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Heterogeneity of Letter Fluency Impairment and Executive Dysfunction in Parkinson's Disease

Published online by Cambridge University Press:  16 August 2013

Lewis Pettit
Human Cognitive Neuroscience - Psychology, University of Edinburgh, Edinburgh, United Kingdom Centre for Cognitive Aging and Epidemiology, University of Edinburgh, Edinburgh, United Kingdom
Martina McCarthy
Human Cognitive Neuroscience - Psychology, University of Edinburgh, Edinburgh, United Kingdom
Richard Davenport
Department of Clinical Neurosciences, University of Edinburgh, Edinburgh, United Kingdom Anne Rowling Regenerative Neurology Clinic, University of Edinburgh, Edinburgh, United Kingdom
Sharon Abrahams*
Human Cognitive Neuroscience - Psychology, University of Edinburgh, Edinburgh, United Kingdom Centre for Cognitive Aging and Epidemiology, University of Edinburgh, Edinburgh, United Kingdom Anne Rowling Regenerative Neurology Clinic, University of Edinburgh, Edinburgh, United Kingdom
Correspondence and reprint requests to: Sharon Abrahams, Department of Psychology, PPLS, University of Edinburgh, 7 George Square, Edinburgh, United Kingdom EH8 9JZ. E-mail:


Letter fluency deficits are commonly detected in non-demented Parkinson's disease (PD) patients but the underlying cause remains uncertain. We investigated the role of slowed processing speed and executive dysfunction. Eighteen non-demented PD participants and nineteen controls were compared on letter fluency using a fluency index (Fi); the average time to “think” of each word, a measure independent of motor speed. Video analyses produced thinking times to switch between word clusters and generate a word within a cluster. Correlational and regression analyses were undertaken with tests of processing speed and executive functioning. The PD group exhibited significantly longer fluency indices than controls across all components. Performance on tests of executive functioning explained a significant proportion of variance whereas performance in processing speed tests did not. Moreover, PD participants with an executive functioning impairment showed significantly worse switching fluency indices only compared with Controls and PD participants without executive dysfunction. PD participants with executive dysfunction exhibited a disproportionate impairment in the time taken to switch between clusters than to think of words within clusters. Executive functioning contributed to fluency performance more than processing speed. Cognitive heterogeneity and motor slowing, may mask the profile of cognitive dysfunction in neurodegenerative disease. (JINS, 2013, 19, 1–9)

Research Articles
Copyright © The International Neuropsychological Society 2013 

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Aarsland, D., Brønnick, K., Larsen, J.P., Tysnes, O.B., Alves, G. (2009). Cognitive impairment in incident, untreated Parkinson disease: The Norwegian ParkWest study. Neurology, 72, 11211126.CrossRefGoogle ScholarPubMed
Abrahams, S., Goldstein, L.H., Kew, J.J., Brooks, D.J., Lloyd, C.M., Frith, C.D., Leigh, P.N. (1996). Frontal lobe dysfunction in amyotrophic lateral sclerosis. A PET study. Brain, 119, 21052120.CrossRefGoogle ScholarPubMed
Abrahams, S., Goldstein, L.H., Simmons, A., Brammer, M.J., Williams, S.C., Giampietro, C.M., Leigh, P.N. (2003). Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses. Human Brain Mapping, 20, 2940.CrossRefGoogle ScholarPubMed
Abrahams, S., Leigh, P.N., Harvey, A., Vythelingum, G.N., Grise, D., Goldstein, L.H. (2000). Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia, 38, 734737.CrossRefGoogle ScholarPubMed
Auriacombe, S., Grossman, M., Carvell, S., Gollomp, S., Stern, M.B., Hurtig, H.I. (1993). Verbal fluency deficits in Parkinson's disease. Neuropsychology, 7, 182192.CrossRefGoogle Scholar
Azuma, T. (2004). Working memory and perseveration in verbal fluency. Neuropsychology, 18, 6677.CrossRefGoogle ScholarPubMed
Azuma, T., Bayles, K.A., Cruz, R.F., Tomoeda, C.K., Wood, J.A., McGeagh, A., Montgomery, E.B. Jr. (1997). Comparing the difficulty of letter, semantic, and name fluency tasks for normal elderly and patients with Parkinson's disease. Neuropsychology, 11, 488497.CrossRefGoogle ScholarPubMed
Azuma, T., Cruz, R.F., Bayles, K.A., Tomoeda, C.K., Montgomery, E.B. Jr. (2003). A longitudinal study of neuropsychological change in individuals with Parkinson's disease. International Journal of Geriatric Psychiatry, 18, 11151120.CrossRefGoogle ScholarPubMed
Baldo, J.V., Schwartz, S., Wilkins, D., Dronkers, N.F. (2006). Role of frontal versus temporal cortex an verbal fluency as revealed by voxel-based lesion symptom mapping. Journal of the International Neuropsychological Society, 12, 896900.CrossRefGoogle ScholarPubMed
Bayles, K.A., Trosset, M.W., Tomoeda, C.K., Montgomery, E.B., Wilson, J. (1993). Generative naming in Parkinson's disease patients. Journal of Clinical and Experimental Neuropsychology, 15, 547562.CrossRefGoogle Scholar
Benton, A.L., deS Hamsher, K.S. (1976). Multilingual aphasia examination. Iowa City: University of Iowa Press.Google Scholar
Bittner, R.M., Crowe, S.F. (2007). The relationship between working memory, processing speed, verbal comprehension and FAS performance following traumatic brain injury. Brain Injury, 21, 709719.CrossRefGoogle ScholarPubMed
Burgess, P.W., Shallice, T. (1997). The Hayling and Brixton Test. Bury St Edmonds, Suffolk: Thames Valley Test Company.Google Scholar
Caviness, J.N., Driver-Dunckley, E., Connor, D.J., Sabbagh, M.N., Hentz, J.G., Noble, B., Alder, C.H. (2007). Defining mild cognitive impairment in Parkinson's disease. Movement Disorders, 22, 12721277.CrossRefGoogle ScholarPubMed
Cooper, J.A., Sagar, H.J., Jordan, N., Harvey, N.S., Suillivan, E.V. (1991). Cognitive impairment in early, untreated Parkinson's disease and its relationship to motor disability. Brain, 114, 20952122.CrossRefGoogle ScholarPubMed
Coughlan, A.K., Hollows, S.E. (1985). The adult memory and information processing battery (AMIPB). Leeds: Coughlan and Hollows.Google Scholar
De Gaspari, D., Siri, C., Di Giola, M., Antonini, A., Isella, V., Pizzolato, A., Pezzoli, G. (2006). Clinical correlates and cognitive underpinnings of verbal fluency after chronic subthalamic stimulation in Parkinson's disease. Parkinsonism and Related Disorders, 12, 289295.CrossRefGoogle ScholarPubMed
Dirnberger, G., Frith, C.D., Jahanshahi, M. (2005). Executive dysfunction in Parkinson's disease is associated with altered pallidal–frontal processing. Neuroimage, 25, 588599.CrossRefGoogle ScholarPubMed
Donovan, K., Siegert, R., McDowall, J., Abernethy, D. (1999). Clustering and switching in verbal fluency in Parkinson's disease. New Zealand Journal of Psychology, 28, 6166.Google Scholar
Dubois, B., Boller, F., Pillon, B., Agid, Y. (1991). Cognitive deficits in Parkinson's disease. In: F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (Vol. 5, pp. 195240). Amsterdam: Elsevier.Google Scholar
Dubois, B., Pillon, B. (1997). Cognitive deficits in Parkinson's disease. Journal of Neurology, 244, 28.CrossRefGoogle ScholarPubMed
Flowers, K.A., Robertson, C., Sheridan, M.R. (1995). Some characteristics of word fluency in Parkinson's disease. Journal of Neurolinguistics, 9, 3346.CrossRefGoogle Scholar
Green, J., McDonald, W.M., Vitek, J.L., Evatt, M., Freeman, A., Haber, M., DeLong, M.R. (2002). Cognitive impairments in advanced PD without dementia. Neurology, 59, 13201324.CrossRefGoogle ScholarPubMed
Hely, M.A., Reid, W.G., Adena, M.A., Halliday, G.M., Morris, J.G. (2008). The Sydney multicenter study of Parkinson's disease: The inevitability of dementia at 20 years. Movement Disorders, 23, 837844.CrossRefGoogle Scholar
Henry, J.D., Crawford, J.R. (2004). Verbal fluency deficits in Parkinson's disease: a meta-analysis. Journal of the International Neuropsychological Society, 10, 608622.CrossRefGoogle ScholarPubMed
Hoehn, M., Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17, 427442.CrossRefGoogle ScholarPubMed
Ivory, S.J., Knight, R.G., Longmore, B.E., Caradoc-Davies, T. (1999). Verbal memory in non-demented patients with idiopathic Parkinson's disease. Neuropsychologia, 37, 817828.CrossRefGoogle ScholarPubMed
Janvin, C.C., Larsen, J.P., Aarsland, D., Hugdahl, K. (2006). Subtypes of mild cognitive impairment in Parkinson's disease: Progression to dementia. Movement Disorders, 21, 13431349.CrossRefGoogle ScholarPubMed
Johnson, A.M., Almeida, Q.J., Stough, C., Thompson, J.C., Singarayer, R., Jog, M.S. (2004). Visual inspection time in Parkinson's disease: Deficits in early stages of cognitive processing. Neuropsychologia, 42, 577583.CrossRefGoogle ScholarPubMed
Kehagia, A.A., Barker, R.A., Robbins, T.W. (2013). Cognitive impairment in Parkinson's disease: The dual syndrome hypothesis. Neuro-degenerative Diseases, 11, 7992.CrossRefGoogle ScholarPubMed
Matison, R., Mayeux, R., Rosen, J., Fahn, S. (1982). “Tip-of the-tongue” phenomenon in Parkinson disease. Neurology, 32, 567570.CrossRefGoogle ScholarPubMed
Mayr, U. (2002). On the dissociation between clustering and switching in verbal fluency: Comment on Troyer, Moscovitch, Winocur, Alexander and Stuss. Neuropsychologia, 40, 562566.CrossRefGoogle ScholarPubMed
McDowd, J., Hoffman, L., Rozek, E., Lyons, K.E., Pahwa, R., Burns, J., Kemper, S. (2011). Understanding verbal fluency in healthy aging, Alzheimer's disease, and Parkinson's disease. Neuropsychology, 25, 210225.CrossRefGoogle ScholarPubMed
McKenna, P., Warrington, E.K. (1983). Graded naming test. Oxford: NFER-Nelson.Google Scholar
Mioshi, E., Dawson, K., Mitchell, J., Arnold, R., Hodges, J.R. (2006). The Addenbrooke's Cognitive Examination Revised (ACE-R): A brief cognitive test battery for dementia screening. International Journal of Geriatric Psychiatry, 21, 10781085.CrossRefGoogle ScholarPubMed
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., Wager, T.D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychology, 41, 49100.CrossRefGoogle ScholarPubMed
Morris, R.G., Downes, J.J., Sahakian, B.J., Evenden, J.L., Heald, A., Robbins, T.W. (1988). Planning and spatial working memory in Parkinson's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 51, 757766.CrossRefGoogle ScholarPubMed
Muslimovic, D., Post, B., Speelman, J.D., Schmand, B. (2005). Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology, 65, 12391245.CrossRefGoogle ScholarPubMed
Owen, A.M. (2004). Cognitive dysfunction in Parkinson's disease: The role of Frontostriatal circuitry. The Neuroscientist, 10, 525537.CrossRefGoogle ScholarPubMed
Owen, A.M., James, M., Leigh, P.N., Summers, B.A., Marsden, C.D., Quinn, N.P., Robbins, T.W. (1992). Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain, 115, 17271751.CrossRefGoogle ScholarPubMed
Pereira, J.B., Junque, C., Marti, M., Ramirez-Ruiz, B., Bargallo, N., Tolosa, E. (2009). Neuroanatomical substrate of visuospatial and visuoperceptual impairment in Parkinson's disease. Movement Disorders, 24, 11931199.CrossRefGoogle ScholarPubMed
Piatt, A.L., Fields, J.A., Paolo, A.M., Koller, W.C., Troster, A.I. (1999). Lexical, semantic, and action verbal fluency in Parkinson's disease with and without dementia. Journal of Clinical and Experimental Neuropsychology, 21, 435443.CrossRefGoogle ScholarPubMed
Raskin, S.A., Sliwinski, M., Borod, J.C. (1992). Clustering strategies on tasks of verbal fluency in Parkinson's disease. Neuropsychologia, 30, 9599.CrossRefGoogle ScholarPubMed
Rende, B., Ramsberger, G., Miyake, A. (2002). Commonalities and differences in the working memory components underlying letter and category fluency tasks: A dual-task investigation. Neuropsychology, 16, 309321.CrossRefGoogle ScholarPubMed
Revonsuo, A., Portin, R., Koivikko, L., Rinne, J.O., Rinne, U.K. (1993). Slowing of information processing in Parkinson's disease. Brain and Cognition, 21, 87110.CrossRefGoogle ScholarPubMed
Ridenour, T.A., Dean, R.S. (1999). Parkinson's disease and neuropsychological assessment. International Journal of Neuroscience, 99, 118.CrossRefGoogle ScholarPubMed
Salthouse, T.A., Atkinson, T.M., Berish, D.E. (2003). Executive functioning as a potential mediator of age-related cognitive decline in normal adults. Journal of Experimental Psychology, General, 132, 566594.CrossRefGoogle ScholarPubMed
Sawamoto, N., Honda, M., Hanakawam, T., Fukuyama, H., Shibasaki, H. (2002). Cognitive slowing in Parkinson's disease: A behavioral evaluation independent of motor slowing. The Journal of Neuroscience, 22, 51985203.CrossRefGoogle ScholarPubMed
Shipley, B.A., Deary, I.J., Tan, J., Christie, G., Starr, J.M. (2002). Efficiency of temporal order discrimination as an indicator of bradyphrenia in Parkinson's disease: The inspection time loop task. Neuropsychologia, 40, 14881493.CrossRefGoogle ScholarPubMed
Taylor, A.E., Saint-Cyr, J.A., Lang, A.E. (1986). Frontal lobe dysfunction in Parkinson's disease. Brain, 109, 845883.CrossRefGoogle ScholarPubMed
Thurstone, L.L., Thurstone, T.G. (1962). Primary mental abilities. Chicago: Science Research Associates.Google Scholar
Tröster, A.I., Fields, J.A., Testa, J.A., Paul, R.H., Blanco, C.R., Hames, K.A., Beatty, W.W. (1998). Cortical and subcortical influences on clustering and switching in the performance of verbal fluency tasks. Neuropsychologia, 36, 295304.CrossRefGoogle ScholarPubMed
Tröster, A. I., Woods, S. P., Fields, J. A., Hanisch, C., Beatty, W. W. 2002. Brain and Cognition, 50, 207–217.Google Scholar
Troyer, A.K., Moscovitch, M., Winocur, G. (1997). Clustering and switching as two components of verbal fluency: Evidence from younger and older healthy adults. Neuropsychology, 11, 138146.CrossRefGoogle ScholarPubMed
Troyer, A.K., Moscovitch, M., Winocur, G., Leach, L., Freedman, M. (1998). Clustering and switching on verbal fluency tests in Alzheimer's and Parkinson's disease. Journal of the International Neuropsychological Society, 4, 137143.CrossRefGoogle ScholarPubMed
Troyer, A.K., Moscovitch, M., Winocur, G., Alexander, M.P., Stuss, D. (1998). Clustering and switching on verbal fluency: the effects of focal frontal- and temporal-lobe lesions. Neuropsychologia, 36, 499504.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, 17871798.CrossRefGoogle Scholar
Zgaljardic, D., Borod, J., Foldi, N.S., Mattis, P. (2003). A review of the cognitive and behavioural sequelae of Parkinson's disease: Relationship to frontostriatal circuitry. Cognitive and Behavioural Neurology, 16, 193210.CrossRefGoogle ScholarPubMed
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