Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-18T11:05:16.420Z Has data issue: false hasContentIssue false
  • English
  • Français

Paradoxical Effect of Dopamine Medication on Cognition in Parkinson’s Disease: Relationship to Side of Motor Onset

Published online by Cambridge University Press:  29 April 2015

Brenda Hanna-Pladdy ,
Rajesh Pahwa  and
Kelly E. Lyons
Brenda Hanna-Pladdy*
Affiliation:
Departments of Neurology, Psychiatry, and Diagnostic Radiology and Nuclear Medicine, University of Maryland School of Medicine, Baltimore, Maryland
Rajesh Pahwa
Affiliation:
Parkinson’s Disease and Movement Disorder Center, Department of Neurology, University of Kansas Medical Center, Kansas City, Kansas
Kelly E. Lyons
Affiliation:
Parkinson’s Disease and Movement Disorder Center, Department of Neurology, University of Kansas Medical Center, Kansas City, Kansas
*
Correspondence and reprint requests to: Brenda Hanna-Pladdy, Department of Neurology, University of Maryland School of Medicine, 110 South Paca Street 3rd Floor, Baltimore, MD 21201. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Parkinson’s disease (PD) is characterized by asymmetric motor symptom onset attributed to greater degeneration of dopamine neurons contralateral to the affected side. However, whether motor asymmetries predict cognitive profiles in PD, and to what extent dopamine influences cognition remains controversial. This study evaluated cognitive variability in PD by measuring differential response to dopamine replacement therapy (DRT) based on hemispheric asymmetries. The influence of DRT on cognition was evaluated in mild PD patients (n=36) with left or right motor onset symptoms. All subjects were evaluated on neuropsychological measures on and off DRT and compared to controls (n=42). PD patients were impaired in executive, memory and motor domains irrespective of side of motor onset, although patients with left hemisphere deficit displayed greater cognitive impairment. Patients with right hemisphere deficit responded to DRT with significant improvement in sensorimotor deficits, and with corresponding improvement in attention and verbal memory functions. Conversely, patients with greater left hemisphere dopamine deficiency did not improve in attentional functions and declined in verbal memory recall following DRT. These findings support the presence of extensive mild cognitive deficits in early PD not fully explained by dopamine depletion alone. The paradoxical effects of levodopa on verbal memory were predicted by extent of fine motor impairment and sensorimotor response to levodopa, which reflects extent of dopamine depletion. The findings are discussed with respect to factors influencing variable cognitive profiles in early PD, including hemispheric asymmetries and differential response to levodopa based on dopamine levels predicting amelioration or overdosing. (JINS, 2015, 21, 259–270)

Keywords

CognitionDopamineMemoryMotor asymmetryParkinson’s disease
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 21 , Issue 4 , April 2015 , pp. 259 - 270
Copyright
Copyright © The International Neuropsychological Society 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aarsland, D., Bronnick, K., & Fladby, T. (2011). Mild cognitive impairment in Parkinson’s disease. Current Neurology and Neuroscience Reports, 11(4), 371–378. doi: 10.1007/s11910-011-0203-1 Google Scholar
Amick, M.M., Grace, J., & Chou, K.L. (2006). Body side of motor symptom onset in Parkinson’s disease is associated with memory performance. Journal of the International Neuropsychological Society, 12(5), 736–740. doi: S1355617706060875 [pii] 10.1017/S1355617706060875 Google Scholar
Beato, R., Levy, R., Pillon, B., Vidal, C., du Montcel, S.T., Deweer, B., & Cardoso, F. (2008). Working memory in Parkinson’s disease patients: Clinical features and response to levodopa. Arquivos de Neuro-Psiquiatria, 66(2A), 147–151. doi: S0004-282X2008000200001 [pii]Google Scholar
Beck, A.T., Epstein, N., Brown, G., & Steer, R.A. (1988). An inventory for measuring clinical anxiety: Psychometric properties. Journal of Consulting and Clinical Psychology, 56(6), 893–897.Google Scholar
Bentin, S., Silverberg, R., & Gordon, H.W. (1981). Asymmetrical cognitive deterioration in demented and Parkinson patients. Cortex, 17(4), 533–543.Google Scholar
Beyer, M.K., Janvin, C.C., Larsen, J.P., & Aarsland, D. (2007). A magnetic resonance imaging study of patients with Parkinson’s disease with mild cognitive impairment and dementia using voxel-based morphometry. Journal of Neurology, Neurosurgery, and Psychiatry, 78(3), 254–259. doi: jnnp.2006.093849 [pii] 10.1136/jnnp.2006.093849 Google Scholar
Blonder, L.X., Slevin, J.T., Kryscio, R.J., Martin, C.A., Andersen, A.H., Smith, C.D., & Schmitt, F.A. (2013). Dopaminergic modulation of memory and affective processing in Parkinson depression. Psychiatry Research, 210(1), 146–149. doi: 0.1016/j.psychres.2013.06.003 Google Scholar
Bohnen, N.I., Kuwabara, H., Constantine, G.M., Mathis, C.A., & Moore, R.Y. (2007). Grooved pegboard test as a biomarker of nigrostriatal denervation in Parkinson’s disease. Neuroscience Letters, 424(3), 185–189. doi: S0304-3940(07)00830-0 [pii] 10.1016/j.neulet.2007.07.035 Google Scholar
Bohnen, N.I., Studenski, S.A., Constantine, G.M., & Moore, R.Y. (2008). Diagnostic performance of clinical motor and non-motor tests of Parkinson disease: A matched case-control study. European Journal of Neurology, 15(7), 685–691. doi: 10.1111/j.1468-1331.2008.02148.x ENE2148 [pii]Google Scholar
Braak, H., Del Tredici, K., Rub, U., de Vos, R.A., Jansen Steur, E.N., & Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiology of Aging, 24(2), 197–211. doi: S0197458002000659 [pii]CrossRefGoogle ScholarPubMed
Brusa, L., Tiraboschi, P., Koch, G., Peppe, A., Pierantozzi, M., Ruggieri, S., & Stanzione, P. (2005). Pergolide effect on cognitive functions in early-mild Parkinson’s disease. Journal of Neural Transmission, 112(2), 231–237. doi: 10.1007/s00702-004-0193-0 Google Scholar
Buongiorno, M., Compta, Y., & Marti, M.J. (2011). Amyloid-beta and tau biomarkers in Parkinson’s disease-dementia. Journal of Neurological Sciences, 310(1-2), 25–30. doi: 10.1016/j.jns.2011.06.046 S0022-510X(11)00381-9 [pii]Google Scholar
Cools, R. (2006). Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson’s disease. Neuroscience and Biobehavioral Reviews, 30(1), 1–23. doi: S0149-7634(05)00054-0 [pii] 10.1016/j.neubiorev.2005.03.024 Google Scholar
Cools, R., Barker, R.A., Sahakian, B.J., & Robbins, T.W. (2001). Enhanced or impaired cognitive function in Parkinson’s disease as a function of dopaminergic medication and task demands. Cerebral Cortex, 11(12), 1136–1143.CrossRefGoogle ScholarPubMed
Cools, R., Barker, R.A., Sahakian, B.J., & Robbins, T.W. (2003). L-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease. Neuropsychologia, 41(11), 1431–1441. doi: S0028393203001179 [pii]Google Scholar
Cools, R., Stefanova, E., Barker, R.A., Robbins, T.W., & Owen, A.M. (2002). Dopaminergic modulation of high-level cognition in Parkinson’s disease: The role of the prefrontal cortex revealed by PET. Brain, 125(Pt 3), 584–594.Google Scholar
Costa, A., Peppe, A., Dell’Agnello, G., Carlesimo, G.A., Murri, L., Bonuccelli, U., & Caltagirone, C. (2003). Dopaminergic modulation of visual-spatial working memory in Parkinson’s disease. Dementia and Geriatric Cognitive Disorders, 15(2), 55–66. doi: 10.1159/000067968 67968 [pii]Google Scholar
Cropley, V.L., Fujita, M., Bara-Jimenez, W., Brown, A.K., Zhang, X.Y., Sangare, J., & Innis, R.B. (2008). Pre- and post-synaptic dopamine imaging and its relation with frontostriatal cognitive function in Parkinson disease: PET studies with [11C]NNC 112 and [18F]FDOPA. Psychiatry Research, 163(2), 171–182. doi: S0925-4927(07)00230-2 [pii] 10.1016/j.pscychresns.2007.11.003 Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Holdnack, J. (2004). Reliability and validity of the Delis-Kaplan Executive Function System: An update. Journal of the International Neuropsychological Society, 10(2), 301–303. doi: 10.1017/S1355617704102191 S1355617704102191 [pii]Google Scholar
Djaldetti, R., Ziv, I., & Melamed, E. (2006). The mystery of motor asymmetry in Parkinson’s disease. Lancet Neurology, 5(9), 796–802. doi: S1474-4422(06)70549-X [pii] 10.1016/S1474-4422(06)70549-X Google Scholar
Drag, L.L., Bieliauskas, L.A., Kaszniak, A.W., Bohnen, N.I., & Glisky, E.L. (2009). Source memory and frontal functioning in Parkinson’s disease. Journal of the International Neuropsychological Society, 15(3), 399–406. doi: 10.1017/S1355617709090572 Google Scholar
Edelstyn, N.M., Shepherd, T.A., Mayes, A.R., Sherman, S.M., & Ellis, S.J. (2010). Effect of disease severity and dopaminergic medication on recollection and familiarity in patients with idiopathic nondementing Parkinson’s. Neuropsychologia, 48(5), 1367–1375. doi: 10.1016/j.neuropsychologia.2009.12.039 Google Scholar
Fera, F., Nicoletti, G., Cerasa, A., Romeo, N., Gallo, O., Gioia, M.C., & Quattrone, A. (2007). Dopaminergic modulation of cognitive interference after pharmacological washout in Parkinson’s disease. Brain Research Bulletin, 74(1-3), 75–83. doi: S0361-9230(07)00159-1 [pii] 10.1016/j.brainresbull.2007.05.009 Google Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.Google Scholar
Fournet, N., Moreaud, O., Roulin, J.L., Naegele, B., & Pellat, J. (2000). Working memory functioning in medicated Parkinson’s disease patients and the effect of withdrawal of dopaminergic medication. Neuropsychology, 14(2), 247–253.Google Scholar
Glick, S.D., Ross, D.A., & Hough, L.B. (1982). Lateral asymmetry of neurotransmitters in human brain. Brain Research, 234(1), 53–63. doi: 0006-8993(82)90472-3 [pii]Google Scholar
Golden, C. (1978). Stroop color and word test. Illinois: Stoelting Company.Google Scholar
Gomperts, S.N., Locascio, J.J., Rentz, D., Santarlasci, A., Marquie, M., Johnson, K.A., & Growdon, J.H. (2013). Amyloid is linked to cognitive decline in patients with Parkinson disease without dementia. Neurology, 80(1), 85–91. doi:.1212/WNL.0b013e31827b1a07 WNL.0b013e31827b1a07 [pii]Google Scholar
Gotham, A.M., Brown, R.G., & Marsden, C.D. (1986). Levodopa treatment may benefit or impair “frontal” function in Parkinson’s disease. Lancet, 2(8513), 970–971. doi: S0140-6736(86)90617-3 [pii]Google Scholar
Gotham, A.M., Brown, R.G., & Marsden, C.D. (1988). ‘Frontal’ cognitive function in patients with Parkinson’s disease ‘on’ and ‘off’ levodopa. Brain, 111(Pt 2), 299–321.Google Scholar
Haaxma, C.A., Helmich, R.C., Borm, G.F., Kappelle, A.C., Horstink, M.W., & Bloem, B.R. (2010). Side of symptom onset affects motor dysfunction in Parkinson’s disease. Neuroscience, 170(4), 1282–1285. doi: S0306-4522(10)01010-9 [pii] 0.1016/j.neuroscience.2010.07.030 Google Scholar
Halbig, T.D., Kopp, U.A., Wodarz, F., Borod, J.C., Gracies, J.M., Ebersbach, G., & Kupsch, A. (2008). Dopaminergic modulation of emotional memory in Parkinson’s disease. Journal of Neural Transmission, 115(8), 1159–1163. doi: 10.1007/s00702-008-0061-4 Google Scholar
Hanna-Pladdy, B., & Heilman, K.M. (2010). Dopaminergic modulation of the planning phase of skill acquisition in Parkinson’s disease. Neurocase, 16(2), 182–190. doi: 917524285 [pii] 10.1080/13554790903379609 Google Scholar
Hanna-Pladdy, B., Jones, K., Cabanban, R., Pahwa, R., & Lyons, K.E. (2013). Predictors of mild cognitive impairment in early-stage Parkinson’s disease. Dementia and Geriatric Cognitive Disorders Extra, 3(1), 168–178. doi: 10.1159/000351421dee-0003-0168 [pii]Google Scholar
Ibarretxe-Bilbao, N., Junque, C., Marti, M.J., & Tolosa, E. (2011). Brain structural MRI correlates of cognitive dysfunctions in Parkinson’s disease. Journal of Neurological Sciences, 310(1-2), 70–74. doi: 10.1016/j.jns.2011.07.054 S0022-510X(11)00476-X [pii]Google Scholar
Jahanshahi, M., Wilkinson, L., Gahir, H., Dharmarinda, A., & Lagnado, D.A. (2010). Medication impairs probabilistic classification learning in Parkinson’s disease. Neuropsychologia, 48(4), 1096–1103. doi: S0028-3932(09)00486-2 [pii] 10.1016/j.neuropsychologia.2009.12.010 Google Scholar
Jokinen, P., Bruck, A., Aalto, S., Forsback, S., Parkkola, R., & Rinne, J.O. (2009). Impaired cognitive performance in Parkinson’s disease is related to caudate dopaminergic hypofunction and hippocampal atrophy. Parkinsonism and Related Disorders, 15(2), 88–93. doi: S1353-8020(08)00102-8 [pii] 10.1016/j.parkreldis.2008.03.005 Google Scholar
Jubault, T., Monetta, L., Strafella, A.P., Lafontaine, A.L., & Monchi, O. (2009). L-dopa medication in Parkinson’s disease restores activity in the motor cortico-striatal loop but does not modify the cognitive network. PLoS One, 4(7), e6154. doi: 10.1371/journal.pone.0006154 Google Scholar
Kang, U.J., & Auinger, P. (2012). Activity enhances dopaminergic long-duration response in Parkinson disease. Neurology, 78(15), 1146–1149. doi: 10.1212/WNL.0b013e31824f8056 WNL.0b013e31824f8056 [pii]Google Scholar
Katzen, H.L., Levin, B.E., & Weiner, W. (2006). Side and type of motor symptom influence cognition in Parkinson’s disease. Movement Disorders, 21(11), 1947–1953. doi: 10.1002/mds.21105 Google Scholar
Kelly, C., de Zubicaray, G., Di Martino, A., Copland, D.A., Reiss, P.T., Klein, D.F., & McMahon, K. (2009). L-dopa modulates functional connectivity in striatal cognitive and motor networks: A double-blind placebo-controlled study. Journal of Neuroscience, 29(22), 7364–7378. doi: 29/22/7364 [pii] 10.1523/JNEUROSCI.0810-09.2009 Google Scholar
Kish, S.J., Shannak, K., & Hornykiewicz, O. (1988). Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. Pathophysiologic and clinical implications. New England Journal of Medicine, 318(14), 876–880. doi: 0.1056/NEJM198804073181402 Google Scholar
Lange, K.W., Robbins, T.W., Marsden, C.D., James, M., Owen, A.M., & Paul, G.M. (1992). L-dopa withdrawal in Parkinson’s disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction. Psychopharmacology, 107(2-3), 394–404.Google Scholar
Luciana, M., Collins, P.F., & Depue, R.A. (1998). Opposing roles for dopamine and serotonin in the modulation of human spatial working memory functions. Cerebral Cortex, 8(3), 218–226.Google Scholar
MacDonald, A.A., Seergobin, K.N., Owen, A.M., Tamjeedi, R., Monchi, O., Ganjavi, H., & MacDonald, P.A. (2013). Differential effects of Parkinson’s disease and dopamine replacement on memory encoding and retrieval. PLoS One, 8(9), e74044. doi: 10.1371/journal.pone.0074044 Google Scholar
Macdonald, P.A., & Monchi, O. (2011). Differential effects of dopaminergic therapies on dorsal and ventral striatum in Parkinson’s disease: Implications for cognitive function. Parkinson’s Disease, 2011, 572743. doi: 10.4061/2011/572743 Google Scholar
McClure, S.M., Laibson, D.I., Loewenstein, G., & Cohen, J.D. (2004). Separate neural systems value immediate and delayed monetary rewards. Science, 306(5695), 503–507. doi: 306/5695/503 [pii] 10.1126/science.1100907 Google Scholar
Melamed, E., & Poewe, W. (2012). Taking sides: Is handedness involved in motor asymmetry of Parkinson’s disease? Movement Disorders, 27(2), 171–173. doi: 10.1002/mds.24048 Google Scholar
Mesulam, M.M., Weintraub, S., Rogalski, E.J., Wieneke, C., Geula, C., & Bigio, E.H. (2014). Asymmetry and heterogeneity of Alzheimer’s and frontotemporal pathology in primary progressive aphasia. Brain, 137(Pt 4), 1176–1192. doi: 10.1093/brain/awu024 Google Scholar
Middleton, F.A., & Strick, P.L. (2000a). Basal ganglia and cerebellar loops: Motor and cognitive circuits. Brain Research Reviews, 31(2-3), 236–250.Google Scholar
Middleton, F.A., & Strick, P.L. (2000b). Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. Brain and Cognition, 42(2), 183–200.Google Scholar
Nagano-Saito, A., Leyton, M., Monchi, O., Goldberg, Y.K., He, Y., & Dagher, A. (2008). Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. Journal of Neuroscience, 28(14), 3697–3706. doi: 28/14/3697 [pii] 10.1523/JNEUROSCI.3921-07.2008 Google Scholar
Nutt, J.G., Carter, J.H., & Woodward, W.R. (1995). Long-duration response to levodopa. Neurology, 45(8), 1613–1616.Google Scholar
O’Carroll, C.M., Martin, S.J., Sandin, J., Frenguelli, B., & Morris, R.G. (2006). Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learning and Memory, 13(6), 760–769. doi: 10.1101/lm.321006 Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113.Google Scholar
Pezze, M., & Bast, T. (2012). Dopaminergic modulation of hippocampus-dependent learning: Blockade of hippocampal D1-class receptors during learning impairs 1-trial place memory at a 30-min retention delay. Neuropharmacology, 63(4), 710–718. doi: 10.1016/j.neuropharm.2012.05.036 Google Scholar
Poletti, M., Frosini, D., Pagni, C., Baldacci, F., Giuntini, M., Mazzucchi, S., &Bonuccelli, U. (2013). The relationship between motor symptom lateralization and cognitive performance in newly diagnosed drug-naive patients with Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 35(2), 124–131. doi: 10.1080/13803395.2012.751966 Google Scholar
Poletti, M., Frosini, D., Pagni, C., Baldacci, F., Nicoletti, V., Tognoni, G., & Bonuccelli, U. (2012). Mild cognitive impairment and cognitive-motor relationships in newly diagnosed drug-naive patients with Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 83(6), 601–606. doi: 10.1136/jnnp-2011-301874 jnnp-2011-301874 [pii]Google Scholar
Randolph, C., Tierney, M.C., Mohr, E., & Chase, T.N. (1998). The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): Preliminary clinical validity. Journal of Clinical and Experimental Neuropsychology, 20(3), 310–319.Google Scholar
Reiss, J.P., Campbell, D.W., Leslie, W.D., Paulus, M.P., Stroman, P.W., Polimeni, J.O., & Sareen, J. (2005). The role of the striatum in implicit learning: A functional magnetic resonance imaging study. Neuroreport, 16(12), 1291–1295. doi: 00001756-200508220-00008 [pii]Google Scholar
Reitan, R.M., & Wolfson, D. (1993). Halstead-Reitan Neuropsychological Battery. Tuscon, AZ: Neuropsychology Press.Google Scholar
Riederer, P., & Sian-Hulsmann, J. (2012). The significance of neuronal lateralisation in Parkinson’s disease. Journal of Neural Transmission, 119, 953–962. doi: 10.1007/s00702-012-0775-1 Google Scholar
Sawamoto, N., Piccini, P., Hotton, G., Pavese, N., Thielemans, K., & Brooks, D.J. (2008). Cognitive deficits and striato-frontal dopamine release in Parkinson’s disease. Brain, 131(Pt 5), 1294–1302. doi: awn054 [pii] 10.1093/brain/awn054 Google Scholar
Scherfler, C., Seppi, K., Mair, K.J., Donnemiller, E., Virgolini, I., Wenning, G.K., & Poewe, W. (2012). Left hemispheric predominance of nigrostriatal dysfunction in Parkinson’s disease. Brain, 135(Pt 11), 3348–3354. doi: 10.1093/brain/aws253 aws253 [pii]Google Scholar
Schicknick, H., Schott, B.H., Budinger, E., Smalla, K.H., Riedel, A., Seidenbecher, C.I., & Tischmeyer, W. (2008). Dopaminergic modulation of auditory cortex-dependent memory consolidation through mTOR. Cerebral Cortex, 18(11), 2646–2658. doi: 0.1093/cercor/bhn026 Google Scholar
Seo, M., Beigi, M., Jahanshahi, M., & Averbeck, B.B. (2010). Effects of dopamine medication on sequence learning with stochastic feedback in Parkinson’s disease. Frontiers in Human Neuroscience, 4, doi: 36 [pii] 10.3389/fnsys.2010.00036 Google Scholar
Shohamy, D., Myers, C.E., Geghman, K.D., Sage, J., & Gluck, M.A. (2006). L-dopa impairs learning, but spares generalization, in Parkinson’s disease. Neuropsychologia, 44(5), 774–784. doi: S0028-3932(05)00263-0 [pii] 10.1016/j.neuropsychologia.2005.07.013 Google Scholar
Shprakh, V.V., & Suvorova, I.A. (2010). [Post-stroke vascular dementia: Risk factors and clinical neuro-imaging features]. Advances in Gerontology, 23(2), 293–300.Google Scholar
Steer, R.A., Rissmiller, D.J., & Beck, A.T. (2000). Use of the Beck Depression Inventory-II with depressed geriatric inpatients. Behaviour Research Therapy, 38(3), 311–318.Google Scholar
Taylor Tavares, A.L., Jefferis, G.S., Koop, M., Hill, B.C., Hastie, T., Heit, G., & Bronte-Stewart, H.M. (2005). Quantitative measurements of alternating finger tapping in Parkinson’s disease correlate with UPDRS motor disability and reveal the improvement in fine motor control from medication and deep brain stimulation. Movement Disorders, 20(10), 1286–1298. doi: 10.1002/mds.20556 Google Scholar
Toga, A.W., & Thompson, P.M. (2003). Mapping brain asymmetry. Nature Reviews Neuroscience, 4(1), 37–48. doi: 10.1038/nrn1009 nrn1009 [pii]Google Scholar
Tomer, R., Aharon-Peretz, J., & Tsitrinbaum, Z. (2007). Dopamine asymmetry interacts with medication to affect cognition in Parkinson’s disease. Neuropsychologia, 45(2), 357–367. doi: S0028-3932(06)00262-4 [pii] 10.1016/j.neuropsychologia.2006.06.014 Google Scholar
Tomer, R., Levin, B.E., & Weiner, W.J. (1993). Side of onset of motor symptoms influences cognition in Parkinson’s disease. Annals of Neurology, 34(4), 579–584. doi: 10.1002/ana.410340412 Google Scholar
Torta, D.M., Castelli, L., Zibetti, M., Lopiano, L., & Geminiani, G. (2009). On the role of dopamine replacement therapy in decision-making, working memory, and reward in Parkinson’s disease: Does the therapy-dose matter? Brain and Cognition, 71(2), 84–91. doi: S0278-2626(09)00066-9 [pii] 10.1016/j.bandc.2009.04.003 Google Scholar
Tucker, D.M., & Williamson, P.A. (1984). Asymmetric neural control systems in human self-regulation. Psychological Review, 91(2), 185–215.Google Scholar
Uitti, R.J., Baba, Y., Whaley, N.R., Wszolek, Z.K., & Putzke, J.D. (2005). Parkinson disease: Handedness predicts asymmetry. Neurology, 64(11), 1925–1930. doi: 64/11/1925 [pii] 10.1212/01.WNL.0000163993.82388.C8 Google Scholar
van der Hoorn, A., Bartels, A.L., Leenders, K.L., & de Jong, B.M. (2011). Handedness and dominant side of symptoms in Parkinson’s disease. Parkinsonism and Related Disorders, 17(1), 58–60. doi: S1353-8020(10)00245-2 [pii] 10.1016/j.parkreldis.2010.10.002 Google Scholar
van Dyck, C.H., Seibyl, J.P., Malison, R.T., Laruelle, M., Zoghbi, S.S., Baldwin, R.M., & Innis, R.B. (2002). Age-related decline in dopamine transporters: Analysis of striatal subregions, nonlinear effects, and hemispheric asymmetries. American Journal of Geriatric Psychiatry, 10(1), 36–43.Google Scholar
Verreyt, N., Nys, G.M., Santens, P., & Vingerhoets, G. (2011). Cognitive differences between patients with left-sided and right-sided Parkinson’s disease. A review. Neuropsychology Review, 21(4), 405–424. doi: 10.1007/s11065-011-9182-x Google Scholar
Wagner, H.N. Jr., Burns, H.D., Dannals, R.F., Wong, D.F., Langstrom, B., Duelfer, T., & Kuhar, M.J. (1983). Imaging dopamine receptors in the human brain by positron tomography. Science, 221(4617), 1264–1266.Google Scholar
Wechsler, D. (Ed.) (2008). Wechsler Adult Intelligence Scale. (4th ed.). San Antonio, TX: Psychological Corporation.Google Scholar
Williams, L.N., Seignourel, P., Crucian, G.P., Okun, M.S., Rodriguez, R.L., Skidmore, F.M., & Fernandez, H.H. (2007). Laterality, region, and type of motor dysfunction correlate with cognitive impairment in Parkinson’s disease. Movement Disorders, 22(1), 141–145. doi: 10.1002/mds.21220 Google Scholar