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Cognitive Impairment in Parkinson’s Disease: More than a Frontostriatal Dysfunction

Published online by Cambridge University Press:  28 October 2014

Iván Galtier*
Affiliation:
Universidad de La Laguna (Spain)
Antonieta Nieto
Affiliation:
Universidad de La Laguna (Spain)
Jesús N. Lorenzo
Affiliation:
Hospital Universitario N.S. La Candelaria (Spain)
José Barroso
Affiliation:
Universidad de La Laguna (Spain)
*
*Iván Galtier. Facultad de Psicología. Universidad de La Laguna. 38205. La Laguna. (Spain). Phone: +34–922317564. Fax: +34–922317561. E-mail: [email protected]

Abstract

Cognitive deficit in Parkinson’s disease has been traditionally considered as being mainly related to executive dysfunction secondary to frontostriatal affectation. However, this traditional consideration has recently been challenged. Forty-three nondemented PD patients (mean age = 59.19; SD = 9.64) and twenty control group subjects (mean age = 60.85; SD = 12.26) were studied. They were assessed on a wide range of cognitive functions. Patients showed motor slowing (p = .012), along with alterations in visuoperceptive (p = .001), visuospatial (p = .007) and visuoconstructive functions (p = .017), as well as in visual span (direct: p = .008; inverse: p = .037). Regarding executive functions, differences were not observed in classical measures for verbal fluency (phonetic: p = .28; semantic: p = .27) or in response inhibition (Stroop test: p = .30), while execution was altered in other prefrontal tasks (Wisconsin Test: p = .003; action fluency: p = .039). Patients showed altered performance in verbal learning processes (p = .005) and delayed memory (free: p = .032; cued: p = .006), visuospatial learning (p = .016) and linguistic functions (naming: p < .001; comprehension: p = .007). Poor performance in visuospatial memory is predicted by deficits in working memory and visuospatial perception. Taken together, the observed alterations not only suggest prefrontal affectation, but also temporal and parietal systems impairment. Thus, cognitive dysfunction in nondemented PD patients cannot be exclusively explained by frontostriatal circuit affectation and the resulting executive dysfunction.

Type
Research Article
Copyright
Copyright © Universidad Complutense de Madrid and Colegio Oficial de Psicólogos de Madrid 2014 

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References

Apostolova, L., Alves, G., Hwang, K. S., Babakchanian, S., Bronnick, K. S., Larsen, J. P., ... M. K, Beyer. (2012). Hippocampal and ventricular changes in Parkinson’s disease mild cognitive impairment. Neurobiology of Aging, 33, 21132124. http://dx.doi.org/10.1016/j.neurobiolaging.2011.06.014 Google Scholar
Barbizet, J., & Cany, E. (1968). Clinical and psychometrical study of a patient with memory disturbances. International Journal of Neurology, 7, 4454.Google ScholarPubMed
Barone, P., Aarsland, D., Burn, D., Emre, M., Kulisevsky, J., & Weintraub, D. (2011). Cognitive impairment in nondemented Parkinson’s disease. Movement Disorders, 26, 24832495. http://dx.doi.org/10.1002/mds.23919.Google Scholar
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561571. http://dx.doi.org/10.1001/archpsyc.1961.01710120031004 .Google Scholar
Benton, A. L., & Hamsher, K. (1989). Multilingual aphasia examination (2 nd Ed.). Iowa City, IA: Department of Neurology and Psychology. The University of Iowa.Google Scholar
Benton, A. L., Hamsher, K. S., Varney, N. R., & Spreen, O. (1983). Contributions of the neuropsychological assessment: A clinical manual. New York: Oxford University Press.Google Scholar
Bertella, L., Albani, G., Greco, E., Priano, L., Mauro, A., Marchi, S., … Semenza, C. (2002). Noun verb dissociation in Parkinson’s disease. Brain and Cognition, 48, 277280.Google Scholar
Beyer, M. K., Bronnick, K. S., Hwang, K. S., Bergsland, N., Tysnes, O. B., Larsen, J. P., ... Apostolova, L. G. (2013). Verbal memory is associated with structural hippocampal changes in newly diagnosed Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 84, 2328. http://dx.doi.org/10.1136/jnnp-2012-303054.Google Scholar
Blesa, R., Pujol, M., Aguilar, M., Santacruz, P., Bertran-Serra, I., Hernández, G., … NORMACODEM Group (2001). Clinical validity of the mini-mental state for Spanish speaking communities. Neuropsychologica, 39, 11501157. http://dx.doi.org/10.1016/S0028-3932(01)00055-0 Google Scholar
Braak, H., Rüb, U., & Del Tredici, K. (2006). Cognitive decline correlates with neuropathological stage in Parkinson’s disease. Journal of the Neurological Sciences, 248, 255258. http://dx.doi.org/10.1016/j.jns.2006.05.011 .CrossRefGoogle ScholarPubMed
Brand, M., Labudda, K., Kalbe, E., Hilker, R., Emmans, D., Fuchs, G., ... Markowitscha, H. J. (2004). Decision-making impairments in patients with Parkinson’s disease. Behavioral Neurology, 15, 7785. http://dx.doi.org/10.1155/2004/578354 Google Scholar
Caballol, N., Marti, M. J., & Tolosa, E. (2007). Cognitive dysfunction and dementia in Parkinson disease. Movement Disorders, 22, 358366. http://dx.doi.org/10.1002/mds.21677.Google Scholar
Cotelli, M., Borroni, B., Manenti, R., Zanetti, M., Arevalo, A., Cappa, S. F., … Padovani, A. (2007). Action and object naming in Parkinson's disease without dementia. European Journal of Neurology, 14, 632637. http://dx.doi.org/10.1111/j.1468-1331.2007.01797.x Google Scholar
Cuetos, F., Ellis, A., & Álvarez, B. (1999). Naming times for the Snodgrass and Vanderwart pictures in Spanish. Behavior, Research, Methods, Instruments, & Computers, 31, 650658. http://dx.doi.org/10.3758/BF03200741 Google Scholar
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (1987). California Verbal Learning Test. Research edition manual. New York, NY: Psychological Corporation.Google Scholar
Druks, J., & Masterson, J. (2000). Object and action naming batter. Hove, UK: Psychology Press.Google Scholar
Dubois, B., Burn, D., Goetz, C., Aarsland, D., Brown, R. G., Broe, G. A., … Emre, M. (2007). Diagnostic procedures for Parkinson’s disease dementia: recommendations from the movement disorder society task force. Movement disorders, 22, 23142324. http://dx.doi.org/10.1002/mds.21844 Google Scholar
Emre, M., Aarsland, D., Brown, R., Burn, D. J., Duyckaerts, C., Mizuno, Y., ... Dubois, B. (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s Disease. Movement Disorders, 22, 16891707. http://dx.doi.org/10.1002/mds.21507.Google Scholar
Fahn, S., & Elton, R. L. (1987). Unified Parkinson’s Disease Rating Scale. In: Fahn, S., Marsden, C. D., Goldstein, M., & Calne, D. B. (Eds.), Recent developments in Parkinson’s disease. (pp. 153163). New York, NY: Macmillan.Google Scholar
Galtier, I., Nieto, A., Barroso, J., & Lorenzo, J. N. (2009). Visuospatial learning impairment in Parkinson disease. Psicothema, 21, 2126.Google Scholar
Golden, C. J. (1978 ). Stroop color and word test. A manual for clinical and experimental uses. Illinois, IL: Stoelting Company.Google Scholar
Gronwall, D. M. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual & Motor Skills, 44, 367–373. http://dx.doi.org/10.2466/pms.1977.44.2.367 Google Scholar
Grossman, M. (1999). Sentence processing in Parkinson’s disease. Brain and Cognition, 40, 387413. http://dx.doi.org/10.1006/brcg.1999.1087 Google Scholar
Grossman, M., Carvell, S., Stern, M. B., Gollomp, S., & Hurtig, H. I. (1992). Sentence comprehension in Parkinson's disease: The role of attention and memory. Brain and Language, 42, 347384. http://dx.doi.org/10.1016/0093-934X(92)90074-O Google Scholar
Heaton, R. K. (1981). Wisconsin Card Sorting Test manual. Odessa: FL: Psychological assessment resources.Google Scholar
Higginson, C. I., Wheelock, V. L., Carroll, K. E., & Sigvardt, K. A. (2005). Recognition memory in Parkinson’s disease with and without dementia: Evidence inconsistent with the retrieval deficit hypothesis. Journal of Clinical and Experimental Neuropsychology, 27, 516528. http://dx.doi.org/10.1080/13803390490515469 Google Scholar
Hochstadt, J., Nakano, H., Lieberman, P., & Friedman, J. (2006). The roles of sequencing and verbal working memory in sentence comprehension deficits in Parkinson’s disease. Brain and Language, 97, 243257. http://dx.doi.org/10.1016/j.bandl.2005.10.011 Google Scholar
Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17, 427442. http://dx.doi.org/10.1212/WNL.17.5.427 CrossRefGoogle ScholarPubMed
Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992). Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: A clinico-pathological study of 100 cases. Journal of Neurology, Neurosurgery, and Psychiatry, 55, 181184. http://dx.doi.org/10.1136/jnnp.55.3.181 Google Scholar
Ibarretxe-Bilbao, N., Tolosa, E., Junque, C., & Marti, M. J. (2009). MRI and cognitive impairment in Parkinson’s disease. Movement Disorders, 24, 748753. http://dx.doi.org/10.1002/mds.22670.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 & Related Disorders, 15, 8893. http://dx.doi.org/10.1016/j.parkreldis.2008.03.005.Google Scholar
Lees, A. J., & Smith, E. (1983). Cognitive deficits in the early stages of Parkinson’s disease. Brain, 106, 257270. http://dx.doi.org/10.1093/brain/106.2.257 Google Scholar
Liozidou, A., Potagas, C., Papageorgiou, S. G., & Zalonis, I. (2012). The role of working memory and information processing speed on Wisconsin Card Sorting Test performance in Parkinson disease without dementia. Journal of Geriatric Psychiatry and Neurology, 25, 215221. http://dx.doi.org/10.1177/0891988712466456 Google Scholar
Muslimovic, D., Post, B., Speelman, J. D., & Schmand, B. (2007). Motor procedural learning in Parkinson’s disease. Brain, 130, 28872897. http://dx.doi.org/10.1093/brain/awm211 Google Scholar
Obeso, I., Casabona, E., Bringas, M. L., Alvarez, L., & Jahanshahi, M. (2012). Semantic and phonemic verbal fluency in Parkinson’s disease: Influence of clinical and demographic variables. Behavioural Neurology, 25, 111118. http://dx.doi.org/10.1155/2012/673610 CrossRefGoogle ScholarPubMed
Pereira, J. B., Junque, C., Marti, M. J., Ramirez-Ruiz, B., Bargallo, N., & Tolosa, E. (2009). Neuroanatomical substrate of visuospatial and visuoperceptual impairment in Parkinson’s disease. Movement Disorders, 24, 11931199. http://dx.doi.org/10.1002/mds.22560 Google Scholar
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. http://dx.doi.org/10.5555/jcen.21.4.435.885 CrossRefGoogle ScholarPubMed
Piatt, A. L., Fields, J. A., Paolo, A. M., & Troster, A. I. (1999). Action (verb naming) fluency as an executive function measure: Convergent and divergent evidence of validity. Neuropsychologia, 37, 14991503. http://dx.doi.org/10.1016/S0028-3932(99)00066-4 CrossRefGoogle ScholarPubMed
Pillon, B., Deweer, B., Agid, Y., & Dubois, B. (1993). Explicit memory in Alzheimer’s, Huntington’s, and Parkinson’s diseases. Archives of Neurology, 50, 374379. http://dx.doi.org/10.1001/archneur.1993.00540040036010 Google Scholar
Rodriguez-Ferreiro, J., Menendez, M., Ribacoba, R., & Cuetos, F. (2009). Action naming is impaired in Parkinson disease patients. Neuropsychologia, 47, 32713274. http://dx.doi.org/10.1016/j.neuropsychologia.2009.07.007 Google Scholar
Schneider, J. S. (2007). Behavioral persistence deficit in Parkinson’s disease patients. European Journal of Neurology, 14, 300304. http://dx.doi.org/10.1111/j.1468-1331.2006.01647.x Google Scholar
Schuhfried, G. (1992). Vienna reaction unit (manual). Vienna, Austria: Schuhfried Ges.m.b.H.Google Scholar
Signorini, M., & Volpato, C. (2006). Action fluency in Parkinson’s disease: A follow-up study. Movement Disorders, 21, 467472. http://dx.doi.org/10.1002/mds.20718.Google Scholar
Skeel, R. L., Crosson, B., Nadeau, S. E., Algina, J., Bauer, R. M., & Fennell, E. B. (2001). Basal ganglia dysfunction, working memory, and sentence comprehension in patients with Parkinson’s disease. Neuropsychologia, 39, 962971. http://dx.doi.org/10.1016/S0028-3932(01)00026-4 Google Scholar
Stefanova, E. D., Kostic, V. S., Ziropadja, L. J., Ocic, G. G., & Markovic, M. (2001). Declarative memory in early Parkinson’s disease: Serial position learning effects. Journal of Clinical and Experimental Neuropsychology, 23, 581591. http://dx.doi.org/10.1076/jcen.23.5.581.1239 Google Scholar
Tröster, A. I., & Fields, J. A. (2005). Frontal cognitive function and memory in Parkinson’s disease: Toward a distinction between prospective and declarative memory impairments. Behavioral Neurology, 8, 5974. http://dx.doi.org/10.3233/BEN-1995-8201 Google Scholar
Uc, E. Y., Rizzo, M., Anderson, S. W., Qian, S., Rodnitzky, R. L., & Dawson, J. D. (2005). Visual dysfunction in Parkinson disease without dementia. Neurology, 65, 19071913. http://dx.doi.org/10.1212/01.wnl.0000191565.11065.11.Google Scholar
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale (3rd Ed.). Administration and scoring manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale (3rd Ed.). Technical manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Whittington, C. J., Podd, J., & Stewart-Williams, S. (2006). Memory deficits in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 28, 738754. http://dx.doi.org/10.1080/13803390590954236.Google Scholar
Witt, K., Nuhsman, A., & Deuschl, G. (2002). Dissociation of habit-learning in Parkinson’s and cerebellar disease. Journal of cognitive neuroscience, 14, 493499. http://dx.doi.org/10.1162/089892902317362001.Google Scholar