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Relation of Parkinson's Disease Subtypes to Visual Activities of Daily Living

Published online by Cambridge University Press:  04 August 2011

Daniel R. Seichepine
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts
Sandy Neargarder
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts Department of Psychology, Bridgewater State University, Bridgewater, Massachusetts
Ivy N. Miller
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts
Tatiana M. Riedel
Affiliation:
Mandel School of Applied Social Sciences, Case Western Reserve University, Cleveland, Ohio
Grover C. Gilmore
Affiliation:
Mandel School of Applied Social Sciences, Case Western Reserve University, Cleveland, Ohio
Alice Cronin-Golomb*
Affiliation:
Department of Psychology, Boston University, Boston, Massachusetts
*
Correspondence and reprint requests to: Alice Cronin-Golomb, Department of Psychology, Boston University, 648 Beacon Street, 2nd floor, Boston, MA 02215. E-mail: alicecg@bu.edu

Abstract

Visual perceptual problems are common in Parkinson's disease (PD) and often affect activities of daily living (ADLs). PD patients with non-tremor symptoms at disease onset (i.e., rigidity, bradykinesia, gait disturbance or postural instability) have more diffuse neurobiological abnormalities and report worse non-motor symptoms and functional changes than patients whose initial symptom is tremor, but the relation of motor symptom subtype to perceptual deficits remains unstudied. We assessed visual ADLs with the Visual Activities Questionnaire in 25 non-demented patients with PD, 13 with tremor as the initial symptom and 12 with an initial symptom other than tremor, as well as in 23 healthy control participants (NC). As expected, the non-tremor patients, but not the tremor patients, reported more impairment in visual ADLs than the NC group, including in light/dark adaptation, acuity/spatial vision, depth perception, peripheral vision and visual processing speed. Non-tremor patients were significantly worse than tremor patients overall and on light/dark adaptation and depth perception. Environmental enhancements especially targeted to patients with the non-tremor PD subtype may help to ameliorate their functional disability. (JINS, 2011, 17, 841–852)

Type
Regular Articles
Copyright
Copyright © The International Neuropsychological Society 2011

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References

Allcock, L.M., Kenny, R.A., Burn, D.J. (2006). Clinical phenotype of subjects with Parkinson's disease and orthostatic hypotension: Autonomic symptom and demographic comparison. Movement Disorders, 21(11), 18511855. doi:10.1002/mds.20996CrossRefGoogle ScholarPubMed
Altgassen, M., Phillips, L., Kopp, U., Kliegel, M. (2007). Role of working memory components in planning performance of individuals with Parkinson's disease. Neuropsychologia, 45(10), 23932397. doi:10.1016/j.neuropsychologia.2007.02.018CrossRefGoogle ScholarPubMed
Alves, G., Larson, J.P., Emre, M., Wentzel-Larson, T., Aarsland, D. (2006). Changes in motor subtype and risk for incident dementia in Parkinson's disease. Movement Disorders, 21(8), 11231130. doi:10.1002/mds.20897CrossRefGoogle ScholarPubMed
Amick, M.M., Grace, J., Ott, B.R. (2007). Visual and cognitive predictors of driving safety in Parkinson's disease patients. Archives of Clinical Neuropsychology, 22(8), 957967. doi:10.1016/j.acn.2007.07.004CrossRefGoogle ScholarPubMed
Amick, M.M., Cronin-Golomb, A., Gilmore, G.C. (2003). Visual processing of rapidly presented stimuli is normalized in Parkinson's disease when proximal stimulus strength is enhanced. Vision Research, 43(26), 28272835. doi:10.1016/S0042-6989(03)00476-0CrossRefGoogle ScholarPubMed
Amick, M.M., Schendan, H.E., Ganis, G., Cronin-Golomb, A. (2006). Frontostriatal Circuits are necessary for visuomotor transformation: Mental rotation in Parkinson's disease. Neuropsychologia, 44(3), 339349. doi:10.1016/j.neuropsychologia.2005.06.002CrossRefGoogle ScholarPubMed
Azulay, J.P., van den Brand, C., Mestre, D., Blin, O., Sangla, I., Pouget, J., Serratrice, G. (1996). Analyse cinématique de la marche du parkinsonien: Effets de la levodopa et de stimulations visuelles. Revue Neurologique (Paris), 152(2), 128134.Google Scholar
Azulay, J.P., Mesure, S., Amblard, B., Blin, O., Sangla, I., Pouget, J. (1999). Visual control of locomotion in Parkinson's disease. Brain, 122(1), 111120. doi:10.1093/brain/122.1.111CrossRefGoogle ScholarPubMed
Benamer, H.T., Patterson, J., Wyper, D.J., Hadley, D.M., Macphee, G.J., Grosset, D.G. (2000). Correlation of Parkinson's disease severity and duration with 123I-FP-CIT SPECT striatal uptake. Movement Disorders, 15(4), 692698. doi:10.1002/1531-8257(200007)15:4<692::AID-MDS1014>3.0.CO;2-V3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Bodis-Wollner, I., Yahr, M.D. (1978). Measurements of visual evoked potential in Parkinson's disease. Brain, 101(4), 661671. doi:10.1093/brain/101.4.661CrossRefGoogle ScholarPubMed
Bodis-Wollner, I., Marx, M.S., Mitra, S., Bobak, P., Mylin, L., Yahr, M. (1987). Visual dysfunction in Parkinson's disease. Loss in spatiotemptoral contrast sensitivity. Brain, 110(pt 6), 16751698. doi:10.1093/brain/110.6.1675CrossRefGoogle ScholarPubMed
Bodis-Wollner, I. (1990). Visual deficits related to dopamine deficiency in experimental animals and Parkinson's disease patients. Trends in Neurosciences, 13(7), 298302. doi:10.1016/0166-2236(90)90113-OCrossRefGoogle ScholarPubMed
Bodis-Wollner, I. (2009). Retinopathy in Parkinson's disease. Journal of Neural Transmission, 116(11), 14931501. doi:10.1007/s00702-009-0292-zCrossRefGoogle Scholar
Brücke, T., Asenbaum, S., Pirker, W., Djamshidian, S., Wenger, S., Wober, C., Podreka, I. (1997). Measurement of the dopaminergic degeneration in Parkinson's disease with [123I] beta-CIT and SPECT. Correlation with clinical findings and comparison with multiple system atrophy and progressive supranuclear palsy. Journal of Neural Transmission Supplementum, 50, 924.CrossRefGoogle ScholarPubMed
Buttner, T., Kuhn, W., Klotz, P., Steinber, R., Voss, L., Bulgaru, D., Przuntek, H. (1993). Disturbance of colour perception in Parkinson's disease. Journal of Neural Transmission, 6(1), 1115. doi:10.1007/BF02252618Google ScholarPubMed
Burn, D.J., Rowan, E.N., Allan, L.M., Molloy, S., O'Brien, J.T., McKeith, I.G. (2006). Motor subtypes and cognitive decline in Parkinson's disease with dementia, and dementia with Lewy bodies. Journal of Neurology, Neurosurgery, and Psychiatry, 77(5), 585589. doi:10.1136/jnnp.2005.081711CrossRefGoogle ScholarPubMed
Burn, D.J., Rowan, E.N., Minett, T., Sanders, J., Myint, P., Richardson, J., McKeith, I.G. (2003). Extrapyramidal features in Parkinson's disease with and without dementia and dementia with Lewy bodies: A cross-sectional comparative study. Movement Disorders, 18(8), 884889. doi:10.1002/mds.10455CrossRefGoogle ScholarPubMed
Chaudhuri, K.R., Schapira, A.H. (2009). Non-motor symptoms of Parkinson's disease: Dopaminergic pathophysiology and treatment. Lancet Neurology, 8(5), 464474. doi:10.1016/S1474-4422(09)70068-7CrossRefGoogle Scholar
Clark, U.S., Neargarder, S., Cronin-Golomb, A. (2008). Specific impairments in the recognition of emotional facial expression in Parkinson's disease. Neuropsychologia, 46(9), 23002309. doi:10.1016/j.neuropsychologia.2008.03.014CrossRefGoogle ScholarPubMed
Clark, U.S., Neargarder, S., Cronin-Golomb, A. (2010). Visual exploration of emotional facial expressions in Parkinson's disease. Neuropsychologia, 48, 19011913. doi:10.1016/j.neuropsychologia.2010.03.006CrossRefGoogle ScholarPubMed
Clay, O.J., Edwards, J.D., Ross, L.A., Okonkwo, O., Wadley, V.G., Roth, D.L., Ball, K.K. (2009). Visual function and cognitive speed of processing mediate age-related decline in memory span and fluid intelligence. Journal of Aging and Health, 21(4), 547566. doi:10.1177/0898264309333326CrossRefGoogle ScholarPubMed
Cronin-Golomb, A., Corkin, S., Growdon, J.H. (1995). Visual dysfunction predicts cognitive deficits in Alzheimer's disease. Optometry and Vision Science, 72(3), 168176.CrossRefGoogle ScholarPubMed
Cronin-Golomb, A., Gilmore, G.C., Neargarder, S., Morrison, S.R., Laudate, T.M. (2007). Enhanced stimulus strength improves visual cognition in aging and Alzheimer's disease. Cortex, 43(7), 952966.CrossRefGoogle ScholarPubMed
Cronin-Golomb, A. (2010). Parkinson's disease as a disconnection syndrome. Neuropsychology Review, 20(2), 191208. doi:10.1007/s11065-010-9128-8CrossRefGoogle ScholarPubMed
Davidsdottir, S., Cronin-Golomb, A., Lee, A.C. (2005). Visual and spatial symptoms in Parkinson's disease. Vision Research, 45(10), 12851296. doi:10.1016/j.visres.2004.11.006CrossRefGoogle ScholarPubMed
Davidsdottir, S., Wagenaar, R., Young, D., Cronin-Golomb, A. (2008). Visuospatial function, optic flow perception, and navigational veering in Parkinson's disease. Brain, 131, 28822893.CrossRefGoogle ScholarPubMed
Devos, H., Vandenberghe, W., Nieuwboer, A., Tant, M., Baten, G., De Weerdt, W. (2007). Predictors of fitness to drive in people with Parkinson disease. Neurology, 69(14), 14341441. doi:10.1212/01.wnl.0000277640.58685.fcCrossRefGoogle ScholarPubMed
Diederich, N.J., Raman, R., Leurgans, S., Goetz, C.G. (2002). Progressive worsening of spatial and chromatic processing deficits in Parkinson disease. Archives of Neurology, 59(8), 12491252.CrossRefGoogle ScholarPubMed
Hariz, G.M., Forsgren, L. (2011). Activities of daily living and quality of life in persons with newly diagnosed Parkinson's disease according to subtype of disease, and in comparison to healthy controls. Acta Neurologica Scandinavica, 123(1), 2027. doi:10.1111/j.1600-0404.2010.01344.xCrossRefGoogle ScholarPubMed
Hoehn, M.M., Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427442.CrossRefGoogle ScholarPubMed
Kemps, E., Szmalec, A., Vandierendonck, A., Crevits, L. (2005). Visuo-spatial processing in Parkinson's disease: Evidence for diminished visuo-spatial sketch pad and central executive resources. Parkinsonism and Related Disorders, 11(3), 181186. doi:10.1016/j.parkreldis.2004.10.010CrossRefGoogle ScholarPubMed
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. European Journal of Neurology, 15(2), 128133. doi:10.1111/j.1468-1331.2007.02011.xCrossRefGoogle ScholarPubMed
Kupersmith, M.J., Shakin, E., Siegel, I.M., Lieberman, A. (1982). Visual system abnormalities in patients with Parkinson's disease. Archives of Neurology, 39(5), 284286.CrossRefGoogle ScholarPubMed
Lee, A.C., Harris, J.P., Calvert, J.E. (1998). Impairments of mental rotation in Parkinson's disease. Neuropsychologia, 36(1), 109114.CrossRefGoogle ScholarPubMed
Lee, A., Harris, J. (1999). Problems with perception of space in Parkinson's disease: A questionnaire study. Neuroopthalmology, 22(1), 115.CrossRefGoogle Scholar
Lewis, S.J., Foltynie, T., Blackwell, A.D., Robbins, T.W., Owen, A.M., Barker, R.A. (2005). Heterogeneity of Parkinson's disease in the early clinical stages using a data driven approach. Journal of Neurology, Neurosurgery, and Psychiatry, 76(3), 343348. doi:10.1136/jnnp.2003.033530CrossRefGoogle ScholarPubMed
Lyros, E., Messinis, L., Papathanasopoulos, P. (2008). Does motor subtype influence neurocognitive performance in Parkinson's disease without dementia? European Journal of Neurology, 15(3), 262267. doi:10.1111/j.1468-1331.2007.02046.xCrossRefGoogle ScholarPubMed
Maeshima, S., Itakura, T., Nakagawa, M., Nakai, K., Komai, N. (1997). Visuospatial impairment and activities of daily living in patients with Parkinson's disease: a quantitative assessment of the cube-copying task. American Journal of Physical Medicine & Rehabilitation, 76(5), 383388.CrossRefGoogle ScholarPubMed
McDowell, S.A., Harris, J. (1997a). Visual problems in Parkinson's disease: A questionnaire survey. Behavioral Neurology, 10, 7781.CrossRefGoogle ScholarPubMed
McDowell, S.A., Harris, J. (1997b). Irrelevant peripheral vision stimuli impair manual reaction times in Parkinson's disease. Vision Research, 37(24), 35493558. doi:10.1016/S0042-6989(97)00188-0CrossRefGoogle ScholarPubMed
Micieli, G., Tassorelli, C., Martignoni, E., Pacchetti, C., Bruggi, P., Magri, M., et al. (1991). Disordered pupil reactivity in Parkinson's disease. Clinical autonomic research: official journal of the Clinical Autonomic Research Society, 1(1), 5558.CrossRefGoogle ScholarPubMed
Montse, A., Pere, V., Carme, J., Francesc, V., Eduardo, T. (2001). Visuospatial deficits in Parkinson's disease assessed by line orientation test: Error analyses and practice effects. Journal of Clinical and Experimental Neuropsychology, 23(5), 592598. doi:10.1076/jcen.23.5.592.1248CrossRefGoogle ScholarPubMed
Oh, J.Y., Kim, Y.S., Choi, B.H., Sohn, E.H., Lee, A.Y. (2009). Relationship between clinical phenotypes and cognitive impairment in Parkinson's disease (PD). Archives of Gerontology and Geriatrics, 49(3), 351354.CrossRefGoogle ScholarPubMed
Owsley, C. (2010). Aging and vision. Vision Research, [Epub ahead of print].Google ScholarPubMed
Pandya, M., Kubu, C.S., Giroux, M.L. (2008). Parkinson disease: Not just a movement disorder. Cleveland Clinic Journal of Medicine, 75(12), 856864. doi:10.3949/ccjm.75a.07005CrossRefGoogle ScholarPubMed
Pieri, V., Diederich, N.J., Raman, R., Goetz, C.G. (2000). Decreased color discrimination and contrast sensitivity in Parkinson's disease. Journal of Neurological Sciences, 172(1), 711. doi:10.1016/S0022-510X(99)00204-XCrossRefGoogle ScholarPubMed
Poewe, W. (2008). Non-motor symptoms in Parkinson's disease. European Journal of Neurology, 15(Suppl. 1), 1420. doi:10.1111/j.1468-1331.2008.02056.xCrossRefGoogle ScholarPubMed
Possin, K.L., Filoteo, J.V., Song, D.D., Salmon, D.P. (2008). Spatial and object working memory deficits in Parkinson's disease are due to impairment in different underlying processes. Neuropsychology, 22(5), 585595. doi:10.1037/a0012613CrossRefGoogle ScholarPubMed
Price, M.J., Feldman, R.G., Adelberg, D., Kayne, H. (1992). Abnormalities in color vision and contrast sensitivity in Parkinson's disease. Neurology, 42(4), 887890.CrossRefGoogle ScholarPubMed
Rajput, A.H., Sitte, H.H., Rajput, A., Fenton, M.E., Pifl, C., Hornykiewicz, O. (2008). Globus pallidus, dopamine and Parkinson motor subtypes: Clinical and brain biochemical correlation. Neurology, 70(16 Pt 2), 14031410. doi:10.1212/01.wnl.0000285082.18969.3aCrossRefGoogle ScholarPubMed
Rajput, A.H., Voll, A., Rajput, M.L., Robinson, C.A., Rajput, A. (2009). Course of Parkinson disease subtypes: A 39-year clinicopathologic study. Neurology, 73(3), 206212. doi:10.1212/WNL.0b013e3181ae7af1CrossRefGoogle ScholarPubMed
Regan, D., Neima, D. (1984). Low-contrast letter charts in early diabetic Retinopathy, ocular hypertension, glaucoma, and Parkinson's disease. The British Journal of Ophthalmology, 68(12), 885889. doi:10.1136/bjo.68.12.885CrossRefGoogle ScholarPubMed
Regan, D., Maxner, C. (1987). Orientation-selective visual loss in patients with Parkinson's disease. Brain, 110(Pt 2), 415432. doi:10.1093/brain/110.2.415CrossRefGoogle ScholarPubMed
Reijnders, J.S., Ehrt, U., Lousberg, R., Aarsland, D., Leentjens, A.F. (2009). The association between motor subtypes and psychopathology in Parkinson's disease. Parkinsonism and Related Disorders, 15(5), 379382. doi:10.1016/j.parkreldis.2008.09.003CrossRefGoogle ScholarPubMed
Rudzinska, M., Marona, M., Bukowczan, S., Banaszkiewicz, K., Mirek, E., Szczudlik, A. (2007). Falls in different types of Parkinson's disease. Neurologia I Neurochirurgia Polska, 41(5), 395403.Google ScholarPubMed
Schendan, H.E., Amick, M.M., Cronin-Golomb, A. (2009). Role of lateralized parietal-basal ganglia circuit in hierarchical pattern perception: Evidence from Parkinson's disease. Behavioral Neuroscience, 123(1), 125136. doi:10.1037/a0013734CrossRefGoogle ScholarPubMed
Selikhova, M., Williams, D.R., Kempster, P.A., Holton, J.L., Lees, A.J. (2009). A clinic-pathological study of subtype in Parkinson's disease. Brain, 132(11), 29472957. doi:10.1093/brain/awp234CrossRefGoogle Scholar
Seibyl, J.P., Marek, K.L., Quinlan, D., Sheff, K., Zoghbi, S., Zea-Ponce, Y., van Dyck, C. (1995). Decreased single-photon emission computed tomographic [123]beta-CIT striatal uptake correlates with symptom severity in Parkinson's disease. Annals of Neurology, 38(4), 589598. doi:10.1002/ana.410380407CrossRefGoogle ScholarPubMed
Shinotoh, H., Uchida, Y., Ito, H., Harrori, T. (2000). Relationship between striatal [123]beta-CIT binding and four major clinical signs in Parkinson's disease. Annals of Nuclear Medicine, 14(3), 199203.CrossRefGoogle ScholarPubMed
Shulman, L.M., Taback, R.L., Bean, J., Weiner, W.J. (2001). Comorbidity of the nonmotor symptoms of Parkinson's disease. Movement Disorders, 16(3), 507510. doi:10.1002/mds.1099CrossRefGoogle ScholarPubMed
Silkis, I.G. (2007a). The contribution of synaptic plasticity in the basal ganglia to the processing of visual information. Neuroscience and Behavioral Physiology, 37(8), 779790. doi:10.1007/s11055-007-0082-8CrossRefGoogle Scholar
Silkis, I.G. (2007b). A hypothetical role of cortico-basal ganglia-thalamocortical loops in visual processing. Biosystems, 89, 227235. doi:10.1016/j.biosystems.2006.04.020CrossRefGoogle ScholarPubMed
Sloane, M.E., Ball, K., Owsley, C., Bruni, J.R., Roenker, D.L. (1992). The Visual Activities Questionnaire: Developing an instrument for assessing problems in everyday visual tasks. Technical Digest, Noninvasive Assessment of the Visual System, Topical Meeting of the Optical Society of America, January, 1992.CrossRefGoogle Scholar
Spiegel, J., Hellwig, D., Samnick, S., Jost, W., Möllers, M.O., & Fassbender, K., Dillmann, U. (2007). Striatal FP-CIT uptake differs in the subtypes of early Parkinson's disease. Journal of Neural Transmission, 114(3), 331335. doi:10.1007/s00702-006-0518-2CrossRefGoogle ScholarPubMed
Siegert, R.J., Weatherall, M., Taylor, K.D., Abernethy, D.A. (2008). A meta-analysis of performance on a simple span and more complex working memory tasks in Parkinson's disease. Neuropsychology, 22(4), 450461. doi:10.1037/0894-4105.22.4.450CrossRefGoogle ScholarPubMed
Taylor, J.P., Rowan, E.N., Lett, D., O'Brien, J.T., McKeith, I.G., Burn, D.J. (2008). Poor attentional function predicts cognitive decline in patients with non-demented Parkinson's disease independent of motor phenotype. Journal of Neurology, Neurosurgery, and Psychiatry, 79(12), 13181323. doi:10.1136/jnnp.2008.147629CrossRefGoogle ScholarPubMed
Uc, E.Y., Rizzo, M., Anderson, S.W., Dastrup, E., Sparks, J.D., Dawson, J.D. (2009). Driving under low-contrast visibility condition in Parkinson's disease. Neurology, 73(14), 11031110. doi:10.1212/WNL.0b013e3181bacf6eCrossRefGoogle Scholar
Uc, E.Y., Rizzo, M., Johnson, A.M., Dastrup, E., Anderson, S.W., Dawson, J.D. (2009). Road safety in drivers with Parkinson's disease. Neurology, 15(24), 21122119. doi:10.1212/WNL.0b013e3181c67b77CrossRefGoogle Scholar
Uc, E.Y., Rizzo, M., Anderson, S.W., Sparks, J.D., Rodnitzky, R.L., Dawson, J.D. (2007). Impaired navigation in drivers with Parkinson's disease. Brain, 130(Pt 9), 24332440. doi:10.1093/brain/awm178CrossRefGoogle ScholarPubMed
Vakil, E., Herishanu-Naaman, S. (1998). Declarative and procedural learning in Parkinson's disease patients having tremor or bradykinesia as the predominant symptom. Cortex, 34(4), 611620. doi:10.1016/S0010-9452(08)70518-5CrossRefGoogle ScholarPubMed
Verbaan, D., Marinus, J., Visser, M., van Rooden, S.M., Stiggelbout, A.M., Middelkoop, H.A., et al. (2007). Cognitive impairment in Parkinson's disease. Journal of neurology, neurosurgery, and psychiatry, 78(11), 11821187.CrossRefGoogle ScholarPubMed
Williams, L.N., Seignourel, P., Crucian, G.P, Okun, M.S., Rodriguez, R.L., Skidmore, F.M., et al. (2007). Laterality, region, and type of motor dysfunction correlate with cognitive impairment in Parkinson's disease. Movement Disorders, 22(1), 141145.CrossRefGoogle ScholarPubMed
Williams-Gray, C.H., Foltynie, T., Brayne, C.E., Robbins, T.W., Barker, R.A. (2007). Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. Brain, 130(Pt 7), 17871798.CrossRefGoogle Scholar
Witjas, T., Kaphan, E., Azulay, J.P., Blin, O., Ceccaldi, M., Pouget, J., Chériff, A.A. (2002). Nonmotor fluctuations in Parkinson's disease: Frequent and disabling. Neurology, 59(3), 408413.CrossRefGoogle ScholarPubMed
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Opthalmologica, 108, 1740. doi:10.1023/B:DOOP.0000019487.88486.0aCrossRefGoogle ScholarPubMed
Worringham, C.J., Wood, J.M., Kerr, G.K., Silburn, P.A. (2006). Predictors of driving assessment outcome in Parkinson's disease. Movement Disorders, 21(2), 230235. doi:10.1002/mds.20709CrossRefGoogle ScholarPubMed
Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M. et al. (1982). Development and validation of a geriatric depression screening scale: a preliminary report. Journal of Psychiatric Research, 17(1), 3749.CrossRefGoogle Scholar
Zaidel, A., Arkadir, D., Israel, Z., Bergman, H. (2009). Akineto-rigid vs. tremor syndromes in Parkinsonism. Current Opinion in Neurology, 22(4), 387393. doi:10.1097/WCO.0b013e32832d9d67CrossRefGoogle ScholarPubMed
Zetusky, W.J., Jankovic, J. (1985). Laterality and symptom association in Parkinson's disease. Archives of Neurology, 42(12), 11321133.CrossRefGoogle ScholarPubMed