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Attentional Set-Shifting in Parkinson’s Disease Patients with Freezing of Gait-Acquisition and Discrimination Set Learning Deficits at the Background?

Published online by Cambridge University Press:  13 October 2014

Elka Stefanova ,
Milica Ječmenica Lukić ,
Ljubomir Žiropadja ,
Vladana Marković ,
Tanja Stojković ,
Aleksandra Tomić ,
Nataša Dragašević Mišković  and
Vladimir Kostić
Elka Stefanova*
Affiliation:
Faculty of Medicine, University of Belgrade, Belgrade, Serbia Clinic of Neurology, CCS, Belgrade, Serbia
Milica Ječmenica Lukić
Affiliation:
Clinic of Neurology, CCS, Belgrade, Serbia
Ljubomir Žiropadja
Affiliation:
Faculty of Philology, University of Belgrade, Belgrade, Serbia
Vladana Marković
Affiliation:
Clinic of Neurology, CCS, Belgrade, Serbia
Tanja Stojković
Affiliation:
Clinic of Neurology, CCS, Belgrade, Serbia
Aleksandra Tomić
Affiliation:
Clinic of Neurology, CCS, Belgrade, Serbia
Nataša Dragašević Mišković
Affiliation:
Faculty of Medicine, University of Belgrade, Belgrade, Serbia Clinic of Neurology, CCS, Belgrade, Serbia
Vladimir Kostić
Affiliation:
Faculty of Medicine, University of Belgrade, Belgrade, Serbia Clinic of Neurology, CCS, Belgrade, Serbia
*
Correspondence and reprint requests to: Elka Stefanova, Faculty of Medicine University of Belgrade, Clinic of Neurology, CCS, 11000 Belgrade, Serbia. E-mail: [email protected]
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Abstract

Cognitive loading aggravates the freezing of gait (FoG), which is observed in approximately 50% of patients with Parkinson’s disease (PD) in the advanced stages. To investigate whether a specific pattern of executive deficits, that is, attentional set-shifting and/or inhibitory control, are associated with FoG in PD, 30 PD patients with FoG (PD-FoG+) and 36 PD patients without FoG (PD-FoG−) and 22 control healthy subjects were examined with a comprehensive neuropsychological battery. Intra-Extra Dimensional Set shifting Test (IED) and Stop Signal Task (SST), selected from the Cambridge Automated Neuropsychological Battery (CANTAB battery), were administered to analyze set-shifting and motor inhibition, respectively. The IED task was significantly sensitive for differentiating between PD-FoG+ and PD-FoG− groups (p<.01), as well Adenbrook’s clock drawing task (p=.033). By contrast, no differences emerged on any aspect of the SST task and other cognitive tasks. The attrition rate during the IED task showed that the problem in the PD-FoG+ group appeared at the pre-ID level, on the discrimination-learning set; the 32% PD-FoG+ subjects did not achieve the ID level of the task in comparison to negligible 4% of the PD-FoG− patients (p=.011). The logistic regression analysis, indicated the higher the IED stage successfully completed, the less likely presence of FoG in PD subjects. These results demonstrate that the complex cognitive–motor interplay might be responsible for FoG in PD and have had real life implication for the patients. (JINS, 2014, 20, 1–8)

Keywords

CognitionDiscrimination learningAttentionMovement disorderhumansFreezing
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 9 , October 2014 , pp. 929 - 936
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

REFERENCES

Almeida, Q.J., & Lebold, C.A. (2010). Freezing of gait in Parkinson’s disease: A perceptual cause for a motor impairment? Journal of Neurology, Neurosurgery, and Psychiatry, 81, 513–518.Google Scholar
Amboni, M., Barone, P., Picillo, M., Cozzolino, A., Longo, K., Erro, R., & Lavarone, A. (2010). A two-year follow-up study of executive dysfunctions in Parkinsonian patients with freezing of gait at on-state. Movement Disorders, 25(6), 800–802.Google Scholar
Amboni, M., Cozzolino, A., Longo, K., Picillo, M., & Barone, P. (2008). Freezing of gait and executive functions in patients with Parkinson’s disease. Movement Disorders, 23(3), 395–400.CrossRefGoogle ScholarPubMed
Downes, J.J., Roberts, A.C., Sahakian, B.J., Evenden, J.L., Morris, R.G., & Robbins, T.W. (1989). Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson’s disease: Evidence for a specific attentional dysfunction. Neuropsychologia, 27, 1329–1343.Google Scholar
Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2005). The FAB: A frontal assessment battery at bedside. Neurology, 55(11), 1621–1626.CrossRefGoogle Scholar
Elliott, R., McKenna, P.J., Robbins, T.W., & Sahakian, B.J. (1995). Neuropsychological evidence for frontostriatal dysfunction in schizophrenia. Psychological Medicine, 3, 619–630.Google Scholar
Fahn, S., & Elton, R.L. (1987). Unified Parkinson’s Disease Rating Scale. In: S. Fahn, Marsden, C.D., Goldstein, M., & Calne, D.B. (Eds.), Recent developments in Parkinson’s disease II (pp. 153–163). New York: MacMillan.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
Giladi, N., Shabtai, H., Simon, E.S., Biran, S., Tal, J., & Korczyn, A.D. (2000). Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism and Related Disorders, 6(3), 165–170.Google Scholar
Giladi, N., Treves, T.A., Simon, E.S., Shabtai, H., Orlov, Y., Kandinov, B., … Korczyn, A.D. (2001). Freezing of gait in patients with advanced Parkinson’s disease. Journal of Neural Transmission, 108(1), 53–61.CrossRefGoogle ScholarPubMed
Hamilton, M. (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology, 32(1), 50–55.Google Scholar
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23, 56–62.Google Scholar
Hampshire, A., & Owen, A.M. (2006). Fractionating attentional control using event-related fMRI. Cerebral Cortex, 16, 1279–1289.Google Scholar
Heremans, E., Nieuwboer, A., Spildooren, J., Vandenbossche, J., Deroost, N., Soetens, E., … Vercruysse, S. (2013). Cognitive aspects of freezing of gait in Parkinson’s disease: A challenge for rehabilitation. Journal of Neural Transmission, 120, 543–557.Google Scholar
Hoehn, M.M., & Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427–442.Google Scholar
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(3), 181–184.Google Scholar
Jazbec, S., Pantelis, C., Robbins, T., Weickert, T., Weinberger, D.R., & Goldberg, T. (2007). Intra-dimensional/extra dimensional set-shifting performance in schizophrenia: Impact of distractors. Schizophrenia Research, 89, 339–349.Google Scholar
Kehagia, A.A., Barker, R.A., & Robbins, T.W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. Lancet Neurology, 9, 1200–1213.Google Scholar
Kringelbach, M.L. (2005). The human orbitofrontal cortex: Linking reward to hedonic experience. Nature Reviews Neuroscience, 6, 691–702.Google Scholar
Kostić, V.S., Agosta, F., Pievani, M., Stefanova, E., Jecmenica-Lukic, M., Scarale, A., … Filippi, M. (2012). Pattern of brain tissue loss associated with freezing of gait in Parkinson disease. Neurology, 78(6), 409–416.Google Scholar
Lewis, S.J.G., & Barker, R.A. (2009). Understanding the dopaminergic deficits in Parkinson’s disease: Insights into disease heterogeneity. Journal of Clinical Neuroscience, 16, 620–625.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(11), 1078–1085.Google Scholar
Naismith, S.L., Shine, J.M., & Lewis, S.J. (2010). The specific contributions of set-shifting to freezing of gait in Parkinson’s disease. Movement Disorders, 25(8), 1000–1004.Google Scholar
Nantel, J., McDonald, J.C., Tan, S., & Bronte-Stewart, H. (2012). Deficits in visuospatial processing contribute to quantitative measures of freezing of gait in Parkinson’s disease. Neuroscience, 221, 151–156.Google Scholar
Nutt, J.G., Bloem, B.R., Giladi, N., Hallett, M., Horak, F.B., & Nieuwboer, A. (2011). Freezing of gait: Moving forward on a mysterious clinical phenomenon. Lancet Neurology, 10(8), 734–744.Google Scholar
Okuma, Y., & Yanagisawa, N. (2008). The clinical spectrum of freezing of gait in Parkinson’s disease. Movement Disorders, 23(Suppl. 2), S426–S430.Google Scholar
Owen, A.M., Downes, J.J., Sahakian, B.J., Polkey, C.E., & Robbins, T.W. (1990). Planning and spatial working memory after frontal lobe lesions in man. Neuropsychologia, 28, 1021–1034.Google Scholar
Owen, A.M., Roberts, A.C., Polkey, C.E., Sahi, B.J., & Robbins, T.W. (1991). Extra-dimensional versus inter-dimensional set shifting performance following frontal lobe excisions, temporal lobe excision and amygdalo-hyppocampectomy in man. Neuropsychologia, 29, 993–1l06.Google Scholar
Padoa-Schioppa, C., & Assad, J.A. (2006). Neurons in the orbitofrontal cortex encode economic value. Nature, 441, 223–226.Google Scholar
Podsiadlo, D., & Richardson, S. (1991). The timed “Up & Go”: A test of basic functional mobility for frail elderly persons. Journal of American Geriatric Society, 39(2), 142–148.Google Scholar
Robbins, T.W. (2007). Shifting and stopping: Fronto-striatal substrates, neurochemical modulation and clinical implications. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 362, 917–932.Google Scholar
Rolls, E.T. (2004). The functions of the orbitofrontal cortex. Brain and Cognition, 55, 11–29.Google Scholar
Royall, D.R., Mahurin, R.K., & Gray, K.F. (1992). Bedside assessment of executive cognitive impairment: The executive interview. Journal of American Geriatric Society, 40(12), 1221–1226.Google Scholar
Shine, J.M., Naismith, S.L., Palavra, N.C., Lewis, S.J.G., Moore, S.T., Dilda, V., & Morris, T.R. (2013). Attentional set-shifting deficits correlate with the severity of freezing of gait in Parkinson’s disease. Parkinsonism and Related Disorders, 19, 388–390.Google Scholar
Shine, J.M., Moustafa, A.A., Matar, E., Frank, M.J., & Lewis, S.J.G. (2013). The role of fronto-striatal impairment in freezing of gait in Parkinson’s disease. Frontiers in System Neuroscience, 7, 61.Google Scholar
Shine, J.M., Naismith, S.L., & Lewis, S.J.G. (2013). The differential yet concurrent contribution of motor, cognitive and affective disturbance to freezing of gait in Parkinson’s disease. Clinical Neurology and Neurosurgery, 115, 542–545.Google Scholar
Tessitore, A., Amboni, M., Cirillo, M., Corbo, D., Picillo, M., Russo, A., … Tedeschi, G. (2012). Regional gray matter atrophy in patients with Parkinson’s disease and freezing of gait. AJNR American Journal of Neuroradiology, 33, 1804–1809.Google Scholar
Tessitore, A., Amboni, M., Esposito, F., Russo, A., Picillo, M., Marcuccio, L., … Barone, P. (2012). Resting-state brain connectivity in patients with Parkinson’s disease and freezing of gait. Parkinsonism and Related Disorders, 18(6), 781–787.Google Scholar
Vandenbossche, J., Deroost, N., Soetens, E., Spildooren, J., Vercruysse, S., Nieuwboer, A., & Kerckhofs, E. (2011). Freezing of gait in Parkinson disease is associated with impaired conflict resolution. Neurorehabilitation and Neural Repair, 25(8), 765–773.Google Scholar