.008Search in Google Scholar PubMed

Jankovic, J. (2008). Parkinson’s disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 79, 368–376.10.1136/jnnp.2007.131045Search in Google Scholar PubMed

Jankovic, J., McDermott, M., Carter, J., Gauthier, S., Goetz, C., Golbe, L., Huber, S., Koller, W., Olanow, C., Shoulson, I., et al. (1990). Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology 40, 1529–1534.10.1212/WNL.40.10.1529Search in Google Scholar

Karachi, C., Grabli, D., Bernard, F.A., Tande, D., Wattiez, N., Belaid, H., Bardinet, E., Prigent, A., Nothacker, H.P., Hunot, S., et al. (2010). Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J. Clin. Invest. 120, 2745–2754.10.1172/JCI42642Search in Google Scholar PubMed PubMed Central

Kelly, V.E., Johnson, C.O., McGough, E.L., Shumway-Cook, A., Horak, F.B., Chung, K.A., Espay, A.J., Revilla, F.J., Devoto, J., Wood-Siverio, C., et al. (2015). Association of cognitive domains with postural instability/gait disturbance in Parkinson’s disease. Parkinsonism Relat. Disord. 21, 692–697.10.1016/j.parkreldis.2015.04.002Search in Google Scholar PubMed PubMed Central

Kim, S.D., Allen, N.E., Canning, C.G., and Fung, V.S. (2013). Postural instability in patients with Parkinson’s disease. Epidemiology, pathophysiology and management. CNS Drugs 27, 97–112.10.1007/s40263-012-0012-3Search in Google Scholar PubMed

King, L.A. and Horak, F.B. (2008). Lateral stepping for postural correction in Parkinson’s disease. Arch. Phys. Med. Rehabil. 89, 492–499.10.1016/j.apmr.2007.11.017Search in Google Scholar PubMed PubMed Central

Koller, W.C., Glatt, S., Vetere-Overfield, B., and Hassanein, R. (1989). Falls and Parkinson’s disease. Clin. Neuropharmacol. 12, 98–105.10.1097/00002826-198904000-00003Search in Google Scholar PubMed

Kringelbach, M.L., Jenkinson, N., Owen, S.L., and Aziz, T.Z. (2007). Translational principles of deep brain stimulation. Nat. Rev. Neurosci. 8, 623–635.10.1038/nrn2196Search in Google Scholar PubMed

Lee, J.E., Cho, K.H., Kim, M., Sohn, Y.H., and Lee, P.H. (2012). The pattern of cortical atrophy in Parkinson’s disease with mild cognitive impairment according to the timing of cognitive dysfunction. J. Neurol. 259, 469–473.10.1007/s00415-011-6203-xSearch in Google Scholar PubMed

Lord, S., Galna, B., Coleman, S., Yarnall, A., Burn, D., and Rochester, L. (2014). Cognition and gait show a selective pattern of association dominated by phenotype in incident Parkinson’s disease. Front. Aging Neurosci. 6, 249.10.3389/fnagi.2014.00249Search in Google Scholar PubMed PubMed Central

Lyons, K.E., Wilkinson, S.B., Troster, A.I., and Pahwa, R. (2002). Long-term efficacy of globus pallidus stimulation for the treatment of Parkinson’s disease. Stereotact. Funct. Neurosurg. 79, 214–220.10.1159/000070834Search in Google Scholar PubMed

Lyoo, C.H., Aalto, S., Rinne, J.O., Lee, K.O., Oh, S.H., Chang, J.W., and Lee, M.S. (2007). Different cerebral cortical areas influence the effect of subthalamic nucleus stimulation on parkinsonian motor deficits and freezing of gait. Mov Disord. 22, 6.10.1002/mds.21609Search in Google Scholar PubMed

Mancini, M., Rocchi, L., Horak, F.B., and Chiari, L. (2008). Effects of Parkinson’s disease and levodopa on functional limits of stability. Clin. Biomech. (Bristol, Avon) 23, 450–458.10.1016/j.clinbiomech.2007.11.007Search in Google Scholar PubMed PubMed Central

Mancini, M., Horak, F.B., Zampieri, C., Carlson-Kuhta, P., Nutt, J.G., and Chiari, L. (2011). Trunk accelerometry reveals postural instability in untreated Parkinson’s disease. Parkinsonism Relat. Disord. 17, 557–562.10.1016/j.parkreldis.2011.05.010Search in Google Scholar PubMed PubMed Central

Marchese, R., Bove, M., and Abbruzzese, G. (2003). Effect of cognitive and motor tasks on postural stability in Parkinson’s disease: a posturographic study. Mov. Disord. 18, 652–658.10.1002/mds.10418Search in Google Scholar PubMed

McVey, M.A., Stylianou, A.P., Luchies, C.W., Lyons, K.E., Pahwa, R., Jernigan, S., and Mahnken, J.D. (2009). Early biomechanical markers of postural instability in Parkinson’s disease. Gait Posture 30, 538–542.10.1016/j.gaitpost.2009.08.232Search in Google Scholar PubMed

Mena-Segovia, J., Bolam, J.P., and Magill, P.J. (2004). Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci. 27, 585–588.10.1016/j.tins.2004.07.009Search in Google Scholar PubMed

Merola, A., Zibetti, M., Angrisano, S., Rizzi, L., Ricchi, V., Artusi, C.A., Lanotte, M., Rizzone, M.G., and Lopiano, L. (2011). Parkinson’s disease progression at 30 years: a study of subthalamic deep brain-stimulated patients. Brain 134, 2074–2084.10.1093/brain/awr121Search in Google Scholar PubMed

Michalowska, M., Fiszer, U., Krygowska-Wajs, A., and Owczarek, K. (2005). Falls in Parkinson’s disease. Causes and impact on patients’ quality of life. Funct. Neurol. 20, 163–168.Search in Google Scholar

Moro, E., Hamani, C., Poon, Y.Y., Al-Khairallah, T., Dostrovsky, J.O., Hutchison, W.D., and Lozano, A.M. (2010). Unilateral pedunculopontine stimulation improves falls in Parkinson’s disease. Brain 133, 215–224.10.1093/brain/awp261Search in Google Scholar PubMed

Muller, M.L. and Bohnen, N.I. (2013). Cholinergic dysfunction in Parkinson’s disease. Curr. Neurol. Neurosci. Rep. 13, 377.10.1007/s11910-013-0377-9Search in Google Scholar PubMed PubMed Central

Nocera, J.R., Price, C., Fernandez, H.H., Amano, S., Vallabhajosula, S., Okun, M.S., Hwynn, N., and Hass, C.J. (2010). Tests of dorsolateral frontal function correlate with objective tests of postural stability in early to moderate stage Parkinson’s disease. Parkinsonism Relat. Disord. 16, 590–594.10.1016/j.parkreldis.2010.08.008Search in Google Scholar PubMed PubMed Central

Nonnekes, J., de Kam, D., Oude Nijhuis, L.B., van Geel, K., Bloem, B.R., Geurts, A., and Weerdesteyn, V. (2015). StartReact effects support different pathophysiological mechanisms underlying freezing of gait and postural instability in Parkinson’s disease. PLoS One 10, e0122064.10.1371/journal.pone.0122064Search in Google Scholar PubMed PubMed Central

Ondo, W.G. and Hunter, C. (2003). Flumazenil, a GABA antagonist, may improve features of Parkinson’s disease. Mov. Disord. 18, 683–685.10.1002/mds.10426Search in Google Scholar PubMed

Paul, S.S., Sherrington, C., Canning, C.G., Fung, V.S., Close, J.C., and Lord, S.R. (2014). The relative contribution of physical and cognitive fall risk factors in people with Parkinson’s disease: a large prospective cohort study. Neurorehabil. Neural Repair 28, 282–290.10.1177/1545968313508470Search in Google Scholar PubMed

Perry, E.K., Curtis, M., Dick, D.J., Candy, J.M., Atack, J.R., Bloxham, C.A., Blessed, G., Fairbairn, A., Tomlinson, B.E., and Perry, R.H. (1985). Cholinergic correlates of cognitive impairment in Parkinson’s disease: comparisons with Alzheimer’s disease. J. Neurol. Neurosurg Psychiatry 48, 413–421.10.1136/jnnp.48.5.413Search in Google Scholar PubMed PubMed Central

Plaha, P. and Gill, S.S. (2005). Bilateral deep brain stimulation of the pedunculopontine nucleus for Parkinson’s disease. Neuroreport 16, 1883–1887.10.1097/01.wnr.0000187637.20771.a0Search in Google Scholar PubMed

Poletti, M., Frosini, D., Pagni, C., Baldacci, F., Nicoletti, V., Tognoni, G., Lucetti, C., Del Dotto, P., Ceravolo, R., and Bonuccelli, U. (2012). Mild cognitive impairment and cognitive-motor relationships in newly diagnosed drug-naive patients with Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 83, 601–606.10.1136/jnnp-2011-301874Search in Google Scholar PubMed

Putzki, N., Maschke, M., Drepper, J., Diener, H.C., and Timmann, D. (2002). Effect of functional NMDA-antagonist flupirtine on automatic postural responses in Parkinson’s disease. J. Neurol. 249, 824–828.10.1007/s00415-002-0727-zSearch in Google Scholar PubMed

Rahman, S., Griffin, H.J., Quinn, N.P., and Jahanshahi, M. (2011). On the nature of fear of falling in Parkinson’s disease. Behav. Neurol. 24, 219–228.10.1155/2011/274539Search in Google Scholar

Rocchi, L., Chiari, L., and Horak, F.B. (2002). Effects of deep brain stimulation and levodopa on postural sway in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 73, 267–274.10.1136/jnnp.73.3.267Search in Google Scholar PubMed PubMed Central

Rocchi, L., Carlson-Kuhta, P., Chiari, L., Burchiel, K.J., Hogarth, P., and Horak, F.B. (2012). Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease. J. Neurosurg. 117, 1141–1149.10.3171/2012.8.JNS112006Search in Google Scholar PubMed PubMed Central

Rodriguez-Oroz, M.C., Obeso, J.A., Lang, A.E., Houeto, J.L., Pollak, P., Rehncrona, S., Kulisevsky, J., Albanese, A., Volkmann, J., Hariz, M.I., et al. (2005). Bilateral deep brain stimulation in Parkinson’s disease: a multicentre study with 4 years follow-up. Brain 128, 2240–2249.10.1093/brain/awh571Search in Google Scholar PubMed

Rosenberg-Katz, K., Herman, T., Jacob, Y., Giladi, N., Hendler, T., and Hausdorff, J.M. (2013). Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 80, 1476–1484.10.1212/WNL.0b013e31828cfaa4Search in Google Scholar PubMed PubMed Central

Sarter, M., Albin, R.L., Kucinski, A., and Lustig, C. (2014). Where attention falls: increased risk of falls from the converging impact of cortical cholinergic and midbrain dopamine loss on striatal function. Exp. Neurol. 257, 120–129.10.1016/j.expneurol.2014.04.032Search in Google Scholar PubMed PubMed Central

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

Schmit, J.M., Riley, M.A., Dalvi, A., Sahay, A., Shear, P.K., Shockley, K.D., and Pun, R.Y. (2006). Deterministic center of pressure patterns characterize postural instability in Parkinson’s disease. Exp. Brain Res. 168, 357–367.10.1007/s00221-005-0094-ySearch in Google Scholar PubMed

Shine, J.M., Frank, M.J., Moustafa, A.A., and Lewis, S.J. (2013). Freezing of gait in Parkinson’s disease is associated with functional decoupling between the cognitive control network and the basal ganglia. Brain 136, 3671–3681.10.1093/brain/awt272Search in Google Scholar PubMed

Shivitz, N., Koop, M.M., Fahimi, J., Heit, G., and Bronte-Stewart, H.M. (2006). Bilateral subthalamic nucleus deep brain stimulation improves certain aspects of postural control in Parkinson’s disease, whereas medication does not. Mov. Disord. 21, 1088–1097.10.1002/mds.20905Search in Google Scholar PubMed

Sidiropoulos, C., Walsh, R., Meaney, C., Poon, Y.Y., Fallis, M., and Moro, E. (2013). Low-frequency subthalamic nucleus deep brain stimulation for axial symptoms in advanced Parkinson’s disease. J. Neurol. 260, 2306–2311.10.1007/s00415-013-6983-2Search in Google Scholar PubMed

Stefani, A., Lozano, A.M., Peppe, A., Stanzione, P., Galati, S., Tropepi, D., Pierantozzi, M., Brusa, L., Scarnati, E., and Mazzone, P. (2007). Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson’s disease. Brain 130, 1596–1607.10.1093/brain/awl346Search in Google Scholar PubMed

St. George, R.J.S., Nutt, J.G., Burchiel, K.J., and Horak, F.B. (2010). A meta-regression of the long-term effects of deep brain stimulation on balance and gait in PD. Neurology. 75, 7.10.1212/WNL.0b013e3181f61329Search in Google Scholar PubMed PubMed Central

Tykocki, T., Mandat, T., and Nauman, P. (2011). Pedunculopontine nucleus deep brain stimulation in Parkinson’s disease. Arch. Med. Sci. 7, 555–564.10.5114/aoms.2011.24119Search in Google Scholar PubMed PubMed Central

Verbaan, D., Marinus, J., Visser, M., van Rooden, S.M., Stiggelbout, A.M., Middelkoop, H.A., and Hilten, J.J. (2007). Cognitive impairment in Parkinson’s disease. J. Neurol. Neurosurg. Psychiatry 78, 1182–1187.10.1136/jnnp.2006.112367Search in Google Scholar PubMed PubMed Central

Visser, J.E., Carpenter, M.G., van der Kooij, H., and Bloem, B.R. (2008). The clinical utility of posturography. Clin. Neurophysiol. 119, 2424–2436.10.1016/j.clinph.2008.07.220Search in Google Scholar PubMed

Volkmann, J., Allert, N., Voges, J., Sturm, V., Schnitzler, A., and Freund, H.J. (2004). Long-term results of bilateral pallidal stimulation in Parkinson’s disease. Ann. Neurol. 55, 871–875.10.1002/ana.20091Search in Google Scholar PubMed

Welter, M.L., Demain, A., Ewenczyk, C., Czernecki, V., Lau, B., El Helou, A., Belaid, H., Yelnik, J., François, C., Bardinet, E., et al. (2015). PPNa-DBS for gait and balance disorders in Parkinson’s disease: a double-blind, randomised study. J. Neurol. 262, 10.10.1007/s00415-015-7744-1Search in Google Scholar PubMed

Whitehouse, P.J., Hedreen, J.C., White, C.L., 3rd, and Price, D.L. (1983). Basal forebrain neurons in the dementia of Parkinson disease. Ann. Neurol. 13, 243–248.10.1002/ana.410130304Search in Google Scholar PubMed

Williams-Gray, C.H., Hampshire, A., Robbins, T.W., Owen, A.M., and Barker, R.A. (2007). Catechol O-methyltransferase Val158Met genotype influences frontoparietal activity during planning in patients with Parkinson’s disease. J. Neurosci. 27, 4832–4838.10.1523/JNEUROSCI.0774-07.2007Search in Google Scholar PubMed PubMed Central

Wood, B.H., Bilclough, J.A., Bowron, A., and Walker, R.W. (2002). Incidence and prediction of falls in Parkinson’s disease: a prospective multidisciplinary study. J. Neurol. Neurosurg. Psychiatry 72, 721–725.10.1136/jnnp.72.6.721Search in Google Scholar PubMed PubMed Central

Yamada, K., Goto, S., Hamasaki, T., and Kuratsu, J.I. (2008). Effect of bilateral subthalamic nucleus stimulation on levodopa-unresponsive axial symptoms in Parkinson’s disease. Acta Neurochir. (Wien) 150, 15–22.10.1007/s00701-007-1451-3Search in Google Scholar PubMed

Yarnall, A., Rochester, L., and Burn, D.J. (2011). The interplay of cholinergic function, attention, and falls in Parkinson’s disease. Mov. Disord. 26, 2496–2503.10.1002/mds.23932Search in Google Scholar PubMed

Received: 2016-1-31
Accepted: 2016-2-14
Published Online: 2016-3-11
Published in Print: 2016-7-1

©2016 by De Gruyter

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