Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T16:17:08.867Z Has data issue: false hasContentIssue false
  • English
  • Français

Symptom Dimensions of Depression and Apathy and Their Relationship With Cognition in Parkinson’s Disease

Published online by Cambridge University Press:  16 October 2017

Sarah M. Szymkowicz ,
Vonetta M. Dotson ,
Jacob D. Jones ,
Michael S. Okun  and
Dawn Bowers
Sarah M. Szymkowicz
Affiliation:
Department of Clinical & Health Psychology, College of Public Health & Health Professions, University of Florida, Gainesville, Florida
Vonetta M. Dotson
Affiliation:
Department of Clinical & Health Psychology, College of Public Health & Health Professions, University of Florida, Gainesville, Florida Department of Neuroscience, College of Medicine, University of Florida, Gainesville, Florida
Jacob D. Jones
Affiliation:
Department of Psychiatry & Biobehavioral Sciences, David Geffen School of Medicine, University of California - Los Angeles, Los Angeles, California
Michael S. Okun
Affiliation:
Department of Neurology, College of Medicine, University of Florida, Gainesville, Florida Center for Movement Disorders & Neurorestoration, College of Medicine, University of Florida, Gainesville, Florida
Dawn Bowers*
Affiliation:
Department of Clinical & Health Psychology, College of Public Health & Health Professions, University of Florida, Gainesville, Florida Department of Neurology, College of Medicine, University of Florida, Gainesville, Florida Center for Movement Disorders & Neurorestoration, College of Medicine, University of Florida, Gainesville, Florida
*
Correspondence and reprint requests to: Dawn Bowers, Department of Clinical & Health Psychology, College of Public Health & Health Professions, University of Florida, P.O. Box 100165, Gainesville, FL 32610-0165. E-mail: dawnbowers@phhp.ufl.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Both depression and apathy, alone and in combination, have been shown to negatively affect cognition in patients with Parkinson’s disease (PD). However, the influence of specific symptom dimensions of depression and apathy on cognition is not well understood. The current study investigated the relationship between symptom dimensions of depression and apathy, based on factors identified in Kirsch-Darrow et al. (2011), and memory and executive function in PD. Methods: A sample of 138 non-demented individuals with PD (mean age=64.51±7.43 years) underwent neuropsychological testing and completed the Beck Depression Inventory, 2nd Edition, and Apathy Scale. Separate hierarchical regression models examined the relationship between symptom dimensions of depression and apathy (“pure” depressive symptoms, “pure” apathy, loss of interest/pleasure [anhedonia], and somatic symptoms) and three cognitive domain composites: immediate verbal memory, delayed verbal memory, and executive function. Results: After adjusting for general cognitive status and the influence of the other symptom dimensions, “pure” depressive symptoms were negatively associated with the delayed verbal memory composite (p<.034) and somatic symptoms were positively associated with the executive function composite (p<.026). No symptom dimensions were significantly related to the immediate verbal memory composite. Conclusions: Findings suggest that specific mood symptoms are associated with delayed verbal memory and executive function performance in non-demented patients with PD. Further research is needed to better understand possible mechanisms through which specific symptom dimensions of depression and apathy are associated with cognition in PD. (JINS, 2018, 24, 269–282)

Keywords

EmotionMoodMemoryExecutive functionNeuropsychologyMovement disorders
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 24 , Issue 3 , March 2018 , pp. 269 - 282
Copyright
Copyright © The International Neuropsychological Society 2017 

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., Marsh, L., & Schrag, A. (2009). Neuropsychiatric symptoms in Parkinson’s disease. Movement Disorders, 24(15), 2175–2186.Google Scholar
Aarsland, D., Pahlhagen, S., Ballard, C.G., Ehrt, U., & Svenningsson, P. (2011). Depression in Parkinson disease--Epidemiology, mechanisms and management. Nature Reviews. Neurology, 8(1), 35–47.Google Scholar
American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders (5th ed.), Washington, DC: American Psychiatric Association.Google Scholar
Army Individual Test Battery. (1944). Manual of Directions and Scoring. Washington, DC: War Department, Adjutant General’s Office.Google Scholar
Assogna, F., Cravello, L., Caltagirone, C., & Spalletta, G. (2011). Anhedonia in Parkinson’s disease: A systematic review of the literature. Movement Disorders, 26(10), 1825–1834.CrossRefGoogle ScholarPubMed
Barone, P. (2010). Neurotransmission in Parkinson’s disease: Beyond dopamine. European Journal of Neurology, 17(3), 364–376.CrossRefGoogle ScholarPubMed
Baune, B.T., Suslow, T., Arolt, V., & Berger, K. (2007). The relationship between psychological dimensions of depressive symptoms and cognitive functioning in the elderly - the MEMO-Study. Journal of Psychiatric Research, 41(3-4), 247–254.Google Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Berardelli, I., Pasquini, M., Roselli, V., Biondi, M., Berardelli, A., & Fabbrini, G. (2015). Cognitive behavioral therapy in movement disorders: A review. Movement Disorders Clinical Practice, 2(2), 107–115.Google Scholar
Bogdanova, Y., & Cronin-Golomb, A. (2012). Neurocognitive correlates of apathy and anxiety in Parkinson’s disease. Parkinsons Disease, 2012, 793076.Google Scholar
Boggio, P.S., Ferrucci, R., Rigonatti, S.P., Covre, P., Nitsche, M., Pascual-Leone, A., & Fregni, F. (2006). Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. Journal of the Neurological Sciences, 249(1), 31–38.Google Scholar
Bonelli, R.M., & Cummings, J.L. (2007). Frontal-subcortical circuitry and behavior. Dialogues in Clinical Neuroscience, 9(2), 141–151.CrossRefGoogle ScholarPubMed
Brailean, A., Comijs, H.C., Aartsen, M.J., Prince, M., Prina, A.M., Beekman, A., &Huisman, M. (2016). Late-life depression symptom dimensions and cognitive functioning in the Longitudinal Aging Study Amsterdam (LASA). Journal of Affective Disorders, 201, 171–178.Google Scholar
Brandt, J., & Benedict, R.H.B. (2001). Hopkins Verbal Learning Test - Revised, Professional Manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Burdick, D.J., Cholerton, B., Watson, G.S., Siderowf, A., Trojanowski, J.Q., Weintraub, D., & Leverenz, J.B. (2014). People with Parkinson’s disease and normal MMSE score have a broad range of cognitive performance. Movement Disorders, 29(10), 1258–1264.CrossRefGoogle ScholarPubMed
Burn, D.J., Landau, S., Hindle, J.V., Samuel, M., Wilson, K.C., & Hurt, C.S., . . . PROMS-PD Study Group. (2012). Parkinson’s disease motor subtypes and mood. Movement Disorders, 27(3), 379–386.CrossRefGoogle ScholarPubMed
Butterfield, L.C., Cimino, C.R., Oelke, L.E., Hauser, R.A., & Sanchez-Ramos, J. (2010). The independent influence of apathy and depression on cognitive functioning in Parkinson’s disease. Neuropsychology, 24(6), 721–730.Google Scholar
Butterfield, L.C., Cimino, C.R., Salazar, R., Sanchez-Ramos, J., Bowers, D., & Okun, M.S. (2017). The Parkinson’s Active Living (PAL) Program. Journal of Geriatric Psychiatry and Neurology, 30(1), 11–25.CrossRefGoogle ScholarPubMed
Cohen, J. (1969). Statistical power analysis for the behavioural sciences. New York, NY: Academic Press.Google Scholar
Cohen, M.L., Aita, S., Mari, Z., & Brandt, J. (2015). The unique and combined effects of apathy and depression on cognition in Parkinson’s disease. Journal of Parkinson’s Disease, 5(2), 351–359.Google Scholar
Costa, A., Peppe, A., Carlesimo, G.A., Pasqualetti, P., & Caltagirone, C. (2006). Major and minor depression in Parkinson’s disease: A neuropsychological investigation. European Journal of Neurology, 13(9), 972–980.CrossRefGoogle ScholarPubMed
Cubo, E., Benito-Leon, J., Coronell, C., Armesto, D., & ANIMO Study Group. (2012). Clinical correlates of apathy in patients recently diagnosed with Parkinson’s disease: The ANIMO study. Neuroepidemiology, 38(1), 48–55.Google Scholar
Damier, P., Hirsch, E.C., Agid, Y., & Graybiel, A.M. (1999). The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain, 122 (Pt 8), 1437–1448.Google ScholarPubMed
Dirnberger, G., & Jahanshahi, M. (2013). Executive dysfunction in Parkinson’s disease: A review. Journal of Neuropsychology, 7(2), 193–224.Google Scholar
Dotson, V.M., Zonderman, A.B., Kraut, M.A., & Resnick, S.M. (2012). Temporal relationships between depressive symptoms and white matter hyperintensities in older men and women. International Journal of Geriatric Psychiatry, 28(1), 66–74.Google Scholar
Dujardin, K., Sockeel, P., Delliaux, M., Destee, A., & Defebvre, L. (2009). Apathy may herald cognitive decline and dementia in Parkinson’s disease. Movement Disorders, 24(16), 2391–2397.Google Scholar
Erro, R., Santangelo, G., Picillo, M., Vitale, C., Amboni, M., Longo, K., & Pellecchia, M.T. (2013). Side of onset does not influence cognition in newly diagnosed untreated Parkinson’s disease patients. Parkinsonism & Related Disorders, 19(2), 256–259.Google Scholar
Fahn, S., Elton, R. & Members of the UPDRS Development Committee. (1987). Unified Parkinson’s disease rating scale. In S. Fahn, C. D. Marsden, D. Calne & N. Holstein (Eds.), Recent developments in Parkinson’s disease, (Vol. 2, pp 153–163). Plurham Park, NJ: Macmillian Healthcare Information.Google Scholar
Fernandez, H.H., & Lapane, K.L. (2000). Estrogen use among nursing home residents with a diagnosis of Parkinson’s disease. Movement Disorders, 15(6), 1119–1124.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Fernandez, H.H., See, R.H., Gary, M.F., Bowers, D., Rodriguez, R.L., Jacobson, C., & Okun, M.S. (2009). Depressive symptoms in Parkinson disease correlate with impaired global and specific cognitive performance. Journal of Geriatric Psychiatry and Neurology, 22(4), 223–227.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
Foster, P.S., Drago, V., Crucian, G.P., Sullivan, W.K., Rhodes, R.D., Shenal, B.V., & Heilman, K.M. (2011). Anxiety and depression severity are related to right but not left onset Parkinson’s disease duration. Journal of the Neurological Sciences, 305(1-2), 131–135.Google Scholar
Foster, P.S., Drago, V., Mendez, K., Witt, J.C., Crucian, G.P., & Heilman, K.M. (2013). Mood disturbances and cognitive functioning in Parkinson’s disease: The effects of disease duration and side of onset of motor symptoms. Journal of Clinical and Experimental Neuropsychology, 35(1), 71–82.Google Scholar
Goetz, C.G., Poewe, W., Rascol, O., Sampaio, C., Stebbins, G.T., & Counsell, C., . . . Movement Disorder Society Task Force on Rating Scales for Parkinson’s, D. (2004). Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: Status and recommendations. Movement Disorders, 19(9), 1020–1028.Google Scholar
Golden, C.J. (1978). Stroop Color and Word Test. Wood Dale, IL: Stoelting Company.Google Scholar
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23, 56–62.Google Scholar
Heaton, R.K., Grant, I., & Matthews, C.G. (1991). Comprehensive norms for an expanded Halstead-Reitan Battery: Demographic corrections, research findings, and clinical applications. Odessa, FL: Psychological Assessment Resources, Inc.Google Scholar
Heller, J., Dogan, I., Schulz, J.B., & Reetz, K. (2014). Evidence for gender differences in cognition, emotion and quality of life in Parkinson’s disease? Aging and Disease, 5(1), 63–75.Google Scholar
Hughes, A.J., Ben-Shlomo, Y., Daniel, S.E., & Lees, A.J. (2001). What features improve the accuracy of clinical diagnosis in Parkinson’s disease: A clinicopathologic study. 1992. Neurology, 57(10 Suppl 3), S34–S38.Google Scholar
Hwang, J.W., Egorova, N., Yang, X.Q., Zhang, W.Y., Chen, J., Yang, X.Y., & . . . Kong, J. (2015). Subthreshold depression is associated with impaired resting-state functional connectivity of the cognitive control network. Translational Psychiatry, 5, e683.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 the Neurological Sciences, 310(1-2), 70–74.Google Scholar
IBM Corp. (2013). IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corp.Google Scholar
Jankovic, J. (2008). Parkinson’s disease: Clinical features and diagnosis. Journal of Neurology, Neurosurgery, and Psychiatry, 79(4), 368–376.Google Scholar
Jones, J.D., Butterfield, L.C., Song, W., Lafo, J., Mangal, P., Okun, M.S., & Bowers, D. (2015). Anxiety and depression are better correlates of Parkinson’s disease quality of life than apathy. The Journal of Neuropsychiatry and Clinical Neurosciences, 27(3), 213–218.Google Scholar
Jones, J.D., Mangal, P., Lafo, J., Okun, M.S., & Bowers, D. (2016). Mood Differences Among Parkinson’s Disease Patients With Mild Cognitive Impairment. The Journal of Neuropsychiatry and Clinical Neurosciences, 28(3), 211–216.Google Scholar
Jones, J.D., Marsiske, M., Okun, M.S., & Bowers, D. (2015). Latent growth-curve analysis reveals that worsening Parkinson’s disease quality of life is driven by depression. Neuropsychology, 29(4), 603–609.Google Scholar
Jurica, P.J., Leitten, C.L., & Mattis, S. (2001). DRS-2: Dementia Rating Scale-2: Professional Manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Kirsch-Darrow, L., Marsiske, M., Okun, M.S., Bauer, R., & Bowers, D. (2011). Apathy and depression: Separate factors in Parkinson’s disease. Journal of the International Neuropsychological Society, 17(6), 1058–1066.Google Scholar
Kulisevsky, J., Pagonabarraga, J., Pascual-Sedano, B., Garcia-Sanchez, C., Gironell, A., & Trapecio Group Study. (2008). Prevalence and correlates of neuropsychiatric symptoms in Parkinson’s disease without dementia. Movement Disorders, 23(13), 1889–1896.Google Scholar
Lafo, J.A., Jones, J.D., Okun, M.S., Bauer, R.M., Price, C.C., & Bowers, D. (2015). Memory similarities between essential tremor and Parkinson’s disease: A final common pathway? The Clinical Neuropsychologist, 29(7), 985–1001.Google Scholar
Lamar, M., Charlton, R., Zhang, A., & Kumar, A. (2012). Differential associations between types of verbal memory and prefrontal brain structure in healthy aging and late life depression. Neuropsychologia, 50(8), 1823–1829.Google Scholar
Leentjens, A.F., Dujardin, K., Marsh, L., Martinez-Martin, P., Richard, I.H., Starkstein, S.E., & Goetz, C.G. (2008). Apathy and anhedonia rating scales in Parkinson’s disease: Critique and recommendations. Movement Disorders, 23(14), 2004–2014.CrossRefGoogle ScholarPubMed
Levy, R., & Dubois, B. (2006). Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cerebral Cortex, 16(7), 916–928.Google Scholar
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), 262–267.CrossRefGoogle ScholarPubMed
Marin, R.S., Biedrzycki, R.C., & Firinciogullari, S. (1991). Reliability and validity of the Apathy Evaluation Scale. Psychiatry Research, 38(2), 143–162.Google Scholar
Marras, C., & Lang, A. (2013). Parkinson’s disease subtypes: Lost in translation? Journal of Neurology, Neurosurgery, and Psychiatry, 84(4), 409–415.Google Scholar
Marsh, L., McDonald, W.M., Cummings, J., Ravina, B., & NINDS/NIMH Work Group on Depression and Parkinson’s Disease. (2006). Provisional diagnostic criteria for depression in Parkinson’s disease: Report of an NINDS/NIMH Work Group. Movement Disorders, 21(2), 148–158.Google Scholar
Mayberg, H.S., & Solomon, D.H. (1995). Depression in Parkinson’s disease: A biochemical and organic viewpoint. Advances in Neurology, 65, 49–60.Google Scholar
McLaren, M.E., Szymkowicz, S.M., O’Shea, A., Woods, A.J., Anton, S.D., & Dotson, V.M. (2017). Vertex-wise examination of depressive symptom dimensions and brain volumes in older adults. Psychiatry Research, 260, 70–75.CrossRefGoogle ScholarPubMed
Meyer, A., Zimmermann, R., Gschwandtner, U., Hatz, F., Bousleiman, H., Schwarz, N., & Fuhr, P. (2014). Apathy in Parkinson’s disease is related to executive function, gender and age but not to depression. Frontiers in Aging Neuroscience, 6, 350.Google Scholar
Miller, I.N., & Cronin-Golomb, A. (2010). Gender differences in Parkinson’s disease: Clinical characteristics and cognition. Movement Disorders, 25(16), 2695–2703.Google Scholar
Modestino, E.J., Amenechi, C., Reinhofer, A., & O’Toole, P. (2017). Side-of-onset of Parkinson’s disease in relation to neuropsychological measures. Brain and Behavior, 7(1), e00590.CrossRefGoogle ScholarPubMed
Moustafa, A.A., Bell, P., Eissa, A.M., & Hewedi, D.H. (2013). The effects of clinical motor variables and medication dosage on working memory in Parkinson’s disease. Brain and Cognition, 82(2), 137–145.Google Scholar
Moustafa, A.A., Krishna, R., Eissa, A.M., & Hewedi, D.H. (2013). Factors underlying probabilistic and deterministic stimulus-response learning performance in medicated and unmedicated patients with Parkinson’s disease. Neuropsychology, 27(4), 498–510.Google Scholar
Panegyres, P.K. (2004). The contribution of the study of neurodegenerative disorders to the understanding of human memory. QJM, 97(9), 555–567.Google Scholar
Pellicano, C., Assogna, F., Cravello, L., Langella, R., Caltagirone, C., Spalletta, G., & Pontieri, F.E. (2015). Neuropsychiatric and cognitive symptoms and body side of onset of parkinsonism in unmedicated Parkinson’s disease patients. Parkinsonism and Related Disorders, 21(9), 1096–1100.Google Scholar
Poletti, M., De Rosa, A., & Bonuccelli, U. (2012). Affective symptoms and cognitive functions in Parkinson’s disease. Journal of the Neurological Sciences, 317(1-2), 97–102.Google Scholar
Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1(3), 385–401.Google Scholar
Ravizza, S.M., Goudreau, J., Delgado, M.R., & Ruiz, S. (2012). Executive function in Parkinson’s disease: Contributions of the dorsal frontostriatal pathways to action and motivation. Cognitive, Affective & Behavioral Neuroscience, 12(1), 193–206.Google Scholar
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 & Related Disorders, 15(5), 379–382.Google Scholar
Riggeal, B.D., Crucian, G.P., Seignourel, P., Jacobson, C.E., Okun, M.S., Rodriguez, R., & Fernandez, H.H. (2007). Cognitive decline tracks motor progression and not disease duration in Parkinson patients. Neuropsychiatric Disease and Treatment, 3(6), 955–958.Google Scholar
Rock, P.L., Roiser, J.P., Riedel, W.J., & Blackwell, A.D. (2014). Cognitive impairment in depression: A systematic review and meta-analysis. Psychological Medicine, 44(10), 2029–2040.Google Scholar
Rothman, K.J. (1990). No adjustments are needed for multiple comparisons. Epidemiology, 1(1), 43–46.Google Scholar
Sacher, J., Neumann, J., Funfstuck, T., Soliman, A., Villringer, A., & Schroeter, M.L. (2012). Mapping the depressed brain: A meta-analysis of structural and functional alterations in major depressive disorder. Journal of Affective Disorders, 140(2), 142–148.Google Scholar
Santangelo, G., Morgante, L., Savica, R., Marconi, R., Grasso, L., Antonini, A., ... PRIAMO Study Group. (2009). Anhedonia and cognitive impairment in Parkinson’s disease: Italian validation of the Snaith-Hamilton Pleasure Scale and its application in the clinical routine practice during the PRIAMO study. Parkinsonism & Related Disorders, 15(8), 576–581.CrossRefGoogle ScholarPubMed
Santangelo, G., Trojano, L., Barone, P., Errico, D., Grossi, D., & Vitale, C. (2013). Apathy in Parkinson’s disease: Diagnosis, neuropsychological correlates, pathophysiology and treatment. Behavioural Neurology, 27(4), 501–513.Google Scholar
Santangelo, G., Vitale, C., Trojano, L., Longo, K., Cozzolino, A., Grossi, D., & Barone, P. (2009). Relationship between depression and cognitive dysfunctions in Parkinson’s disease without dementia. Journal of Neurology, 256(4), 632–638.Google Scholar
Schrag, A., Barone, P., Brown, R.G., Leentjens, A.F., McDonald, W.M., Starkstein, S., & Goetz, C.G. (2007). Depression rating scales in Parkinson’s disease: Critique and recommendations. Movement Disorders, 22(8), 1077–1092.Google Scholar
Seichepine, D.R., Neargarder, S., Miller, I.N., Riedel, T.M., Gilmore, G.C., & Cronin-Golomb, A. (2011). Relation of Parkinson’s disease subtypes to visual activities of daily living. Journal of the International Neuropsychological Society, 17(5), 841–852.Google Scholar
Sheikh, J.I., & Yesavage, J.A. (1986). Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version. Clinical Gerontologist, 5, 165–173.Google Scholar
Snaith, R.P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., & Trigwell, P. (1995). A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. British Journal of Psychiatry, 167(1), 99–103.Google Scholar
Snaith, R.P., & Zigmond, A.S. (2000). Hospital Anxiety and Depression Scale (HADS). In A. J. Rush (Ed.), Handbook of psychiatric meaures (pp 547–548). Washington, DC: American Psychiatric Association.Google Scholar
Snyder, H.R. (2013). Major depressive disorder is associated with broad impairments on neuropsychological measures of executive function: A meta-analysis and review. Psychological Bulletin, 139(1), 81–132.Google Scholar
Spalletta, G., Fagioli, S., Caltagirone, C., & Piras, F. (2013). Brain microstructure of subclinical apathy phenomenology in healthy individuals. Human Brain Mapping, 34(12), 3193–3203.Google Scholar
Starkstein, S.E., Mayberg, H.S., Preziosi, T.J., Andrezejewski, P., Leiguarda, R., & Robinson, R.G. (1992). Reliability, validity, and clinical correlates of apathy in Parkinson’s disease. The Journal of Neuropsychiatry and Clinical Neurosciences, 4(2), 134–139.Google Scholar
Starkstein, S.E., Petracca, G., Chemerinski, E., Teson, A., Sabe, L., Merello, M., & Leiguarda, R. (1998). Depression in classic versus akinetic-rigid Parkinson’s disease. Movement Disorders, 13(1), 29–33.Google Scholar
Tekin, S., & Cummings, J.L. (2002). Frontal-subcortical neuronal circuits and clinical neuropsychiatry: An update. Journal of Psychosomatic Research, 53(2), 647–654.Google Scholar
Trivedi, M.H., & Greer, T.L. (2014). Cognitive dysfunction in unipolar depression: Implications for treatment. Journal of Affective Disorders, 152-154, 19–27.Google Scholar
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), 611–620.Google Scholar
Varanese, S., Perfetti, B., Ghilardi, M.F., & Di Rocco, A. (2011). Apathy, but not depression, reflects inefficient cognitive strategies in Parkinson’s disease. PLoS One, 6(3), e17846.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. Neuropsychological Review, 21(4), 405–424.Google Scholar
Visser, M., Leentjens, A.F., Marinus, J., Stiggelbout, A.M., & van Hilten, J.J. (2006). Reliability and validity of the Beck depression inventory in patients with Parkinson’s disease. Movement Disorders, 21(5), 668–672.Google Scholar
Vrieze, E., Demyttenaere, K., Bruffaerts, R., Hermans, D., Pizzagalli, D.A., Sienaert, P., & Claes, S. (2014). Dimensions in major depressive disorder and their relevance for treatment outcome. Journal of Affective Disorders, 155, 35–41.Google Scholar
Wechsler, D. (1997). The Wechsler Memory Scale (3rd ed.), San Antonio, TX: Psychological Corporation.Google Scholar
Wen, M.C., Chan, L.L., Tan, L.C., & Tan, E.K. (2016). Depression, anxiety, and apathy in Parkinson’s disease: Insights from neuroimaging studies. European Journal of Neurology, 23(6), 1001–1019.Google Scholar
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), 1787–1798.Google Scholar
Zahodne, L.B., Bowers, D., Price, C.C., Bauer, R.M., Nisenzon, A., Foote, K.D., & Okun, M.S. (2011). The case for testing memory with both stories and word lists prior to dbs surgery for Parkinson’s Disease. The Clinical Neuropsychologist, 25(3), 348–358.Google Scholar
Supplementary material: File

Szymkowicz et al supplementary material

Tables S1-S6

Download Szymkowicz et al supplementary material(File)
File 47.3 KB